The Euglenoid Flagellates

Transcription

THE EUGLENOID FLAGELLATES
P
BY THEODORE LOUIS JAHN
StateUniversity
ofIowa
ZoologicalLaboratories,
ROBABLY no otherorderof free-living Euglenoidsare foundmostabundantlyin small
freshwater
pools rich in organicmatter. This is
especiallytrueof the generaEuglena,Phacus,and
Tracleloamonas
whichare oftenfoundin sufficient
quantitiesto colorthe water(greenor red forEuglena,green for Phacus, and yellow-brownfor
Traccelomonas),especially if the temperatureis
above 25?C. (e.g.,Senior-White,
1928;Sands,1934;
earlierliteraturecited by Naumann, 1922). Euglenoidsare sometimesthe dominantformson the
surfaceof thick bottom deposits of ponds, especiallyiftheorganiccontentis high(Lund, 1942).
The euglenoidsare sometimesstatedto be indicatorsofsewagepollution. However,Lackeyand
Smith(1940) have pointedout that manyspecies
are abundant wherepollutionis absent. When
euglenoidsare foundin pollutedstreamsthemaximumnumberis manymilesdownstream
fromthe
peak of sewagepollution,in the regionwherethe
wateris becomingclarifiedbut is stillhighin dissolvedorganicmatter. The generaEuglena,Phacus, and Trachelomonas
are very commonin the
sewage polluted Scioto River below Cincinnati,
Ohio (Lackey,1939a),butnotin thepollutedDuck
THE ORDER EUGLENIDA
and Cumberlandriversbelow Columbia (Tenn.)
The euglenoidsconsistof both greenand color- and Nashville (Tenn.), respectively(Lackey and
less flagellates,usually with one or two flagella Smith,1940). The presenceof largenumbersof
whicharise fromthe invaginatedanteriorregion euglenoidsis evidenceof a highdissolvedorganic
when contentbut not necessarilyof its sewage origin.
ofthecellknownas thegullet. Chloroplasts
wastes
presentare almostpuregreen,and all chlorophyll- Many euglenoidsare tolerantof distillery
bearingspecies possess a red stigma. Metaplas- (Lackey,1942).
SomespeciesofEuglenainhabitdampmudalong
micreservematerialsconsistofparamylum.
the banks of rivers,estuaries,and salt marshes
OCCURRENCE: CONDITIONS WHICH AFFECT GROWTH
wherethey may color the mud over wide areas,
Factors whichcontrolthe occurrenceof eugle- and theappearanceofthecolorsometimesshowsa
noidsare,in general,thesamefactorswhichcontrol perbdicityrelatedto the tidesand lightintensity
growthof the organisms. Therefore,a thorough (Bracher,1919, 1929; Gard, 1922; Fraser, 1932;
oftheirecologyinvolvesa thorough Carter,1933). The ecologicaldistribution
understanding
ofvaritheir ous species of Euglena is discussedby Gunther
oftheirphysiology,especiallyof
understanding
nutritionand of the effectsof teinperature,
pH, (1928),andthetypesofhabitat(catharobic,oligo-,
and oxygen concentrationupon them. The re- meso-,or polysaprobic)formanyspeciesare listed
lationshipsof thesefactorsare discussedby Jahn by Fairand Whipple(1927).
(1934) and Lackey (1938b).
Certainspeciesof Euglena (e.g., E. gracilis)are
Protista has received such widespread
attention as the Euglenida. This is
largelytheresultoftheuniquetaxonomic
position of the order. The obvious
plant-like characteristicsof some genera (e.g.
Euglena) and the obviousanimal-likecharacteristics of others (e.g., Peranema) require that the
euglenoid flagellates be considered by both
botanistsand zoologists. The absenceofanyclear
line of demarcationbetweengreenand colorless
formsmakes it seem inadvisableto assortthe organismsamongtheplantand animalkingdomsand
therebyseparate,on the basis of obviouslyarbitrarycriteria,the membersof a closelyrelatedalgroup.
heterogeneous
thoughsuperficially
The purposeofthepresentpaperis to discussthe
generalbiologyoftheeuglenoidsand to citeenough
so that
to thewidelyscatteredliterature
references
mayeasilybe found.
availabledetailedinformation
The most usefulgeneraltreatmentsof the group
are those of Smith (1933), Dangeard (1933),
Fritsch(1935), and Kudo (1946).
246
This content downloaded from 140.203.12.4 on Thu, 18 Dec 2014 09:42:44 AM
All use subject to JSTOR Terms and Conditions
THE EUCLENOID FLAGELLATES
247
able to growover a verywide pH range (Jahn, in numberof flagellamay be consideredas adapta1931; Alexander,1931) whileothers(E. desesand tionsto the endozoicmode of life.
Numerous genera have been reported from
E. anabaena)are able to growonlywithina very
restrictedpH range (Dusi, 1930; Hall, 1933a). brackish water (Euglenca,Wermel, 1924b; van
Euglenamutabilisis the mostcommonorganismin Goor,1925,Schiller,1925,Biecheler,1937,Carter,
coal mine pits (pH 1.8-3.9, Lackey, 1937; Eutreptia,Steuer, 1904, van Goor, 1925,
water-filled
1938a, 1939b) and exhibitsmaximalgrowthonly Schiller,1925; Tracckelomnonas,
Phacus, and Khawvan Goor, 1925) and fromsalt water (Euw
in an acid medium(von Dach, 1943). Lepocirclis kineea,
ovunhas also been observedin largenumbersin a glena, Schiller,1925, Lackey, 1936; Heteronema,
minepit at a pH 2.5 (Lackey, 1939b). Wermel Lemmermann,1906, Kahl, 1928, Lackey, 1936;
(1924a) has describedseveraleuglenoidsfromacid Lepocinclis, Phacus, Colaciurm,Lemmermann,
(pH 2 to 4) peat bogs. Astasiasp. and Khawkinea 1906;Astasia,Traclelomonas,
Eutreptia,Euglenophalligrowmostrapidlyin an almost neutralme- sis, Urceolus,Peranema,Petalomonas,Tropidoscydium (Schoenbom,1936),but K. halli also grows phus,Distigma,Notosolenus,
Anisonema,Dinema,
Lackey, 1936). Euglena has also been reported
welloverthepH range4.0 to 8.0 (Elliott,1938).
Cystsof Euglena have been reportedfromtree fromthe Great Salt Lake (Jones, 1944). The
bark,(Briscoe,1939)and moistor driedsoil (many genera Ploeotia, Eutreptiella,Chloranima,Chlore.g.,Gunther,1928;Johnson,1944).
acisne,
Klebsiella,Triangulomonas,
observers,
Peranemopsis
and
The saprophyticcolorlessspecies are seldom Clautriaviahave apparentlybeen describedonly
foundin largenumbers,but theygrowbest when fromsalt or brackishwater(Walton,1915;Schiller,
is present 1925; Pascher,1931; Lackey, 1940a).
a considerableamountof putrefaction
(e.g., Scioto River, Lackey, 1938a). Pringsheim The occurrehceofthesame speciesin bothfresh
(1942 and earlier)has beenverysuccessfulin cul- and salt waternaturallyleads to the questionof
turingthemin speciespure culturesin tubescon- adaptability to high osmotic pressures. Finley
E.
taininggardensoil, CaCO,, and a suitableorganic (1930) foundthat Euglenaoxyuris,E. terricola,
can be acclimatedto
material such as starch. Peranema and other sp., and Phacus pleuronectes
holozoiceuglenoids,of course,requirethepresence fullstrengthsea water,Entosiphonto 40 per cent,
and two endozoicspecies of Khawkineato 80 per
of particulatefood (diatoms,algae, debris).
thetolerancesvaryfrom
Sessilespeciesgrowuponalgae,plantdebris,and cent. For directtransfer
smallcrustaceans. One speciesofEuglenamaybe 5 to 40 per cent for the same species. Loefer
attached to Volvoxcolonies. There are a few (1939) foundthat Astasia remainsviable in 100
oligochaetes, per centsea water,but that motilityis lost above
euglenoidswhichlive in flatworms,
rotifers,nematodes,amphibcopepods,gastrotrichs,
40 per cent. He also foundthat Euglenagracilis
ians,and theeggs of nudibranchmolluscs(litera- lives and growsonly in concentrations
below 40
ture, Kirby, 1941a). The endozoic species are per cent. Loeferfound that the euglenoids(in
usuallyconsideredto be distinctfromthosewhich contrastto ciliates and other flagellates)do not
and Jandaand Jirovec(1937) were exhibita gradualadaptationto higherconcentraare free-living,
not able to infectmolluscs,crustaceans,or insects tionsbutare almostas resistanton thefirsttransfer
witha colorlessstrainofEuglenagracilis.
as on the thirteenth
(twomonthsor morelater).
and Hegneria)have
Two genera(Euglenamorpha
Almostall euglenoidgenerahave been reported
been found only in the intestinesof amphibia,
soil samples (Sandon, 1927; Singh, 1941)
Wenrich, from
usuallyfrogor toad tadpoles (literature,
and
Lackey
(1940b)has identified
forty-two
species
1935; Kirby, 1941a). Thereare two varieties(or
from
tree
to
fifteen
belonging
holes.
genera
one greenwith three
species) of Euglenamorpha,
Few studiesof the directeffectof temperature
flagellaand a stigma,and the othercolorlesswich
on
growthhave been made. Jahn (1935) found
The
colorless
no
and
stigma.
two to six flagella
of Euglenagracilis
organismswith the more numerousflagellamay that the optimumtemperature
in
a
in
is 10?C.and that
peptone
medium
darkness
be divisionstages. However,Hegneria,whichis
an
of
division
increasing
percentage
cystsoccurs
very similarto the colorlessspecies of Euglenaabove
When
is
sodium
15?C.
acetate
present,the
has
seven
flagella,
six)
(sometimes
usually
mnorpha,
is 23?C.,a pointapproaching
stages or chlorophyll-bearingoptimaltemperature
and no triflagellate
speciesare known. Wenrichhas pointedout that the optimumin the light. The resistanceto high
varieswithpH. E. gracilisis killed
and the increase temperatures
the loss ofstigmaand chlorophyll
248
THE QUARTERLYREVIEW OF BIOLOGY
twiceas rapidlyby exposureto 40?C. whenthepH
is 5.0 as whenit is 4.0 or 8.0 (Jahn,1933a).
Verylittleis knownabout the oxygenrequirementsof euglenoids. Lackey (1932) foundthat a
numberof genera (Distigma,Entosiphon,Euglena
gracilis, Heteronema,Rhabdomonas,Peranema,
and Petalomonas)werepresentunder
Notosolenus,
anaerobicconditionsin sewagedigestiontanksbut
onlyin smallnumbers.
Von Dach (1940) foundthatAstasiagrewalmost
as well undersemi-anaerobicconditionsas at atmosphericoxygentension,in spiteofthe factthat
theorganismmay consumeconsiderablequantities
of oxygen (Von Dach, 1942). Lindeman (1942)
acus, H. sp.,
foundthat Euglenadeses,Heteronemca
survivedanaeroand Trachelomonas
Phacuspyrum,
bic conditionsfor30 days at 0-5?C., but at 10?C.
only Heteronemaacus survived. The occurrence
ofanaerobiosisis discussedbyvon Brand (1944).
Apparentlyno quantitativestudiesof the effect
of visiblelighthave been made, but the growthof
species is obviouslyenmost chlorophyll-bearing
hanced by illumination. Swann and del Rosario
(1931, 1932) studiedthe toxiceffectsof ultraviolet
irradiationand of alpha particles. The toxic
actionofcertaindyesand the counphotodynamic
ter effectof Germanin(Bayer 205) against the
photodynamiceffectand also against ultraviolet
radiationhave been describedby Jirovec(1934a)
and Jlrovecand Vacha (1934a, 1934b).
Fossil euglenoidsare apparentlyrare. However,Bradley(1929) reportedPhacus caudatafrom
a gelatinouscompactedlithifiedlacustrineooze.
The name "Trachelomonas"
has been erroneously
whichhave a siliapplied to fossilChrysomonads
ceousskeleton(Deflandre,1934a; 1935).
CELL EXTERIOR
into a
The exteriorof the cell is differentiated
periplastor pellicle,whichmay be rigid,so that
the cell has a fixedshape (e.g., Phacus, Rhabdomonas,Menoidium);or may be quite flexible,so
that the shape may change considerablyduring
"metabolic movements" (e.g., Euglena gracilis,
E. deses,Distigmaproteus);or maybe onlyslightly
flexible,so that metabolicmovementsare minimized (e.g., E. trisulcata,E. tripteris). In some
speciesthepellicleis smoothor veryfinelystriated
(e.g., Astasia torta,Distigmasennii),and in others
it is longitudinallyor spirally striated (e.g.,
Phacus),or withspiralridges(e.g.,Phacus pyrum),
arrangedpunctae
or withspirallyor longitudinally
whichmaybe simple(e.g.,Euglenaspirogyra,
Pkacus monilata)or complex in structure(e.g., E.
fusca, Lefevre,1934). In Euglena rubra,but not
in most other species of Euglena, the pellicle is
separated fromthe protoplastby Noland's flxative (Johnson,1942).
and P.
In somespeciesofPhacus (P. pleuronectes
longicaudabut not P. caudatavar. polonica,or P.
pusilla) there is, in addition to the longitudinal
striaea numberof closelyspaced crossstriations.
These striationsofPhacus,as wellas othersurface
Euglena,Entosiphon
sculpturingof Rhabdomonas,
and Anisonemahave been describedby Jfrovec
(1929) and Klein (1930) as a "silverline"system.
The identityof the silverlinesystemand the surface sculpturinghas been pointed out by Hall
(1931) and Deflandre(1931). The surfacesculpturingis widelyused as a specifictoxonomiccharacter (discussion,Swirenko,1927; Lefevre,1931).
However, it has been demonstratedby Lefevre
(1932a, 1932b,1932c)thatwhenEuglenaspirogyra
is maintainedin culturethe pellicularornamentationsmay decreaseand eventuallydisappear. It
seemspossiblethatthistendencyforvariationwith
the conditionsof culturemay accountforsomeof
thenumerousdescribedvarietiesofcertainspecies.
Some species of Euglena lack a flagellumand
move in an amoeboid manner(discussion,Elenkind, 1924a, 1924b). Pascher (1930) considered
and a stigma
a colorlessamoeba withzoochlorellae
to be a euglenoid. Valkanov (1934) tentatively
assignedanotheramoeba to the genusEuglena.
In fourgenera (Tracielomonas,Stromnbomonas,
Ascoglena,Klebsiella)the cell is sorroundedby a
lorica,withan openingat one end fromwhichthe
Stromboflagellumprotrudes. In Trachelomonas,
monas,and Klebsiellatheloricais carriedabout; in
Ascoglenait is attached to the substrate. The
lorica is composedof a firmgelatinousor a rigid
material,withno traceof cellulose(Klebs, 1883).
The shape of the lorica is used forseparatingthe
species,but theexactshape
generaand identifying
may differconsiderablywithinthe species (Deflandre,1926-27; Gordienko,1929). When first
formedtheloricais verypale in colorbut laterit
becomesa dark brown.
In somespecies (e.g.,Euglenaterricola,
Gunther,
1928; Klebsiella,Pascher,1931) the posteriorportion of the cell secretesa substance(throughfine
pores) whichservesto attachthe organismto substrateor lorica.
249
vacuoleis replacedbya newvacuoleformedby the
At the anteriorend of the euglenoidcell is the fusionof severalsmallervacuoles. The morpholcytostomewhich opens intoa flask-shaped
gullet ogy of the vacuole in a numberof euglenoidshas
consisting
ofa narrowtube,the cytopharynx,
and been describedby Haye (1930) and Chadefaud
(1937). Hyman (1937, 1938> has describedthe
formation
ofthevacuolein Euglena,Phacus,Entosiphon,and Peranema (Fig. 2) and has clearly
demonstrated
that fusionof small vacuolesoccurs
(cf. Haye, 1930). The formationof the large
vacuole by fusionof smallervesiclesis apparently
of generaloccurrenceamongthe Protozoa (King,
GULLET, RESERVOIR, AND CONTRACTILE VACUOLE
Entoiphoen
Euglenr
K.
a.
Peranema
4.
Phacus
FIG. 1. EuGLENA AND HETERONEMA
FIG. 2. BEJIAvIOR Or CONTRACTmLE
VACUOLE
1-2. MotilestageofEuglenarubrashowing
structures In all fourspeciesshownthesmallvacuolesfuseto
visiblein a livingorganism.Organism
1 wasinshade, forma largevacuolewhichemptiesbyfusionwiththe
and hematochrome
is centrally
located. Organism
2 reservoir.(AfterHyman,1938).
was in brightsunlightand hematochrome
is located
peripherally.
Abbreviations:
fg,flagellum;
gu, gullet
re,reservoir;
(cytopharynx);
st,stigma;cv,contractile 1935;Weatherby,1941). Klebs (1883) foundthat
vacuole; cp, chloroplast;
pb, paramylum
body; nu, the maximumrate of contractionin Euglenadeses
nucleus;hc,hematochrome.
(After
Johnson,
1939).
3-5. Heteronema,
anteriorend,showinggulletand and E. ehrenbergi(one contractionevery 22
rodapparatus. 3. As seenfromleftside. seconds) occurredat 32?C. but that the vacuole
pharyngeal
Regionsof organismindicatedas follows:d, dorsal; continuedto contractas the temperture was
v, ventral;r, right;1,left. 4. Reconstruction
of3 as
wouldbe seenfrom
anterior
end. Thecircleabovethe raised,up to 500C.
ofthegullet;
rodapparatus
pharyngeal
is a crosssection
Accordingto Gatenby, Singh, and Browne
flagellaareindicatedby twodots. 5. Reconstruction(1938) the reservoirpulsates and is part of the
of 3 as would,beseen fromthe dorsalside. (After
vacuolarsystemand may at timesbe closedto the
Loefer,1931).
outside. This is an idea expressedby Klebs (1883)
an enlargedposteriorportion,thereservoir(Fig. 1, and one whichhas receivedalmostno otherrecog1). Usuallylateral but sometimesposterior(As- nitionsince the classicalpaper by Wager (1899),
tasia linealis,Pringsheim,1942) to the reservoir in whichhe statedthatthereservoir
is permanently
thereis a contractile
vacuole(twoin Piacus, Haye, open to theexterior.
1930) whichemptiesinto the reservoirby fusion
It is this Klebsian conceptof the reservoiras a
and obliterationof the separatingwalls. This primaryvacuole (the real vacuole being called
250
secondary)thatis denotedby the characterization thiscystostome
is separatefromtheopeningofthe
"vacuolesystemcomplex"in someoftheliterature gullet. Rhodes (1926) made a similarstatement
proof about Heteronema.However, it was definitely
on theeuglenoids. In theabsenceofdefinite
it seemsbestnotto revivethisconcept,but to con- demonstratedby Hall (1933b) that in Peranerna
sider the reservoirto be permanentlyconnected foodis ingestedthroughthe gulletand that food
to the outside and not to referto it as the vacuoles are formedin the posteriorend of the
reservoir. Accordingto Hall and Powell (1928),
"primary"vacuole.
natureofthe reser- Hall (1933b), and Hyman (1936), the functionof
In supportofthe contractile
voir,Gatenby,Singh,and Browne(1938) cite the the rodsis to supportthelip ofthe cytostomedurpresenceof a peri-oral(or perivestibular)ringof ing ingestion. Ivanic (1935) describedpseudopoosmiophilicmaterialwhichis supposedto act as a dial feedingof Peranemaon diatomswhichwere
sphincter. This materialhas been seen by other larger than the flagellate. In Entosiphonthe
(Euglena,Hamberger,1911,Gunther, pharyngealapparatus (siphon) is well developed
investigators
1928; Phacus,Haye, 1930),but its functionis un- and slightlyprotrusible. However,accordingto
Lackey (1929a) the organism is saprozoic (cf.
known.
Schiller(1925) has assignedtwogreenflagellates Lemmerman,1913). On the other hand, Scytowithouta gullet (Chloranimaand Chlorachne)to monasand Euglenopsisare holozoicbut possessno
rods.
thefamilyEuglenidae.
PHARYNGEAL ROD APPARATUS; INGESTION
The pharyngealrod appratusoccursin the Peranemidaebut not in the otherfamilies. In Peranema(Halland Powell,1927;1928;Hyman,1936)
(Loefer,1931) the apparatusconand Heteronema
sists of two parapharyngealrods which are
apparentlyattachedto each otherand sometimes
to a shortcurvedtrichitewhichlies near
anteriorly
the cytostome(Fig. 1, 3-5). In Urceolusthe anteriorend of the rod apparatusdoes not reachthe
2.
cytostome(openingofgullet),and thereis a sepaoF FLAGELLA
FIG.
3.
STRUCTURE
AND
ACTION
rate indentationofthepellicleas far back as the
of
1-3.
Structure
stichonematic
flagellum
ofPhacus
anteriorend of the rod. In Entosiphonthe rod pleuronectes,
Astasia dangeardii,and Rhabdomonas
a
apparatusconsistsofa tube (oftencalled siphon) incurvum,
respectively.Nigrosinpreparations.The
of Phacus is shownin 1
whichis as longas the animaland possessesthree finersurfacesculpturing
(1-3afterDeflandre,
1934c).
longitudinal thickenings(Lackey, 1929a). In
Anisonemathe siphonis presentbut ratherinconFLAGELLA; MOVEMENT
spicuous. In Dinema (Walton, 1915) and PerThe flagellaare insertedinto the base of the
anemopsis(Lackey, 1940a) the rodsare similarto
thoseof Peranema. Accordingto Brown(1930a), reservoirand project throughthe cytopharynx.
rods are also presentin Petalomonas,Tropidoscy- In all generacarefullyinvestigated(Distigma,Asand Scytomonas.In Pe- tasia,Phacus,Euglena,Lepocinclis,Trachelomonas,
phus, Marsupiogaster,
the flagellumconsistsof
talomonasthe rodsare supposedto be quite short Urceolus,Rhabdomonas)
axonemesurrounded
by a sheath
to recognize. Rods a typicalflagellar
and apparentlyare difficult
have not beendescribedforothergenera. During to whichare attacheda numberof diagonallyar(Fischer,1894;Mainx, 1928;
divisionthe rod apparatus degenerates,and two rangedmastigonemes
new sets are formedin the daughtercells (Hetero- Petersen, 1929; Deflandre, 1934c, 1934d; Vlk,
nema,Loefer,1931;Peranema,Brown,1930a;Ento- 1938)as shownin Fig. 3, 1-3. In someeuglenoids
theseare noteasilydemonstrated
(cf.Mainx, 1928;
siphon,Lackey,1929a).
The pharyngealrods are usually assumed to Deflandre,1934a), but the claims of Dellinger
functionin theingestionoffood. In Peranema,at (1909) and of Korschikow(1923) that they are
least, there is evidence for this assumption. artifacts are now disregarded. These mastiBrown(1930a) statedthat in Peranemathereis a gonemesmay be observedaftermordantstaining
or in the
at theanteriorend oftherodsand that methods,in driednigrosinpreparations,
cystostome
X@51S~~~
251
whentakento indicate
livingcell witha dark-fieldmicroscope. In Eu- "tractellum"is a misnomer
are 3.0 to 3.5 Mlong anythingexceptthelocationoftheflagellum. Remastigonemes
glenagracilisthe
and spaced 1.0 to 1.5 u apart. On thebasis ofthe cent workon flagellarmovementis discussedby
thetypeofflagel- Barker(1943).
ofthemastigonemes
distribution
to as
Gunther(1928) showedthatthe rateof locomolum possessedby the euglenoidsis referred
condiDeflan- tionin six speciesofEuglenaunderuniform
"stichonematic"("flagellestichonemate,"
dre, 1934c; "eensidig Fjersvingtraad,"Petersen, tionsvarieswiththe ratioof the flagellarto body
Vlk, length. The rate varieswiththe speciesbetween
1929; "Einseitswendigeor Flimmergeissel,"
1938) or "ciliary"(Kudo, 1939). The functionof 0.02 and 0.22 mm/sec. The species of Trachelomonaswhichhave flagellamany times the body
is apparentlyunknown.
mastigonemes
One outstandingand probablythe most char- lengthmovemuchmorerapidlythanmanyspecies
acteristicthingabout Peranemais the behaviorof of Euglenain spiteof the dragof the lorica. Sev1904;Mast and
(Jennings,
the swimmingflagellumwhichis held in frontof eral otherinvestigators
is Gover,1922;Deflandre,1929;and Lefevre,1932c)
the cell. This forwardpositionof the flagellum
responsiblefor the glidingmotion (withoutcell have describedthe path and velocityof Phacus
of severalgenera and Euglena.
rotation)whichis characteristic
The typeof insertionof the flagellumwas proofthePeranemidaeand also ofthegeneraDistigma
and Sphenomonasof the familyAstasiidae. In posed by R. P. Hall and Jahn(1929a) as an addithe familyEusome genera one flagellumis trailingand ap- tional criterionfordistinguishing
parentlybeatsonlynearthetip,therebyproducing glenidaefromthe otherfamiliesof the order,and
this subject has received considerableattention
a similarglidingor creepingeffect.
High speed motionpicturesof the flagellaof fromotherinvestigators.
Euglena,Phacus,Peranema,Astasia,Rhabdomonas, In all membersofthegreengeneraofEuglenidae
and Distigmahave been takenby Lowndes (1941, whichhave been examinedthe flagellumis bifur1944). In all species studied he foundthat the cated at the base and bears a flagellarswelling
wave like motionbeginsat the base of the flagel- eitherat or slightlyposteriorto thepointofbifurlum, progressestowardthe tip, and has its main cation (Fig. 4, 1-4). In all of the colorlessflagelcomponentof forcedirectedaway fromthe tip. lates examinedby Hall and Jahn(1929a, Astasia,
Peranema,Euglenopsis)the flagelIn Euglena viridisthe flagellumpushes obliquely Rhabdomonas,
and withouta
backward therebyproducingrotation,gyration, lumwas foundto be non-bifurcated
and a forwardcomponent,all of whichcontribute flagellarswelling(Fig. 4, 5-8). It was suggested
speciesof
of the stigma-bearing
to forwardmovement. In regardto the position that the flagellum
of the flagellumduringgyrationthe figuresof Astasiashouldbe examinedand thattheorganisms
Lowndes(1944) are not in agreementwiththoseof should be placed in the familyEuglenidaeif the
flagellum
werebifurcated. A bifurcated
flagellum
Jennings(1906).
its characteristic with a swellingwas found in a stigma-bearing
WhenPeranemais undergoing
is colorlessflagellateby S. R. Hall (1931), and he
glidingmotionthedistalportionoftheflagellum
also directedobliquelybackward,and the wave is placed this organism in the genus Euglena.
colorlessorganismwas
acceleratedas it movesfromthebase. The power Anotherstigma-bearing,
for forwardmovementcomes fromthe rapidly describedbyJahnand McKibben(1937),and these
createdthe genus Khawkineawhich
movingwave near the tip. Lowndesis skeptical investigators
from
differs
onlyin the absenceof chlorobe
Euglena
of
Peranema
to
of
of the ability the flagellum
the chiefmechanismof locomotionunder these plasts.
In vegetativestages of the biflagellategenus
conditions,but he offersno alternative. When
Peranemais not gliding,actionof the flagellumis Eutreptia (Steuer, 1904) and the triflagellate
the same as in othereuglenoids. Lowndes (1944) Euglenamorphahegneri (Wenrich, 1924), each
thereis probablyno flagellumbears a swellingbut is not bifurcated.
foundthat in Rhabdomonas
and Euglenamorphapellucidais a possible exception
forwardcomponentin the flagellarmovement,
he concludesthatpropulsionis merelytheresultof whichhas beendiscussedbyHall and Jahn(1929a).
Apparentlythere has never been any serious
rotationand gyration.
withthethesisthatall monoflagellate
Sincethepowerofthe strokein all oftheeugle- disagreement
noids studied (and probablyin all flagellates)is membersof the familyEuglenidaehave a bifuralwaysin thedirectionaway fromthetip,theterm cated flagellumwitha flagellarswellingand that
252
the stigma-bearing
colorlessflagellatesbelong in
this family. (Colaciumis in a separatefamily.)
However,in regardto the flagellum
ofthe colorless flagellatesthere has been considerabledis-
movement. This was corroboratedby Hall
(1934), who pointedout that Hartmannand Chagas (1910) and Korschikow(1924) had previously
described the second flagellum. At presentall
workersagreethattheflagellaofPeranemaare not
bifurcatedand bear no flagellarswellings. The
second flagellumcan be caused to separatefrom
the pellicle in the living flagellateby the use
ofweakgentianvioletsolutions(Korschikow,1929,
see Hall, 1934; Dunham, 1937), and Chadefaud
(1938) has noteda separationwithbichromate
fixatives.
Lackey (1934a) stated, in contradiction
to all
previousinvestigators,
that the flagellumof Astasia is bifurcated. Lackey also pointedout that
such a bifurcation
permitsone to sketcha phylogeneticseriesin whicha hypothetical
formwitha
singleflagellum
and flagellarswellingbut no bifurcationgave riseto two bifurcated
types,one with
(Euglena) and one without(Astasia) a swelling
(Fig. 4, 9). The bifurcatedflagellumin the organism without the swelling eventually split
itslengthand gave riseto the biflagelthroughout
late organisms(Peranema,Heteronema,
Distigma)
whichhave neitherbifurcation
nor flagellarswellings. It now seems apparentthat the structure
of Colaciumcorrespondsto the hypotheticalancestralform(D. F. Johnson,1934). Eutreptiaand
could be derivedfromthe hypoEuglenamorpha
theticalancestralformmerelyby an increasein
OF EUGLENODS
INsERTION
FIG. 4. FLAGELLUM
(1-4),Astasia(5-8),andpossiblephylogeny thenumberof flagella. Smyth(1943) publisheda
Euiglena
(9). 1, Euglena,vegetative
stageshowingbifurcated figureof Astasia karrisiiwithflagellarbifurcation
withflagellar
therhizoplast
flagellum
extendswelling,
ingfrom
oneoftheblepharoplasts
toa granule("extra- and swellingbut did not commenton theproblem.
on the nuclearmembrane. 2,
nuclearcentrosome")
In all of the euglenoidsstudiedthereis a basal
Late prophaseor metaphase,with two bifurcated
the blepharoplastor mastigosome,
granule,
at the
flagellabut no flagellarswellings.3, Anaphase.
or ofeach ramusofa flagel4, Telophase. 5,Astasia,vegetative
stageshowing
non- base ofeach flagellum
bifurcated
flagellumwithoutflagellarswelling,and lum. In themonoflagellate
Euglenidaeone ofthe
to centrosome
on nuclearmemrhizoplast
extending
and
in
the
the sole bleAstasiidae
blepharoplasts,
brane. 6, Late prophase. 7, Anaphase. 8, Telophase. 9, Phylogeneticdevelopmentof flagellum pharoplast,is connectedto an extranuclearceninsertion
according
to Lackey(1934a).
a. Hypotheticalancestorwith swellingbut no trioleby means of a rhizoplast,as shownin Fig.
a condition
latershownbyJohnson
bifurcation,
(1934) 4, 1-5 (Hall, 1923; Hall and Jahn, 1929a). In
to existin Colacium.b. Conditionin Euglena(1, Peranemathe extranuclearcentrioleis connected
to Lackey,
in Astasiaaccording
above). c. Condition
in Peranema
butnotas in 5 above. d. Condition
and by a rhizoplastto one of the blepharoplasts(Hall,
Ieteronerna
(see also Fig. 1, 3-5, and Fig. 6, 9-15). 1934). In Euglena sanguinea Haase (1910) re(1-8 afterHall andJahn,1929a).
portedthatthetworamiare continuedthroughthe
cussion. Brown (1930a) stated (in contradiction cytoplasmto a regionposteriorto the nucleus,but
(Gojdics,1939).
to Hall and Powell, 2928, and others) that the thisreporthas notbeen confirmed
The mechanicsof "metabolic" or "euglenoid
flagellumof Peranema is bifurcated. Lackey
(1933) discoveredthat the extra ramus described movementhave not been studied. These moveby Brownis reallythe base of a second flagellum mentsare most pronouncedin Distigmabut also
which lies close to the pellide duringordinary occurin mostnon-rigid
species.
&(
253
chlor-iodide,
is insolublein boilingwater,may be
hydrolyzedto glucose,dissolvesin concentrated
The chloroplastsof the euglenoidsappear to
sulfuricacid and potassiumhydroxide,
sometimes
but extractsof
containalmost pure chlorophyll,
dissolvesin formalin,and swells in weak (6 per
the whole cell contain carotenoids. Absorption cent) potassiumhydroxideto displaya concentric
spectraare very similarto those of greenplants
stratification
(Molisch, 1923; Czurda, 1928; De(Baas-Beckingand Ross, 1926; Gunther,1928).
flandre,1934b; Fritsch, 1935). This concentric
The chloroplastsvary greatlyin size, shape, and
stratification
may oftenbe seen witha polarizing
species,and these differences microscopewithoutthe
numberin different
use of hydroxide.
usedas specificcharacters,
especially
are sometimes
When viewed under crossedNicol prisms,the
in the genus Euglena (discussion,Lefevre,1931). paramylumbodies of
most species are definitely
If Euglena is grownin darknessthe amount of
anisotropic. Most speciesof Phacus and some of
and the numberof chloroplastsis rechlorophyll
Euglena show fourradial lightand dark sections
duced (Zumstein,1900; Ternetz, 1912; Mainx, in
each paramylumbody. In othergreenspecies
1928),even to the pointof extinction(Lwoffand
and in Astasia the sectorsare less pronounced,
alwaysarisefrom
Dusi, 1935). Since chloroplasts
and in Rkabdomonas,
Distigma,Petalomonas,
Anipre-existingchloroplasts,loss of all chloroplasts
sonema,and Entosiphon
the bodiesare apparently
may resultin the beginningof a colorlessstrain.
isotropic. These variations in anisotropy are
A list of the colorlessstrainsof normallychlorocaused partlyby visibledifferences
in size, shape,
phyll-bearingspecies is given by Pringsheim
and positionof the bodies but probablyalso by
of greenand colorless
(1937), and the relationship
differences
in the ultramicroscopic
or molecular
(1941) and Kirby
formsis discussedby Pringsheim
structure(Deflandre,1934b).
(1941a).
Paramylumbodies assume a varietyof shapes
possessa pyreIn somespeciesthe chloroplasts
(flatdiscs,concavo-convex
discs,rods,rings,etc.).
noid whichconsistsof hemisphericalprojections
The shape and size undoubtedlyundergo condiscs of
fromeithersurface. Watch-glass-shaped
ofthe
siderablevariationwiththestateofnutrition
paramylummaybe formedon one or bothsurfaces
cell (discussion,Lefevre, 1931), but the larger
of the pyrenoid. Later the paramylummay becharacteristically
shaped bodies seem to possessa
comedetached(Mainx, 1928),and a newsheathis
remarkabledegreeof persistenceand are used for
(Mainx, 1926) the pyreformed. In E. m-ucifera
ofspecies. Developmentofthe
thedifferentiation
noids are on special shortprocesseson the inner
more complexshapes has been discussedby Butsurface of the chloroplast. The pyrenoidsare
schli (1906), Czurda (1928), and Heidt (1937).
viscousmassesofprotein,usuallyarise by division
The ring shaped paramylumbodies of Euglena
of pre-existing
pyrenoids,and when presentare
sanguineaare formedfirstas a cup, and thenthe
apparentlyresponsibleforthe formationof paracentermaybe dissolved(Heidt,1937).
mylum. The pyrenoidsof the Euglenidaare differentin structurefromthose of the ChlorophySTIGMA
ceae (Czurda,1928).
The stigma is composed of numerous red
Formationofparamylumis not limitedto pyrenoidsand inmostspeciesit is notformedin contact granulesembeddedin a colorlessconcavo-convex
with the chloroplasts(e.g., Phacus, Lepocinclis, matrix(Fig. 1, 1, 2; 5, 1-5). Wager (1899) debetweenthestigmaand the
some species of Euglena, and all colorless eu- scribedtherelationship
glenoids). Wherethe paramylumbodiesare large flagellarswellingwhichlies close to the cavityof
and have a definiteshape and orientation,it is the stigma,and emphasizedthe probabilitythat
assumedthat theyare formedin associationwith eithertheswellingor thestigmais a photoreceptor.
definitecytoplasmicstructureswhich are some- Engelmann(1882) had previouslyshownthat the
timesdistinguishable
(E. deses,E. viridis)and have anteriorend of the organismis mostsensitiveto
lightand thatthestigmaprobablyis a photorecepwronglybeen termedpyrenoids(Czurda, 1928).
to as part
Paramylum(sometimesspelled paramylon)is tor. The swellingis sometimesreferred
the typical carbohydrateof the euglenoidsand ofthestigma. It is nowgenerallyagreedthatthe
apparentlyis not foundin otherordersof flagel- stigmais responsiblefororientationof euglenoids
lates or algae. Paramylumis a higherpolysac- ina beamoflight(Mast, 1911).
Colorlessstrainsof Euglenidae which have a
charidewhichdoes not stain withiodineor zincCHLOROPLASTS, PYRENOIDS, AND PARAMYLUM
254
butthoseEuglenidaewhich lated by Tischer(1936),whofoundit to be a tetrastigmaare phototactic,
have no stigma,as well as membersof the non- keto-beta-carotene
which he called euglenarhofamiliesAstasiidaeand Peranemi- don; severalothercarotinoidswerealso present.
stigma-bearing
dae, are not phototactic (Pringsheim,1937).
The red speciesof Euglenaare mostcommonin
Membersof the colorlessfamilies(e.g., Peranema) pools richin organicmatter,especiallyifthe temare sensitiveto changesin intensityof lightbut peratureis above 30?C. Under these conditions
respondby some reactionotherthan phototaxis theymay forma darkred scumoverthe surface
(see motor responses, below). Tchakhotine of the waterduringbrightsunshine,and thescum
(1936a, 1936b),by meansofa rayof intenseultra- becomesgreenwheneverthesunshineceases (Kol,
violetlightfocussedon the regionof the stigma, 1929;Heidt,1934;Hardtl,1935;Johnson,1939).
renderedEuglena incapableof respondingto a reIf the hematochrome
granulesare concentrated
ductionof intensityof visiblelight. The present in thecenterofthecell (Fig. 1, 1) theorganismapevidenceindicatesthatthe.flagellarswellingis the pearsgreenbecauseofthemoreperipheral
arrangeorganellesensitiveto light,and that the function ment of the chloroplasts. However, when the
ofthestigmais to act as a shield,which,depending granules are scattered more or less uniformly
maypreventlightfromreaching thoughoutthe cell (Fig, 1, 2), the generalappearon theorientation,
the swelling(Mast, 1911;see motorresponses,be- ance is red (Heidt, 1934; Hardtl, 1935; Johnson,
1939). It has been foundby severalworkersthat
low).
In two specieseach of Euglenaand Lepocinclis, dispersionof the granulesoccurs in responseto
Sokoloff(1933, 1935a, 1935b) describedan amyla- very brightlight,and Johnsonand Jahn (1942)
ceous body,lyingon theside ofthe gulletopposite foundthat the blue end of the visiblespectrumis
the stigma,whichis supposedto act as a lens in much more effectivethan the red. Heating to
focussinglight on the swelling;apparentlythis temperatures
above 30?C. by eitherimmersion
or
by otherin- infra-red
observationhas not been confirmed
radiationalso causes dispersion.
vestigators. In view of thefactthat Mast (1927)
CYTOPLASMIC INCLUSIONS
showed that light is not focussedin any of the
interpretation
Sokoloff's
studied,
he
euglenoids
Cytoplasmic inclusions have attracted the
shouldnotbe acceptedwithoutconfirmation.
attention of many investigators(iterature on
The stigma sometimesdivides into two parts plant-likeflagellatescited by Hall, 1936; see also
duringcell division(Grasse,1926; Gunther,1928; MacLennan, 1941,Weatherby,1941; and Smyth,
S. R. Hall, 1931; Baker, 1933),and apparentlyit 1944). In addition to the chloroplasts,stigma,
does notarisede novo. The coloredgranules,how- and associated structuresthe euglenoids have
ever,may disperseduringthe prophaseand then been consideredto have fourtypesof cytoplasmic
reaggregateduringthe anaphase (Hall and Jahn inclusions:1) mitochondriaor chondriome,2)
1929b;Gojdics,1934).
vacuome,3) Golgimaterial,and 4) mucusbodies.
All of thesestructurescan be blackenedby osmic
RED
SPECIES
HEMATOCHROME;
acid. In addition, the mitochondriacan be
Several species of Euglena (E. ruba,E. haema- stained vitally by Janus green B, the vacuome
E. rubida,E. flava,E. orien- withneutralred,the Golgimaterialpossiblywith
todes,E. sangguinea,
and Colaciumsanguinea neutral red, and the mucus bodies by either
talis,and E. heliorubescens)
(Lackey, 1934b) are sometimesred in color and neutralred or Janusgreen,or possiblyby neither,
containnumerousgranules(0.5 , or less in dia- dependingupon the species under consideration.
the same or Afterosmification
meter)of thepigmenthematochrome;
the Golgimaterialis supposedly
a very similar pigmentis sometimesfound in most resistantto bleachingby oxidizingagents.
smallerquantitiesin normallygreenspecies (e.g., It has been demonstrated
by use ofthe centrifuge
E. gracilis,E. anabaena,E. klebsii,E. stellata,E. that the specific gravities of the cytoplasmic
Hall, 1933c). structures
and Colaciumvesiculum,
pisciformis,
and vacuome
are as follows:paramylum
The pigmentfromE. sanguineahas been the > chloroplasts
> mitochondria
(Patten and Beams,
subject of several chemicaland spectroscopicin- 1936), as shown in Fig. 5, 2, 3, 5.
vestigations(von Wittich, 1863; Garcin, 1889;
Mitockondria
Kutscher,1898; Kylin, 1927) whichhave demonSmall spherical or bacilliformgranules have
stratedthat it consistsof threecarotinoids. The
been
identified as mitochondria in Euglena
was
isofrom
E.
heliorubescens
pigment
principle
255
(Causey, 1926; Brown, 1930b; R. P. Hall, 1931; has described subcuticular structures which
stainsbut whichare not
Baker, 1933;Pattenand Beams, 1936; Chadefaud, stain withmitochondrial
1937), Colacium (Johnson,1934), Astasia (Hall, identicalwiththemucusbodies.
NR
P.~~~~~~~~~~~~~P
FIG. 5. CYTOPLASMIC
INCLUSIONS
OF EUGLENA(1-5) ANDRHABDOMO0NAS
(6-9)
1, Living Euglena, stained with neutralred, not centrifuged. 2-3, Same as 1, but centrifuged.
Note that
stratification
bears no relationto morphologicalpolarity. 4, Uncentrifuged,
Kolachev preparation. 5, Centrifuged,Kolachev preparation. Note the "peripheral"of "mucus" bodies (X) which are not affectedby centrifUging. 6, Living Rhabdomonas,
strainedwithneutralred,not centrifuged. 7, Same as 6 but centrifuged,
lateral
stratification. 8, Rhabdomonas,stained vitallywith neutralred, then exposed to osmic vapor 48 hrs. 9, Same
ar , exceptexposed for60 hrs. Drawings 8 and 9 mightequally well have been made fromosmic preparations
not 'reviously stainedwithneutralred or fromMann Kopsch preparationswithor withoutvital .staining. (After
Abbreviations:NR, neutral-red
bodiesoflivingorganismsand "vacuome" offixedpreparations;C,ch]oroplasts;
M, probablemitochondria;P. paramylumbodies; S, stigma;X, peripheralor mucusbodies; Y, posteriorrefractile
bodies of undeterminednature.
1930), Rhabdomonas(R. P. Hall, 1931), Entosiphon(Lackey, 1929a), and Peranema (Hall,
1929; Chadefaud, 1938). These granules are
usuallyscatteredin the cytoplasm(Fig. 5, 2, 3, 5);
some of those which are arrangedperipherally
may be identicalto the mucusbodies (see below).
In Petalomonasand Entosiphon,Hollande (1940)
Vacuome
Othersmall granulesscatteredthroughoutthe
cytoplasmhave been identifiedas the vacuome
(Fig. 5, 1-3, 6-9) in Euglena (R. P. Hall, 1931;
Patten and Beams, 1936; Chadefaud, 1936),
Rhabdomonas
(R. P. Hall, 1931;Pattenand Beams,
1936), Peranema (Hall, 1929; Chadefaud, 1938),
256
Colacium (Johnson, 1934), Phacus (Dangeard,
1928a). These granules can be distinguished
fromthe mitochondria
by stainingwitha mixture
of neutralred and Janusgreen. If thesegranules
are firststained vitallyby neutralred, they can
thenbe observedto blackenwithosmicacid during
direct microscopicalexamination. However, in
most cases they also blacken with osmic acid
before vital staining. The function of the
vacuome is discussed by Dufrenoy (1940).
Golgi Material
The blackeningof the vitallystainedvacuome
granulesby osmicacid, togetherwiththe blackening by usual Golgi methods and the general
occurrenceof thesegranulesamongthe protozoa,
has been takenby R. P. Hall (1930,1931,1936) to
indicate that these structuresmay be identical
with the Golgi material. This view has been
opposed on the basis of observationsof centrifuged material by Patten and Beams (1936,
Euglena), Beams and King (1935, bean root)
and Daniels (1938, gregarines). The possible
homologyof the vacuomeand Golgielementshas
been reviewedrecentlyby Kirkmanand Severinghaus (1938), Hirsch (1939), Guilliermond
and
Atkinson(1941), Baker (1944), Smyth(1944) and
Hibband (1945). In some cases the neutralred
stainingmaterialof flagellatesmay not be the
same as that whichstainswithosmicacid (centrifugingexperiments,
above) but in othercases the
two are identical (Hall, 1936). Althoughexposureto neutralred may inducethe appearance
of granuleswhichcan later be stainedwithosmic
acid (Patten and Beams, 1936), this does not
preclude the possibilitythat some osmiophile
materialmay be presentbeforeexposure. It is
stated by some cytologists(Cowdry, 1943, and
reviews cited above) that Golgi material in
multicellularorganisms does not stain with
neutralred (althoughit may be associated with
neutral red stainingmaterial). If this criterion
should be applied to unicellularorganisms,then
the vacuome would be therebyeliminatedas a
homologueof the Golgi materialof higherorganisms.
The stigmaof Euglena is sometimescalled the
Golgi material(Grasse, 1925, 1926; Duboscq and
Grasse, 1933). However, since it is a highly
specialized structureordinarilyassociated with
chlorophyll,it is usually eliminatedfrom con-
siderationas such (Mangenot, 1926; Hall, 1936;
Pattenand Beams, 1936).
vacuoleor othernearbymaterial
The contractile
in Euglena(Sigot,1931;Gatenbyand Singh,1938),
Rhabdomonas (Smyth, 1943, 1944), Astasia
(Smyth,1944), and ciliates (Nassonov, 1924) is
oftenblackenedby osmic acid. Since the contractilevacuole is associatedwithexcretion,there
has been a considerabletendency to hold it
homologouswith the Golgi material (Gatenby
and Singh, 1938; Smyth, 1944; cf., Hall and
Nigrelli, 1937). However, some ciliates have
contractilevacuoles which do not blacken with
osmicacid (citationsby Smyth,1944) and others
have no osmiophilicmaterial whatsoever. In
flagellates,the evidence is also variable. Hall
(1930) has demonstratedthat the contractile
vacuole in Chilomonasblackens much less consistentlythan the small granules(cf. Mast and
Doyle, 1935) and that the vacuole of an unidentified species of Astasisadoes not blacken. However, Smyth (1944) succeeded in blackeninga
vacuolar structurenear the gullet in Astasia
harrisii.
In Peranema,Brown (1930a) has apparently
describedthe pellicularstriationsas a homologue
of the Golgi material (R. P. Hall, 1931, 1936).
Brown (1930b) and Baker (1933) have identified
small sphereswith osmiophiliccoveringsas the
Golgimaterialin Euglena,but Patten and Beams
(1936) were unable to confirmthe existenceof
thesestructures.
Hollande (1938) has described endoplasmic
osmiophilicbodies whichdo not take vital stains
in Parastasia, Peranema,Entosiphon,Anisonema,
Euglena,Penatomozas,and threespeciesofHeterronema,and whichhe believesrepresentthe Golgi
materialof the euglenoids. He found that the
numberofsuch bodiesvariedfromone to twentyfiveand was moreor less constantforthe species.
The onlygeneralconclusionthat can be made is
of Golgimaterialin euglenthat the identification
oids is most uncertain. This is the viewpoint
taken by Hall (1936) and by Patten and Beams
(1936), and at present there seems to be no
necessityforrevisingthisstatementbecauseofthe
more recent contributionsabove (cf., however,
Smyth,1944).
a protistan
of identifying
Much of the difficulty
homologueof the Golgiapparatusof multicellular
organismsis that there seems to be no clear
definitionof this material in terms of staining
reactions, morphology,behavior, or function
whichis acceptable to most cytologists(cf. Hall,
1930). The only point of universal agreement
seems to be the name "Golgi," and most of the
difficulty
has centeredaroundattemptsto attach
this name to a structurein spite of the fact that
are not generallyaccriteriafor identification
cepted. In mostcases thereis no doubtthat the
describedstructuresexist,althoughthe formand
quantity may vary with the conditionsunder
which the organismswere grownand with the
techniquesused forstaining;thepointofdisagreementis usuallythat of homology. SimilarGolgi
problemsin metazoa are discussed by Hibbard
among the confusionof
(1945). Unfortunately,
ideas concerninghomologies,the possible importhemselvesis oftenignored.
tanceofthestructures
Mucus Bodies
257
bodies" verysimilarin shape and positionto the
above mentionedmucus bodies, but they were
able to stain themonly withosmicacid and not
withvital stains.
Chadefaud(1936), on the basis of his homology
of the peripheralbodiesof the flagellateswiththe
of ciliates,has createda new groupof
trichocysts
Protista, the Protogastr6ades,to include the
Ciliata, Dinoflagellida,Crytomonadida,Chloromonadida,and Euglenida,all of whichare supposed to possess trichocysthomologues. In this
group,in contrastto the Gastr6adesor Metazoa,
into
the digestivesystem is not differentiated
cell layers, but consistsonly of the gullet and
reservoir,and even this in many cases is not
used for ingestion. Trichocysthomologuesare
also discussedby Reukauf (1940).
NUCLEAR STRUCTURE AND MITOSIS
In several species of Euglena (but definitely
not in others,Chadefaudand Provasoli,1939), in
The nucleus of the euglenoidscontainsone or
Peranema,and in othercolorlesseuglenoidsthere more centrally located endosomes (Hall and
are smallsphericalor elongateinclusionsarranged Powell, 1928; Loefer, 1931) and a number of
in spiral or longitudinalrows just beneath the irregularly
shaped chromatingranuleswhichare
pellicle(Fig. 5, 4). In EuglenaPattenand Beams distributedbetween the endosomeand the nu(1936) were unable to displace them by centri- clear membrane. In Astasia and Distigmna
these
fuging(Fig. 5, 5). In some species these bodies chromatingranulesmay constitutea permanent
stainwithJanusgreen("peripheralmitochondria" spireme(Lackey, 1934a). In Khawkinealeucops
in number,and each
ofPeranema,Hall, 1929); in otherstheystainwith the granulesare twenty-two
neutralred (Euglena,Anisonema);in othersthey granulegivesriseto a chromosome
duringmitosis
are not stainable with either (Euglena, Patten (S. R. Hall, 1931). However,thiscorrespondence
and Beams, 1936). These structuresare some- betweenchromatin
has
granulesand chromosomes
times referredto as "mucus bodies" and ap- not been noted for other euglenoids. In all of
to the gelatinousmembranous the euglenoids the nuclear membranepersists
parentlycontribute
division(Figs. 4, 6).
coveringof the non-motilestages, especially in throughout
Euglena velata(Dangeard, 1902) and E. mucifera The endosomedivides duringmitosisbut does
(Mainx, 1926). Chadefaud (1937, 1938, 1939) not contributematerialtowardthe formationof
considersmucus bodies to be homologouswith the chromosomes(Fig. 6, 1-8). In Distigma,
the trichocysts
of ciliatesand also withthe par- Lackey (1934a) describeda small intranuclear
abasal body of animal flagellates. Furthermore, body of unknown functionwhich differedin
he states that thereis no essentialdifference
be- stainingreactionfromtheendosome. In Euglena,
tween those which stain with Janus green and Baker (1926) assumed that the endosomegives
those which stain with neutral red and cresyl rise to a bud whichgives rise to the centrosome
violet. The latter in Euglena have been con- and blepharoplasts,and Ratcliffe(1927) made
sidered to representthe vacuome (Dangeard, similar assumptions for another intranuclear
1928a), but it is also possibleto stainthevacuome body. These proposals have been criticizedby
and the mucus bodies in the same organism Hall and Powell (1928).
Mitosis in a variety of euglenoidshas been
(Chadefaud,1937; Dangeard, 1928a; Grasse and
Poisson, 1933). Chadefaud (1938) defines the describedby numerousinvestigators(early litermaterialwhichis ature cited by Hall, 1923; Rhabdomnonas:
mucus bodies as mitochondrial
Hall,
associated with the locomotor-elements and 1923; Euglena: Baker, 1926; Ratcliffe, 1927;
whichcan elaborateeithera glycogen-like
material S. R. Hall, 1931; Gojdics, 1934; Krichenbauer,
or one whichcan be stained with vacuome dyes. 1937; Peranema:Hall and Powell, 1928; Brown,
Patten and Beams (1936) described"peripheral 1930a; Lackey, 1933; Hall, 1934; Colacium:
258
Loefer, 1931; EnJohnson, 1934; Heteronema:
tosiphon:Lackey, 1929a; Distigma:Lackey, 1934;
4
3
6
7
5
a
2
~~~~~~~~~~1
1 4~~~1
FIG. 6. MITOSIS IN EUGLENA,PERANEMA,AND
ENTOSIPHON
1-8, Nuclear phenomenain Euglena. 1, Equatorial
"plate" stage,optical section,somewhatdiagrammatic.
2, Slightlylater stage, unfoldingof V's is pronounced.
3-8, Behavior of chromosomes,hypotheticalcase with
four chromosomes,showinglongitudinalsplitting.
9-13, Peranema, pharyngeal rods not shown. 9,
Stage figuredby Hall and Powell (1928) and interpreted
as outgrowthof a new flagellumin binaryfission,possiblya separationphase earlierthan 10. 10, Prophase
showing one large flagellumon each side ofwidened
gullet. 11, 13, Early anaphases withone large flagellum and one shortoutgrowthin each daughtergullet.
12,Telophase,showingonelargeand one smallflagellum
in each gullet.
sulcatum.14, Late "prophase,"
14-15,Entosiphon
showingretentionof old flagellaand outgrowthof two
new ones. 15, Later stage,flagellagrownbeyondcytostome. (1-8, After Hall, 1937a; 9-12, after Hall,
1934; 13, after Lackey, 1933; 14-15, after Lackey,
1929a).
forEuglena by Jirovec(1926), but this was apparentlya misinterpretation.
Duringdivisionof organismswithone flagellum
the blepharoplastdivides,and one part passes to
each daughtercell. The flagellummay remain
and a newflagellum
attachedto one blepharoplast,
then grows out from the other (e.g., Astasia,
Lackey, 1934a). In E. gracilis, Krichenbaur
(1937) has describedthe separationof the ramiof
the flagellumso that one ramus goes to each
daughter. In organismswith two flagellaboth
flagella may go to one daughter (Entosiphon,
Lackey, 1929a; Fig. 6, 14-15) or each daughter
may receive one of the old flagella(Heteronema,
Loefer,1931; Peranema,Hall, 1934; Fig. 6, 9-13).
In the Euglenidaethe flagellarswellingdisappears
during the prophase and later reappears (Fig.
4, 1-4).
During the prophase stages the chromatin
granules(if they have not already done so) become recognizableas definitechromosomesand
apparentlybecome divided longitudinally.This
longitudinalsplittingof the chromosomeshas
been described as occurringin the prophase
(Baker, 1926, Euglena agilis) metaphase (Ratand telophase (Tschencliffe,1927,E. spirogyra),
zoff,1916,E. viridis)stages.
During the metaphase the endosome is
formwhatsuperelongated,and the chromosomes
ficiallyappears to be an equatorial plate (Fig.
6, 1). However, upon closer examinationthis
"plate'" is seen to be made up of a numberof
and each double
V and Y-shaped chromosomes,
has one armtowardeach ofthepoles.
chromosome
This has been observed for Peranema,Astasia,
Distigma, Rhabdomonas,Heteronema,Colacium,
and Euglena (literaturecited by Lackey, 1934a;
Hall, 1937a). These V's and Y's unfoldsothat
one half goes to each pole. The divisionof the
is definitely
longitudinal(cf. S. R.
chromosomes
Hall, 1931; Gojdics, 1934), and the chromosomes
of the euglenoids during the metapbhasediffer
fromthosein typicalmetazoanmitosisonlyin that
theydo not becomegreatlyshortenedand are not
arrangedin one plane.
The effectof chronic arsenic poisoning on
nuclear structureis discussed by Rybinskyand
Zrykina(1935).
LIFE HISTORY; REPRODUCTION, CYSTS, AND
Astasia: Belar, 1926, Lackey, 1934a). Early
PALMlELLA STAGES
observationswere reviewedby Belari(1926), and
ofeuglenoidmitosiswas discussed
The lifehistoryof a euglenoidmay consistof
the significance
was
described
Amitosis
and encysted stages, with palmella
flagellated
by Drezepolski (1929).
259
stages in the Euglenidae and Colaciidae, and organismsembeddedin a gelatinousmatrixwhich
plasmodialstages in the Colaciidae only. Repro- is oftenfoundattachedto thewallofold laboratory
ductionis usually by longitudinalbinaryfission cultures. Divisionoccursin thepalmella,and the
of the flagellatedstage. Transversedivisionhas organismsmay become flagellatedand leave the
been reportedonly by Tannreuther(1923). In matrix. The palmella stage is one of the two
some species of Euglena division may occur in characteristic
stages of Colacium,is less common
thin-walled cysts or in palmella stages. In among the genus Euglena,and does not occur in
Trachelomonas
divisionusually occurs in the old the colorlessfamilies. It is the most common
test,and one of the daughterssecretesa new one stage of the genusEuglenocapsa(Steinecke,1932).
(Klebs, 1883; Gimesi, 1930). However, the Palmellastagesof euglenoidscan be distinguished
flagellatemay leave the test beforedivision,and from those of other flagellatesby the typical
then each daughtersecretesa new test (Wilson, euglenoidstigmaand the presenceof paramylum.
fromall othergenera in
1928). Colaciumdiffers
According to Mainx (1928), formation of
that divisionapparentlydoes not occur in the palmellastagesmay be determinedby the foliowflagellated
stage (see below).
ing: 1) Content and concentrationof medium.
Encystedstageshave been describedforseveral They occuron agar in manyspecies. 2) Extremes
genera, includingEuglena (many investigators, of temperature,especially when change is sudespecially Mainx, 1928, and Gunther, 1928), den. 3) SuddenchangeofpH. 4) Suddenchanges
Phacus (Smith, 1933), Trachelomonas(Smith, fromlightto darkness,or vice versa,dependingon
1933), Eutreptia (Steuer, 1904), Rhabdomonas amountofreservematerialin cell.
(Lemmerman, 1913) and Distigma (Lackey,
SEXUAL PHENOMENA
1934a),and probablyexistforothers.
reportsof gameticunion
Thereare unconfirmed
The cyst wall in Euglena is composedof an
(B1utschli,
1906). Cysts for several euglenoids. The most often cited
unidentified
carbohydrate
are usually spherical but may be flask-shaped example is that of Copromonas(Dobell, 1908),
(E. orientalis,
E. tuba) or pentagonal (Distigma). but the detailsof copulationand even the identiIn the lifehistoryof some species of Euglena, ficationof this organismare in doubt (Gatenby
theremay be formedas many as threetypes of and Singh, 1938; Gatenby and Smyth, 1940;
cystsand a palmellastage (Mainx, 1928; Gunther, Chadefaud,1938). The structureof the nucleus
insertionwould indicate
and the type of filagellar
1928). The typesof cystsare:
1) Protectivecysts. Singlecelled,withheavy, that the organismdescribedby Dobell is not a
sometimesstratifiedwall, usually cementedto a euglenoid. Abnormal divisions of Khawkinea
ornamented
in E. chiamy- halli whichresultedin binucleateindividualsand
palmella-like
membrane,
dophora. Seldom occur in culture,except spor- which could easily be mistakenfor copulation
adically in very old ones. Occur in E. deses have been described by Jahn and McKibben
(1937),whoemphasizedthisas a possiblesourceof
at 0-40C.
Binucleate individuals of E. deses
confusion.
2) Reproductiveor division cysts. Uni- to
multicellularwith thin, elastic, and permeable have been reported by Gojdics (1934) and a
membranewhichincreasesin diameteras the cells trinucleateKhawkineaocellataby Mainx (1928).
divide. Not present in most species. In E. Haase (1910) describedwhat she supposed were
gracilisand E. viridismay containup to 32 or sexual stages in Euglena sanguinea,but it has
been suggestedthat these wereparasites(Mainx,
even 64 cells. Cells non-flagellated.
3) Temporary,resting, or transitorycysts. 1928),and no sexualstageshave been reportedby
Wall thickbut not completelyclosed,cell usually more recent investigators(e.g., Gojdics, 1939)
flagellatedand free to move about in cavity. who have studied the same species. Biecheler
Formed in response to strongsunlight. Occur (1937) observed (a dozen times) the fusionof
species of Euglena
in E. gracilis,in the mud-dwellingE. terricola, pairs of cellsof an unidentified
E. geniculata,E. sanguinea,and perhaps in E frombrackishwater. He was unableto repeatthe
observation with Euglena from other sources.
viridisand E. piscitormis.
In some speciesthereare also thin-walledcysts Krichenbauer(1937) has describedbi- and quadriin which reproductionis not known to occur nucleatestages of Phacus whichhe consideredto
be evidence of reductionand autogamy. How(E. tuba).
Pochmann (1942) has suggestedthat these
ever,
of
consists
The palmella stage
non-flagellated
260
may be the resultof abnormalcultureconditions
(see also, Mainx, 1928). Lackey k1929b)made
a verycarefulsearchforendomixisor conjugation
in Entosiphonand Peranemaand was unable to
find evidence that they exist. At present the
existenceof sexual phenomenain the euglenoids
remainsunconfirmed.The question of whether
the euglenoidcell is normallyhaploidor diploidis
discussed by Chadefaud (1940), but in the absenceofproofoftheexistenceofsexualphenomena
this questionseems somewhatfar-fetched.
photoautotrophic,
photomesotrophic,
and photometatrophic.
Photoautotrophic
organismsare able to utilize
ammoniumand nitrate compoundsas nitrogen
sources. Examples of facultative photoautotrophsare E. anabaena,E. gracilis(Schoenborn,
1942),E. klebsii,E. stellata,E. terricola,
E. geniculata, E. viridis;no obligatoryphotoautotrophis
known.
Media whichhave been used underconditions
which permit only photoautotrophicnutrition
(Hall and co-workers)containa numberof chemNUTRITION
ical elementsin eitherappreciablequantitiesor
yearsmanyphototrophic traces. It shouldbe possibleby meansofsuccesDuringthepast fifteen
and saprozoic euglenoids have been grown in sive eliminationsto determineexactly which
bacteria-freeculture, and measurementshave elementsare necessary. It has been determined
been made oftheeffecton growthofvariousfatty that the calcium requirementof E. stellatais
acids, alcohols, amino acids, peptones,proteins, apparentlyhigherthan that of othereuglenoids,
minerals,and vitamins. Numer- and thatMn acceleratesthegrowthofE. anabaena.
carbohydrates,
at
ous studiesof this type have been performed
Otherspeciesof Euglena requirecertainamino
and F. Mainx,at the acids as a nitrogensource (photomesotrophs);
Prague by E. G. Pringsheim
Pasteur Instituteby A. Lwoff,H. Dusi, and L. an example of an obligatoryphotomesotroph
is
and other E. deses,an organismwhichapparentlycan not
Provasali,and at New York University
Americanlaboratoriesby R. P. Hall, T. L. Jahn, grow in inorganicmedia. Several species are
J. B. Loefer,A. M. Elliott,and H. W. Schoen- known to be facultativephotomesotrophs
(i.e.,
born. The nutritionof the euglenoidshas been are also photoautotrophs):E. anabaena, E.
reviewedby von Brand (1935),Hall (1939,1941a), gracilis,E. klebsii,and E. stellata. One interesting
and Doyle (1943), whose papers should be featureof photomesotrophic
nutritionis that a
consultedforthe literature. Methodsofisolation particularamino acid may supportgrowthof one
consistofsuccessivewashingin sterilemedium,of species but not of another. Forexample,phenylchoosingcoloniesfroman agar streak,of allowing alanine was satisfactoryfor E. anabaena, E.
the flagellatesto migrateaway fromthe bacteria, gracilis,and E. stellata,but not forE. desesand
and the killingof bacteriafound with encysted E. klebsii,while serinewas adequate for all of
stages by chemical agents (literaturecited by the above exceptE. anabaena. ComparabledifMainx, 1928; Hall, 1937c; Kidder, 1941).
are knownforotheraminoacids. Growth
ferences
genus whichhas of photomesotrophic
The only chlorophyll-bearing
species is accelerated by
been intensivelystudied fromthe viewpointof the addition of organic carbon sources (e.g.,
nutritionis Euglena. All membersof this genus sodium acetate) to a mediumcontainingone or
are apparently both phototrophicand hetero- more amino acids.
trophic,i.e., theycan utilizeeithercarbondioxide
Photometatrophic
nutrition(utilizationof pepor dissolved organic compounds as a carbon tonesor proteinsas nitrogensource)is possiblefor
to thestatementofTannreuther all greenflagellatesthat have been grownin pure
source. Contrary
(1923) and to those foundin several elementary culture. It is
possible that E. pisciformis may
and semi-popularbooks,Euglena seldom,if ever, be an
obligatoryphotometatroph,
but there is
ingestsparticulatefood(Hall, 1933c,Baker, 1933).
some evidenceto the contrary. Certain species
The statementsof Tannreutherare commonlyreare known to produce proteolytic enzymes.
garded as the result of a misinterpretation.
Accelerationof growthof Euglena underphoNutrition
Phototrophic
conditionscan be obtainedby the
tometatrophic
use
of
media
salts of certainorganic
containing
utilize
carbon
can
Phototrophic organisms
dioxideas a carbonsourcein the presenceof light, acids, variouscarbohyd:ates,and alcohols. Salts
and on thebasisofthetypeofnitrogencompounds of acetic and butyricacids are particularlyefneeded may be classified into three groups; fective.
Heterotrophic
nutrition
organismsdo not containchloroHeterotrophic
phylland must depend ubon organiccompounds
for a source of carbon. Euglena in the dark,
however,may be considereda facultativeheterotroph. On the basis of the nitrogen source
needed,threetypescan be distinguished:heteroautotrophic, heteromesotrophic,and heterometatrophic.
nutrition(utilizationof inorHeteroautotrophic
ganic nitrogencompounds)is knownto occur in
Astasia and in Euglena gracilisin darknesswhen
grown in a mediumof ammoniumnitrate and
betwcenthe minacetate. The only difference
finumnutritionalrequirementsof Astasia and
the photoautotrophic
species of Euglena is that
Astasia needs a simpleorganicsource of carbon.
Heteromesotrophicnutrition (use of amino
acids) has not been definitelyproven for any
euglenoid but is known for membersof other
orders.
nutrition(use of peptones
Heterometatrophic
plus possible addition of other organic carbon
sources) is knownto occur in all of the colorless
euglenoidswhichhave been investigatedand in
some chlorophyll-bearing
species in darkness.
Growthof most euglenoidsis accelerated by
certainlowerorganicacids and in somespeciesby
lower alcohols. The general occurrenceof an
accelerationof growthand increase in carbohydrate reservesin the presenceof acetate is consideredby Lwoffand Dusi (1936) to indicatethat
acetic acid is a normalstep in the synthesisof
carbohydratefrom carbon dioxide. The importanceof acetate metabolismis also discussed
by Pringsheim(1935). Wheneverthe utilization
of an organicacid is studied it is necessaryto
controlthe pH so that the effectof the organic
ion may be separated fromthat of the undissociated molecule (Jahn, 1934), especially since
these effectsmay be opposed. Evidence of such
an effectwas obtained by von Dach (1940) for
Astasiaklebsii.
The questionof whetheror not euglenoidsrequire specificchemicalgrowthfactorshas been
reviewedby Hall (1943). It has been demonstrated that the photoautotrophicspecies of
Euglena (listed above) do not require thiazole,
pyrimidine,or thiamin. These substances are
also not necessaryfor the growthof Astasia sp.
and ofEuglenagracilisin darknesswhenin acetate
mineralmedium,nor forE. anabaena in the light
261
in asparagineor aminoacid-mineral
media. HIowever, in the lattermedia thereis some evidence
that thiazole and pyrimidine,but not thiamin,
are necessaryfor growthof E. pisciformis,
and
and that pyrimidine
but not thiazoleor thiamine
forgrowthof E. gracilisin darkness. Since these
positive results apparentlyrequire confirmation
(Hall, 1943), it seems as if thereis no conclusive
evidencethateuglenoidsneed any of thesegrowth
factors.
Elliott (1937, 1938) demonstratedthat growth
of Euglena gracilisin lightbut not in darknessis
acceleratedby theadditionofauxinto the culture
medium,especiallyifthepH is about 5.6. Growth
of Khawkinea halli is not accelerated at any
pH by auxin.
In additionto the mineralrequirements
noted
above, it has been claimedby Pringsheim(1926)
that calcium is not necessaryfor the growthof
Euglena gracillis. However, the conclusionhas
been questionedby Mast and Pace (1939) who
found calcium presentin magnesiumsalts such
as those used by Pringsheim. Mainx (1928)
foundthat ironoxide producesa definiteacceleration of the growthof E. desesand E. viridis,a
slightaccelerationof E. muciferaand E. velata,
but no accelerationofE. gracilisand E. intermedia.
The oligodynamic
effectofmetalshas beenstudied
by Jfrovec
(1934b).
The chemical changes produced in culture
mediahave beenstudiedby Hall (1937b). Gelatin
is liquefiedby Euglena gracilis,slightlyliquefied
by E. klebsii,but not by several other species.
No species was foundwhich can produce indol.
Reductionof nitrateto nitritein the absence of
sugar is performedby E. anabaena, E. deses,
E. klebsii,E. pisciformis,
E. viridis,and Colacium
vesiculumbut not by E. stellata. In the presence
of dextrose,reductionis performedby all of the
above exceptE. desesand E. stellata.
Holozoicnutrition
Holozoic species have not been obtained in
bacteria-freeculture,and very little is known
about theirnhtritional
requirements.
RESPIRATION
The only thoroughstudy of respirationof a
euglenoidwas made by von Dach (1942), who
used bacteria-freeculthres of Astasia klebsii
He foundthat respirationis increasedto a level
(compared to that in inorganicmedia) of 783
262
per cent by the additionof acetate, 489 per cent
by ethanol,328 per cent by propionate,195 per
cent by butyrate,168 per cent by hexosediphosphate, and 158 per cent by formate,but is not
changed by the addition of a variety of other
quotient
organicacids or sugars. The respiratory
in both organicand inorganicmedia is approximately 1.0. Von Dach determined spectroa, b, and c are present.
scopicallythatcytochromes
In inorganicmedia, respirationis reduced by
cyanide but accelerated by azide. However, in
the presenceof acetate respirationis reduced by
both cyanide and azide. Therefore,two respiratory mechanismsmust be present. The only
ina euglenoidis that
otherdetectionofcytochrome
of Lwoff (1933), who found the cytochromec
band in E. gracilis. The methods,theories,and
interpretationsinvolved in such measurements
have been reviewedby Jahn(1941).
lightand theswellingand causesa suddendecrease
in illuminationof the swelling,and this produces
a shockreactionwhichendsin a correctivechange
in the directionofmovement. Orientation,then,
is the result of rotation-of the organismon its
longitudinalaxis and the ability of the flagellar
swellingto produceshock reactionsupon sudden
changesof intensity. If light fromtwo sources
strikesthe animal,the directionof locomotionis
determinedby the relativeintensities. Euglena
is normallyphotopositivein weak and photonegative in stronglight,but reversalof the photopositive responsemay occur if the intensityis held
constantand the temperatureloweredby 10 to
15?C. These changesare closelycorrelatedwith
the state of adaptation.
Several investigators(Mast 1917, 1927, 1941;
Dangeard, 1928b) have studied the effectiveness
of variouswavelengthsin the responseof Euglena
to light. For fivespecies of Euglena,forPhacus,
and for Tracielomonasthese are 410 to 540 mi/,
MOTOR RESPONSES
at about 485 m,u;
with a peak of effectiveness
All the green genera and the stigma-bearing forPeranemathe most effectivewavelengthsare
colorlessformsare phototactic;the non-stigma- 302 mu and 505 mj. Tchakhotine (1936a,b)
bearing formsmay respond to light by other has demonstratedthat the entire surface,and
reactionsbut are neverphototactic. Our present especiallythe anteriorend, of Euglenais sensitive
knowledgeof the motorresponsesof Euglenaand to stimulationby intense ultravioletlight.
of Peranemato light is largelythe result of inPeranemarespondsto a rapid increase in investigationswhichhave been carriedon formany tensityby a 900 change in direction. A rapid
years at Johns Hopkin's Universityby H. S. decrease or a slow increasehas no effect. The
Jenningsand S. 0. Mast and their associates wholeorganismis sensitiveto light,the flagellum
and students,M. Gover,B. Hawk, L. B. Shettles, being most sensitiveand the posteriorend least
and C. Hassett. This subject has been reviewed sensitive. As measuredby the reactiontime,the
by Jennings(1906), Mast (1911, 1936, 1941) and darkadaptationcurveofPeranemais veryinterestWarden,Jenkins,and Warner (1940), and these ing. If Peranema is transferredfrom light to
publicationsshould be consulted for literature darkness,uponexposureto 2000metercandlesthe
priorto 1941.
reaction time decreases fromabout 31 seconds
Euglenaswimsina spiralpath withtheflagellum after15 minutesin darknessto 4.5 secondsafter
directedobliquelybackwardneartheside opposite an hour, and then increasesto 63 seconds after
the stigma,i.e., the ventralside (Fig. 5, 1), and six hours. During lightadaptation the reaction
the cell rotatesso that the stigma maintainsa timedecreasesto a minimumof about 15 seconds
constantpositionin relationto the main axis of in 30 minutes,and then increasesto a constant
progression. In photopositiveorganisms,if the level of about 20 to 25 seconds. The phenomena
intensityis rapidlydecreasedthe organismstops of adaptation are apparentlycomplex, and no
suddenly,turnsin a directiontowardthe surface adequate theoryhas been proposed which will
on which the stigma occurs,and then proceeds explain the results. Shortess(1942) foundthat
in a different
direction.
constantlightof moderateintensityhas no effect
Euglena may be eitherphotopositiveor photo- on the rate of locomotion,but that at high innegative. If it is photopositiveand is oriented, tensitythe rate is increasedbelow 14TC. and is
the positionof the stigmain relationto the path decreased above 14?C. Hassett (1944) demonremains constantand light falls continouslyon stratedthat the sensitivityof Peranemato light,
the flagellarswelling. If the directionof the as measured by the reaction times, is greatly
dyes(eosin,
light is changed,the stigma comes betweenthe increasedbythepresenceoffluorescent
263
rose bengal, neutral red). This photodynamic sist of amoeboid organismswhich grow in the
effectis not in accord with the reciprocitylaw. cytoplasm and later undergo multiple fission
Membersof the Euglenidaeand Astasiidaeare (Sphaerita) or repeated binary fission (Pseudofreeswimming. However,some sphaerita)to formmany spores. The spores are
characteristically
but acfew species which have short flagella or none oftendescribedas being non-flagellated,
in Sphaerita
(e.g.,E. deses,E. x., see Mast, 1911) sometimesor cordingto Sparroware monoflagellate
always "glide" on the substratum. Membersof and biflagellatein Pseudosphaerita.The spores
the familyPeranemidaeare usually in contact are releasedthroughan openingin the host cell,
thoughtto be sexual stages of
witha surfaceand move by a "gliding"motion. and vere formerly
This may be linked withthe holozoicmethodof the host. Infectionof a new host occurs either
nutritionin the latter. If the flagellumof Per- by attachmentof the flagellateto the pellicleor
anemastrikesa sand grain,theresponseis a typical possiblyby entrancethroughthe gullet. Sexual
shockreaction,witha 90? changein the direction phenomenahave been reported. A list of describedspecies is givenby Jahn (1933b).
of locomotion.
The genus Olpidium occurs in Euglena and
Bancroft(1913) found that Euglena is either
positivelyor negativelygalvanotropicand that differsfromSphaeritain that the spores are rethe abilityofthe animalto responddependsupon tained untilfullyformedin a sac whichis partly
the acidity of the medium. Schroder (1927) on theoutsideofthehost.
The genus Polyphagus,whichaittacksEuglena,
reportedanodal galvanotropismwhichis greater
however,is develops outside the host body, into whichit
in a basic medium. Galvanotropism,
a phase of euglenoidphysiologywhich has not projects a rhizoid. A single Polyphiagus,by
means of branchedrhizoids,may attack as many
yetbeenadequatelyexplored.
All of the Euglenidae,most of the Astasiidae, as fiftyflagellates,from which it extracts cybut not most of the Peranemidaeare negatively toplasm. Numerous flagellated zoospores are
copulationoccurs,and thezygotebecomes
geotropicand tend to aggregateat the surfaceof formed,
cultures,especially toward the light. Euglena a resistantspore. Polyphagusmay be parasitized
also reacts against centrifugalforce when the by Pleolpidium.
is epibiotic on
The genus Scherffeliomyces
magnitudeof the forceis betweenone half and
Euglena.
eightand a halftimesgravity.
De Wildeman (1894) found that Euglena is
IMMUNITY REACTIONS
but that high temperatureis such
thermotactic,
that the
a weak stimulusfornegativethermotaxis
A number of investigatorshave studied the
organismscan be attracted by light to lethal serologicalreactionsproduced in vertebratesby
(de Wildeman,1928).
temperatures
theinjectionofeuglenoidsor ofeuglenoidextracts.
Much of the earlierworkis invalid because the
PARASITES
euglenoidswere not free of bacteria (literature,
Parasitesofthe euglenoidsconsistofone species Steinecke, 1925). However, the existence of
of bacteriumand at least five genera of Phy- definiteantibodies has been demonstratedby
comycetes,all of whichare usually fatal to the Mary Elmore Sauer (citationsbelow) and Tanzer
host. Literaturecitations are given by Kirby (1941). The injected vertebrate produces a
(1941b) and Sparrow (1943). Sparrow's book cytotoxicantibodywhichcauses loss of flagellum
containsclear diagnosesof generaand should do and death whenthe immuneserumis added to a
much toward relieving confusionin this field freshculture (Elmore, 1928a). An anaphylactic
reaction can also be demonstratedwith guinea
among protozoologists.
The sole bacterial parasite, Caryococcushy- pigs (Elmore, 1928b). The antibody is therwas describedby Dangeardin 1902in mostable,is speciesspecific(antibodyforEuglena
pertropisicus,
the nucleusof Euglena deses,and apparentlyhas gracilisis not toxicforE. proximaor E. polymorexhibitscertain
pha), doesnotrequirecomplement,
notagain beenreported.
are the often absorptivephenomena,and may producepassive
The mostcommonPhycomycetes
confusedgenera Sphaerita and Pseudosphaerita. sensitization. In short, it behaves as a true
These organismas
apparentlyhave been seen in antibody(Sauer, 1935a). It has also been demonTropi- strated that the green and colorless (grown in
Euglena,Phacus,Peranema,Trachelomonas,
doscyphus,and Anisonemna.The parasites con- darkness) strainsof E. gracilisare serologically
264
distinct(Elmore, 1928b) and that thereare also
two greenstrainswhichdiffern theirreactions
(Sauer, 1935b). Tanzer (1941) obtainedcytotoxic
antisera for Astasia sp., Khawkinea halli, K.
ocellata,Euglena gracilis,and E. viridis. The
serumfor K. halli producednot only loss of the
ofa gelatinousexudate.
buttheformation
flagellum
Tanzer also showed that K. halli is serologically
distinctfromK. ocellata,and thatthesetwospecies
are morecloselyrelatedto Euglenathanto Astasia.
apparentlylost duringone or more unequal cell
divisions (Khawkinea linealis, K. ocellata, K.
quartana,K. halli,Hyalophacusocellata,Trachelomoizas reticulata,T. volvocinahyalina, Euglena
sanguinea hyalina, E. viridis hyalina). In a
fewcolorlessspeciesthe stigmahas also been lost
hyalina;
(Euglenaacus hyalina,Phacuspleuronectes
literature cited by Pringsheim, 1937). The
assignedto thisfamilyare the
organismscommonly
green genera Euglena, Phacus, Lepocinclis,
Trachelomonas, Strombomonas, Euglenocapsa,
POPULATION STUDIES
Ascoglena, Klebsiella, Eutreptia, Eutreptiella
Euglenahas been used forpopulationstudiesby (syn. Gymnastica), and Euglenamorphia,and
several investigators.Jahn (1930) showed that the colorless genera Khawkinea and Hegneria.
growthtended to followthe autocatalyticculve The name Lepocinclisis preferableto Crumenula
and that this precludedthe action of an "auto- in spite of the priorityof the latter(Deflandre,
catalyst." Jahn(1929) and Hall and Schoenborn 1932).
(1939) found an inverse relationshipbetween
Colaciidae
growth rate and initial population density.
Colaciidae
(Colaciaceae) was created
The
family
between
Sweet (1939) showedthattherelationship
to
contain
the genus Colacium.
Smith
(1933)
by
with
growthrate and initial densitymay vary
conditionsand sometimesmay be The life historyof Colaciumas determinedby
environmental
directratherthan inverse. Populationproblems Johnson(1934) and othersshows that the sepof the euglenoidsare discussedby Hall (1941b). aration is well warranted. The organism apparentlyspends most of its life cycle in nonTAXONOMY OF FAMILIES
flagellatedstages, either as a palmella or as a
The order Euglenida is usually consideredto stalked dendroidcolony. In the palmella stage
consistof threefamilies(Euglenidae; Astasiidae; both binaryfissionand nuclear divisionwithout
and Peranemidae,Anisonemidae,or Heteronem- cytoplasmicdivision may occur, so that either
idae) or sometimesfourwhen a separate family mononucleatedor plasmodialpalmellastagesmay
is created forthe genus Colacium (Smith,1933). result. The plasmodialstages give rise to monoDoflcinand Reichenow(1928-1929)combinedthe nucleateflagellatesby budding. Flagellatestages
familiesEuglenidaeand Astasiidaeon the basis of may also arise directlyfroma dividingmononubut his combinationhas cleate palmellacell. The flagellatehas a stigma,
the type of symmetry,
withoutbifurcation
beenseverelycriticized(Hall and Jahn,1929a)and a gullet,and a singleflagellum
swelling(Fig. 4, 9a). Division
is not adopted by recentinvestigators. Calkins but witha flagellar
(1933), in a bold but vain attemptto separate does not occur in the flagellatedstage, and the
all ofthe colorless flagellatemay develop intoeithera palmella or a
plantsfromanimals,reclassified
euglenoidsamong the animal flagellates(Proto- stalked colony. In developinginto the stalked
monadida) solely on the basis of absence of formthe anteriorend of the flagellatebecomes
chlorophyll.This schemealso has been criticized attached,the flagellumis lost, and a gelatinous
(Hall, 1934; Jahnand McKibben, 1937; Hyman, coveringis secreted. The stalk results froma
moreprofusesecretionat the anteriorend. The
1938) and generallydiscarded.
dichotomousbranchingof the dendroid colony
Euglenidae
resultsfromlongitudidaldivisionand thesecretion
The familyEuglenidae consistsof the chloro- of morestalk by each daughtercell.
phyll-bearingspecies and thcse which are imAstasiidaeand Peranemidae
mediatelyderivedfromthem. All membersofthe
The
colorless
euglenoids(otherthanthoselisted
the
all
of
and
familypossess a flagellarswelling
flagellum. above) are ordinarilydividedintotwo families:1)
generahave a bifurcated
monoflagellate
Most of the colorlessspeciesposscssa stigmaand the Astasiidae and 2) the Peraremidae,Heterocounterparts demidae or Anisonemidae. Various criteriafor
differfromtheirchlorophyll-bearing
inwhich was separatingthe familiesare used by different
of
chlorophyll,
only in the absence
265
and none of themis completelysatisThe typeof flagelluminsertionis characteristic
vestigators,
factory. Some possiblecriteriaare: typeof loco- forthefamiliesEuglenidaeand Colaciidae,but the
motion,the Astasiidae being consideredas free only clue to the separationof the genus Astasia
swimmingand rotatingand the Peranemidaeas fromtheothercolorlessformsis theobservationby
Astasiidaebeingsaprozoic,Per- Lackey (1934a) ofa bifurcation.This has notyet
gliding;nutrition,
anemidae holozoic; pharyngealrods, absent in been confirmed
and certainlycan not be used as a
Astasiidae,present in Peranemidae; number of convenientfamilycharacter.
The pharyngealrodapparatusis easilyidentified
flagella,one in Astasiidae,two in Peranemidae;
radial in Astasiidae,bilateralin in Peranema,Heteronema
and Entosiphon,but is
typeofsymmetry,
Peranemidae;the type of flagelluminsertion,dis- not so easily seen in other genera (e.g., Petalocussed above. Certain organisms have been monas),and, therefore,
does not seem veryuseful
placed in either family, depending upon the as a familycharacteristic.
chosen.
The criterion
ofsymmetry
used by Lemmeiman
particularcriterion
If we accept Peranemaas the typegenusforthe (1913) forseparatingthe Astasiidaefromthe Persecondfamilywe thenhave a typegenuswhichis anemidaeis apparentlyuseless. Many speciesare
holozic,normallymovesby gliding,and possesses better described as asymmetrical. The genus
two flagellaand a pharyngealrodapparatus. This Rhabdomonas
differs
fromMenoidiumonlyin that
organismis the most commonand best knownof thecellsare cylindrical
in crosssectionratherthan
thefamilyPeranemidaeand is easilydistinguished flattened(Pringsheim,
1942); thesegeneraare obfromall generaof the Astasiidae. For theseand viouslycloselyrelatedand shouldnot be placed in
also forhistoricalreasons(Hall, 1934; cf.Lackey, separatefamilies.
If we defineholozoicnutrition
1934b) it seems to be the best choice fora type
as a characteristic
is in choosinga of the Peranemidaewe have a characterwhichis
genus. The only real difficulty
suitable criterionforseparatingthe Peranemidae easilyobservablein somegenera,but not so easily
fromthe Astasiidaein such a way that confusion observedinthesmallgenerawhichmayingestbacand teria only a few at a time. Lemmerman(1913)
ofgenerawillbe at a minimum
in identification
that phylogeneticrelationshipswill seem most lists the followinggeneraas holozoic: Peranema,
probable.
Euglenopsis,Urceolus,Petalomonas,Scytomonas,
The abilityto glideor creepby meansoflimited Heteronema,Tropidoscyphus,
Notosolenus,Anisoofmost nema,Entosiphon(cf.Lackey, 1929a) and Dinema.
is equallycharacteristic
movement
flagellar
other genera of the Peranemidae as it is of The only othergenus includedin the familywas
in whichthemodeofnutrition
Peranemaand couldpossiblybe usedas a criterion, Marsupiogaster,
was
in the unknown. In manycases themodeofnutrition
therebyplacingDistigmaand Sphenomonas
is
Peranemidae. Althoughall of the Peranemidae not easilydetermined
by observation.
are apparentlycapable ofglidingmovement,some
It seemsas ifanyofthesecriteriawillgiveriseto
of themmayrotateas theyswim(evenPeranema). both practical and theoreticaldifficulties,
and
generathatare whichgroupofevils willbe theleast is a matterof
Thereare severalmonoflagellate
assignedto the Astasiidaebecause theyare mono- conjecture. One way out of the dilemmawould
flagellateor to the Peranemidaefor some other be to have onlyone colorlessfamilyinsteadoftwo,
reason (Petalomonas,Urceolus,Scytomonas,and but this would resultin an unusual diversityof
Peranemopsis). In- typeswithinthe family.
Clautriavia,Triangulomonas,
asmuchas the second flagellumin the large and
TAXONOMITCSURVEYS
verycommonPeranemaremainedundetectedforso
The latest monographswhich list all known
many years it seems quite possiblethat some of
these may prove to be biflagellate. However, speciesof the euglenoidsare thoseof Lemmerman
whichgenerawerebi- (1913) and Walton (1915). More recent taxoeven if we knewdefinitely
flagellateit would not seem practical to sepa- nomic surveyshave been limitedto one genus.
on greengenera,
rate the familieson the basis of the numberof Thereare severallongmonographs
flagellawhen in some generaone flagellumis or- but thereis no completetreatmentof the genus
species and eleven
dinarilynot detectedeven by carefulobservation. Euglena. However,forty-one
The use of Heteronema(Calkins, 1926; Lackey, varietiesare describedby Johnson(1944), and
are givenby Drezepolski
1934a) or Anisonema(Kudo, 1939) as the type otherusefuldescriptions
(1925), Mainx (1926, 1928), Gunther(1928), and
genusdoesnothelpthesituation.
266
THE QUARTERLY REVIEW OF BIOLOGY
Szabados (1936). The more commonspecies of groovesfor the flagella,which he consideredto
Phacus are describedby Allegreand Jahn(1943), indicate a relationshipto the dinoflagellates.
and all knownspecies by Pochmann (1942) and Chadefaud also discussed phylogeneticrelationSkvortzow (1928). A complete survey of the shipswithinthe order. Schiller(1925) has placed
genusLepocincliswas publishedby Conrad (1934, twogreenmarinestigmategenerawithouta gullet
was surveyedby amongtheeuglenoids,and it seemspossiblethata
1935). The genusTracielomonas
Deflandre (1926, 1926-1927, 1927) and also by furtherinvestigationof the cytologyof the
Skvortzow(1925, 1926), and certain taxonomic generamightshed lighton the phylogenetic
relaproblemswere discussed by Gordienko (1929). tionshipsofthegroup. Senn (1900) pointedout a
Deflandre(1930) createdthe genusStrombomonaspossiblerelationship
withthe Chloromonadida
be(Tracielomonaspro parte)and describedall the cause of the gulletand typeof flagellum
insertion.
knownspecies (cf. Balech and Dastugue, 1938). The phylogenyof the Euglenidae,especiallythe
The green genera Eutreptiella(= Gymnastica relationshipof amoeboid to rigidspecies, is disand Chloranima(=
cussed by Elenkin (1924a, 1924b) and Mainx
Pascher, 1927), Chlorachne,
Ottonia,Strand,1928) were describedby Schiller~ (1928). The genus Colaciurn,because of the pre(1925), and Euglenocapsaby Steinecke (1932). dominanceof palmellaand stalkedstages,may be
is usually includedin Eu- consideredmore closelyrelatedto thealgae than
The genus Amblyophis
glena(cf.,Bhatia,1930),andthegenusAmphitropis other membersof the familyEuglenidae. This
(Gicklhorn,1920) is apparentlya Phytomonad idea is strengthened
by the factthat the flagellum
insertionis of the type postulated by Lackey
(Chodat,1925).
on thecolor- (1934a) for the hypotheticalancestraleuglenoid
Thereare no extensivemonographs
studiedspecies (Fig. 4, 9a), but it mustalso be fittedintothecomless genera. A numberofcarefully
and Rhabdomonas monconceptthatthe algae have evolvedfromthe
ofAstasia,Distigma,Menoidium,
(= Menoidiumpro parte)are describedby Pring- flagellates. Most of the euglenoidsare so specialsheim (1936, 1942), and a key to the genus ized that thereare no clear lines of development
Peranemais givenby van Oye (1926). Two new eitherto or fromalgal or otherflagellategroups.
and Peranemopsis)were Aftera ratherextensiveconsideration
genera (Triangulomonas
of the subdescribedby Lackey (1940a), and the morecom- ject, Fritsch(1929, 1935) carefullyrefrainedfrom
mon species of Petalomonasare described by drawingconclusionson the phylogenetic
relationships.
Shawhan and Jahn (1946).
It is generallyassumedthatthe colorlessspecies
The numberofspeciesthathave been described
for some genera is surprisingly
large. In many arose fromthe greenones by loss of chlorophyll
are small,and someof (Pringsheim,1937, 1941) and that some of the
cases thespecificdifferences
the newerspecies will eventuallybe reduced to colorlessformseventuallybecameholozoic. Howsynonymy. Yet thereare newspeciescontinually ever, the reportby Mast and Pace (1933) that
nutritionoccurs in Chilomonas
beingdescribedwhichare quitedistinctfromany- chemoautotrophic
thingin the literatureand whichapparentlywill and thediscoveryby Schoenborn(1940) thatheternot becomesynonyms. The only way to be cer- oautotrophicnutritionoccursin Astasia makes it
tain that minordifferences
are geneticis to main- seem possiblethat some primitivecolorlessflageltain all knownspeciesin pureculture. So farthis lates mighthave existed beforethe chlorophyllifone assumesthat
methodis impracticable,but its value has been bearingspecies. Furthermore,
discussedby Lefevre (1931), Pringsheim(1941), thegreenspeciesoccurredfirst,
thentheonlynecesand others. The extensivecollectionsof Pring- sity fora foodstuff
whichwas introducedby the
sheimand R. P. Hall are a step in thisdirection.
loss of chlorophyllwas that of acetate or some
similarsimple compound(see nutrition,above).
PHYLOGENY
The problemof adaptationto the loss of chloroseem reticentto discussthe phyllwas apparentlya simpleone. Indeed,some
Most investigators
possiblephylogenyof the euglenoidsand theirre- of the greenspecies of Euglena (E. deses,and E.
lationshipwith otherflagellatesor algae. How- pisciformis)are no longerable to use inorganic
ever, Chadefaud (1936, 1937, 1938) pointed out nitrogencompoundsand are in this respectmore
that they possess certain cytoplasmicstructures dependenton otherorganismsthanis Astasia (dis(see mucus bodies, above), and in some cases cussionsby Schoenborn,1940; Hall, 1941a).
Addenda
a monograph
Aftertheabove articlewas written,
by AndreHollande, entitled"Etude cytologique
et biologiquede quelques flagelleslibres (Volvocales, Cryptomonadines,
Eugl6niens,Protomastigines)," (Arch.Zool. exp. gen., 83: 1-268. 1942)
whichcontainsabout one hundredpages on the
euglenoids,became available in this country.
Hollande's monographcontainsa detaileddiscussion of mitosisand cytoplasmicinclusionsbased
largely on his own observations. He offersa
of the bifurcation
of the flagellumof
confirmation
Astasia and the theorythat thismode offlagellar
insertionwas derivedby regressionfromthat of
267
Euglena (cf. Lackey, above). The paper also
offivenew speciesofPetalocontainsdescriptions
monas.
HarleyP. Brown(On thestructure
and mechanics of the protozoanflagellum,
Ohio J. Sci., 45:
247-278. 1945) by use of the electronmicroscope
has confirmedthe existenceof mastigonemeson
the eugienoidflagellumand has pointedout that
the coreoftheflagellum
ofEuglenaand ofAstasia
is double. This latter observationfitsinto the
idea thattheflagellaofbothgeneraare bifurcated.
Brown also substantiatesLowndes' theorythat
forwardmovementis largelya resultof gyration
ratherthan of a directforwardcomponentfrom
the flagellum.
LIST OF LITERATURE
ALEXANDER,GORDON. 1931. The significance of
hydrogenion concentrationin the biology of
Euglena gracilisKlebs. Biol. Bull., 61: 165-184.
ALLEGRE, C. F., and JARN, T. L. 1943. A survey
of the genus Phacus Dujardin (Protozoa;
Euglenoidina). Trans. Amer. micr. Soc., 62:
233-244.
BAAS-BECKING,
LOURENS G. M., and Ross, P. A.
1926. Notes on microspectra. I. The absorptionspectrumof Euglena. J. Gen. Physiol.,
9: 111-114.
BAKER, C. L. 1933. Studies on the cytoplasmic
components of Euglena gracilis Klebs. Arch.
80: 434-468.
Protistenk.,
BAKER, J. R. 1944. The structureand chemical
composition of the Golgi element. Quart. J.
micr.Sci., 85: 1-71.
BAKER,W. B. 1926 Studies on the life historyof
Euglena. I. E. agilis Carter. Biol. Bull., 51:
321-362.
BAIECH,
E., and DASTUGUE, C. 1938. Nota
preliminar sobre "Strombomomas"y "Trachelomonas." Physis, B. Aires, 12: 354-357.
BANCROFT,F. W. 1913. Heliotropism,differential
sensibility and galvanotropism in Euglena.
J. exp. Zool., 15: 383-428.
BARKER, D. 1943. Recent work on flagellarmovement. New Phytol.,42: 49-53.
BEAMS,H. W., and KING, R. L. 1935. The effect
on the cells of the root tip of
of ultracentrifuging
the bean (Phaseolus vulgaris). Proc. roy. Soc.,
B., 118: 264-276.
BELAi, K. 1926. Der Formwechselder Protistenkerne. Ergebn. Fortschr.Zool., 6: 235-654.
BHATIA, B. L. 1930. On some freshwaterrhizopods
and flagellatesfromKashmir. Arch.Protistenk.,
72: 359-364.
BIEcHELER, B. 1937. Sur l'existence d'une copulation chez une euglene verte et sur les con-
ditionsglobalesqui la d6terminent.C. R. Soc.
Biol. Paris,124: 1264-1266.
BRACHER,R. 1919. Observations
on EIuglena
deses.
Ann.Bot.,33: 93-108.
. 1929. The ecologyof the Avon banks at
Bristol. J. Ecol.,17: 35-81.
BRADLEY,W. H. 1929. Freshwateralgae fromthe
Green River formation of Colorado. Bull.
Torrey
bot.Club,56: 421-428.
1935. Der Stoffwechsel
der Protozoen. Ergebn.
Biol.,12: 161-220.
. 1944. Occurrence
of anerobiosisamong invertebrates.Biodynamica,
4: 185-328.
BRISCOE,M. S. 1939. A sourceoi Euglena. Trans.
Amer.micr.Soc.,58: 374.
BROWN,V. E. 1930a. Cytologyand binaryfission
of Peranema. Quart.J. micr.Sci., N. S., 73:
VON BRAND, T.
403-419.
. 1930b. Cytoplasmicinclusionsof Euglena
gracilisKlebs. Z. Zellforsch.
mikr.Anat., 11:
244-254.
1906. Beitrage zur Kenntnis des
Paramylons. Arch. Protistenk.,7: 197-228.
CALKINS, G. N. 1926, 1933. The biologyof the
BfiTSCHLI, 0.
Protozoa.Lea and Febiger,Philadelphia. 1926,
623pp.; 1933,XI + 607pp.
CARTER,N. 1933. A comparativestudy of the
algal flora of two salt marshes. II.
21: 128-208.
J. Ecol.,
. 1937. Neworinteresting
algaefrombrackish
water. Arch.Protistenk.,
90: 1-68.
CAUSEY, D. 1926. Mitochondria
in Euglenagracilis
Klebs. Univ. Colo. Publ. Zool., 28: 217-224.
CHADEFAUD, M.
1936. Protistes trichocystiferes
ou Protogastr6ades.
Ann. Protist.,Paris, 5:
323-341.
-.
1937. Anatomiecompareedes Eugleniens.
Botaniste,
Ser.28,pp 85-185.
268
M. 1938. Nouvelles recherchessur
des Eugl6niens:les PeraneI'anatomiecompar6e
. 1930. Strombomonas,
nouveau genre d'Euglenacees (Trackelomonas Ehrb. pro. parte).
Arch.Protistenk.,69: 551-614.
CHADEFAUD,
mines .Rev.Algol.,11: 189-220.
. 1939. Sur l'organisationd'Euglena stellata
des Euglenes
Mainx et sur la discrimination
.
1931. Sur la structure
de la membrane
chez
quelques Phacus. Ann. Protist.,Paris, 3: 41-43.
. 1932. Contributions
a la connaissancedes
viridoides. Arch. Zool. exp. gen., Paris, 80:
49-54.
Flagelles libres. I. Ann. Protist.,Paris, 3: 219-
sexuelschez les Euglen. 1940. Ph6nom6mes
iens. Rev.Sci., 78: 179-180.
CHADEFAUD,M., and PROVASOLI,L. 1939. Une
nouvelle Eugl6ne graciloide;Euglena gracilis
246.
1934a. Sur I'abus de 1'emploi,
en paleontologie du nomde genreTrachelomonas
et sur la
naturede quelquesex "Trachelomonos"
siliceux
(Chrysomonadines)
tertiaireset quaternaires.
-.
Klebs var. urophora n. var. Arch. Zool. exp.
gen.,Paris, 80: 55-60.
faitesa la Linnaea
CHODAT,R. 1925. Observations
1923-1925. Bull. Soc. bot.Geneve,17: 180-251.
-.
W. 1934. Materiauxpour une MonoCONRAD,
graphie du genre Lepocinclis Perty. Arch.
Protistenk.,82: 203-249.
Ann. Protist.,Paris, 4: 151-165.
1934b. Sur les proprietes
optiquesdu paramylon (Variations de l'anisotropie).Butl.
biol.,68: 382-384.
. 1934c. Sur la structuredes flagelles. Ann.
Protist.,Paris, 4: 31-54.
du genreLepocin1935. Etudesystematique
-
clis Perty. Mem. Mus. Hist. nat. Belg., 1: 1-84.
COWDRY, E. V. 1943. Microscopic technique in
Biology and Medicine. Williams & Wilkins,
. 1934d. Existencesur les flagellesde filamentslaterauxau terminaux
(mastigonemes).
C. R. Acad. Sci., Paris, 198: 497-499.
. 1935. Trackelomonas,Archaemonadacees et
Baltimore.206pp.
Chrysostomatace6s.
Responsea une note de
1928. Morphologieund Physiologie
J. Frenguelli.Arch. Protistenk.,
85: 306-311.
Beih. bot. Zbl., 45: DELLINGER,0. P. 1909. The ciliumas a keyto the
des Algenstairkekornes.
97-270.
structure
of contractile
protoplasm.J. Morph.,
VON DACH, H. 1940. Factors which affectthe
20: 171-209.
growth of a colorless flagellate,Astasia klebsii, DOBELL, C. C. 1908. The structure
andlifehistory
in pure cultures. Ohio J. Sci., 40: 37-48.
of Copromonas,
nov. gen.,nov. spec.: a contribution to our knowledgeof the Flagellata.
. 1942. Respiration of a colorless flagellate,
CZURDA. V.
Astasia klebsii. Biol. Bull., 82: 356-371.
.
Quart.J. micr.Sci., 52: 75-120.
DOFLEIN, F., and RxICHENOW, E. 1928-1929.
Lekrbuchder Protozoenkunde.Gustav Fischer,
1943. The effectof pH on pure culturesof
Euglena mutabilis. Ohio J. Sci., 43: 47-48.
surlesEugleniens.
P. 1902. Recherches
DANGEARD,
Jena.1262pp.
Botaniste,8: 7-370.
DoYLE, W. L. 1943. The nutritionof the pro-
-
-.
-.
. 1928a. L'appareilmucifere
etle vacuomechez
les Eugleniens. Ann. Protist., Paris, 1: 69-74.
des mouvements
1928b. Le determinisme
chez les organismesinferieurs.Ann. Protist.,
Paris, 1: 3-10.
1933. Trait6 d'Algologie. Paul Lechevalier,
Paris. 441pp.
studyof the
DANIELS, M. I. 1938. A cytological
gregarineparasites of Tenebriomolitor,using the
ultracentrifuge.Quart.J. micr.Sci., 80: 293-320.
TraDEFLANDRE, G. 1926. Monographiedu gentre
chelomonasEhr. Nemours. 162 pp.
-.
1926-1927. Monographiedu genre Trachelomonas Ehr. 1926, 38: 358-380, 449-469, 518528, 580-592, 646-658, 687-706; 1927, 39: 26-51,
73-98.
-.
1927. Remarques sur la systematique du.
genre TrachelornonasEhr. Bull. Soc. bot. Fr.
74: 285-287, 657-665.
1929. Observations sur les mouvements
-.
propres, pistes et vitesses de deplacement de
quelques Protistes. Ann. Protist.,Paris, 2: 1-40.
tozoa. Biol.Rev.,18: 119-136.
1925. Supplement
A la connaisance des Eugl6niensde la Pologne(Polishwith
Frenchsummary).Kosmos,Lwow,50: 173-270.
. 1929. L'evolutiondu noyauet son r6lechez
DREZEPOLSKI,R.
les Eugl6nes. Ann. Protist.,Paris, 2: 109-118.
DUBoscQ,and GRASSf, P.
1933. L'appareil pa-
rabasal des flagelles. Arch. Zool. exp. gen.,
73: 3816-21.
DUFRENOY,J. 1940. On the physiological
significance of the vacuome. Biodynamica,3: 171-190.
DUNHAM, D. W. 1937. The flagella of Peranemna.
Science,85: 206.
en
Dusi, H. 1930. Limites de la concentration
ions H pour la culturede quelquesEuglenes.
C. R. Soc. Biol. Paris, 104: 734-736.
sineflagelloELENKIN,A. A. 1924a. De Euglenarum
sectione nova. Not. syst. Inst. crypt.Hort. Bot.
Reip. Rossic, 3: 124-160.
. 1924b. Ueber die Stellungder cilienlosen
Sektion(Amastigatae)im SystemderEuglenen.
Not. syst. Inst. crypt.Hort. Bot. Reip. Rossic,
3: 161-170.
269
ELLIOTT,A. M. 1937. Plant hormonesand growth -.
1939. Some observations in Euglena sanof Euglena in relation to light. Anat. Rec.,
guinea Ehrbg. Trans. Amer. micr. Soc., 58:
70 (Suppl.): 128.
241-248.
. 1938. The influence of certain plant hor- VAN GOOR, A. C. J. 1925. Die Euglenineae des
mones on growth of Protozoa. Physiol. Zool.,
Hollandischen Brackwassers mit besonderer
11:31-39.
Beruicksichtigungihrer Chromatophoren. Rec.
ELMORE, M. E. 1928a. Antigenic properties of
Trav. Bot. Neerl., 22: 292-314.
Euglena gracilis. J. Immunol., 15: 21-32.
GORDIENKO, M. 1929. Zur Frage der Systematik
. 1928b. The production of anaphylaxis with
der Gattung TrachelomonasEhrenberg. Arch.
Euglena gracilis and other unicellular chlorProtistenk.,
65: 258-267.
ophyll-bearing organisms. J. Immunol., 15: GRASSP, P. P. 1925. Le vacuome et l'appareil de
33-36.
Golgi des Euglenes. C. R. Acad. Sci., Paris
ENGELMANN, T. W. 1882. Ueber Licht- und
181: 482-484.
FarbenperceptionniedersterOrganismen. Arch.
. 1926. Sur le stigma ou appareil parabasal des
ges. Physiol.,28: 387-400.
Euglenes. C. R. Soc. Biol., Paris, 94: 1012-1014.
FAIR, G. M., and WHIPPLE, M. C. 1927. The
and POISSON, R. 1933. Nouvelles obser,
ofdrinkingwater. By G. C. Whipple.
microscopy
vations sur la cytologie des Eugldnes. C.
John Wiley and Sons, New York, 4th ed.
R. Soc. Biol., Paris, 114: 662-666.
FINLEY, H. E. 1930. Toleration of fresh water GUILLIERMOND,
A., and ATKINSON, L. R. 1941.
protozoa to increased salinity. Ecology, 11:
The cytopiasmof theplant cell. Chronica Botan337-347.
ica, Waltham,Mass.
FISCHER, A. 1894. Ueber die Geisseln einiger GiTNTHER, FRANZ.
1928. Uber den Bau und die
Flagellaten. J. wiss. Bot., 26: 187-235.
Lebensweise der Euglenen, besonders der Arten
FRASER, J. H. 1932. Observations on the fauna
E. terricola,geniculata,proxima,sanguinea, und
and constituentsof an estuarine mud in a pollucens nov. spec. Arch.Protistenk.,
60: 511-590.
luted area. J. Marine biol. Ass. Unit. King., HAASE, G. 1910. Studien uiberEuglena sanguinea.
18: 69-85.
Arch.Protistenk.,
20: 47-59.
FRITSCH,F. E. 1929. Evolutionary sequence and HALL, R. P. 1923. Morphologyand binary fission
affinities among Protophyta. Biol. Rev., 4:
of Menoidium incurvum(Fres.) Klebs. Univ.
103-151.
Colo. Publ. Zool., 20: 447-476.
. 1935. The structureand reproductionof the
. 1929. Reaction of certain cytoplasmic inalgae. Vol. I. Macmillan Company,New York
clusions to vital dyes and their relation to
and London. + 791 pp.
mitochondriaand Golgi apparatus in the flagelGARCIN, A. 1889. Sur le pigment de 1'Euglena
late Peranema trichopkorum.J. Morph., 48:
sanguinea. J. Bot., 3: 189-194.
105-122.
GARD, M. 1922. Recherches sur une nouvelle
. 1930. Osmiphilicinclusions similar to Golgi
espece d'Euglene (Euglena limosa, nov. sp.).
apparatus in the flagellates,Chromulina,ChiloBull. Soc. bot.Fr., 69: 184-196,241-250, 306-313.
monas and Astasia. Arch.Protistenk,
69: 7-22.
GATENBY, J. B., and SINGH, B. N. 1938. Golgi
. 1931. Cytoplasmic inclusions of Menoidium
apparatus of Copromonassubtilis and Eugiena
and Euglena, with special referenceto the vacusp. Quart. J. micr. Sci., 80: 567-591.
ome and Golgi apparatus in euglenoidflagellates.
GATENBY, J. B., SINGH, B. N., and BROWNE, K. M. R.
Ann. Protist.,Paris, 3: 57-68.
1938. Further notes on the association be. 1933a. On the relation of hydrogen-ion
tween Golgi apparatus and the vacuole systemin
concentrationto the growthof Euglena anabaena
Euglena and Copromonas.Cellule, 47: 227-236.
var. minorand E. deses. Arch. Protistenk.,79:
GATENBY, J.B., and SMYTH,J.D. 1940. The Golgi
239-248.
apparatus and pyrenoids of Chilomonas para. 1933b. The methodof ingestionin Peranema
meciumwith remarks on the identificationof
and its bearing on the pharyngeal
trichophorum
Copromonassubtilis. Quart. J. micr.-Sci., 81:
rod ("Staborgan") problem in the Euglenida.
595-617.
81: 308-317.
Arch.Protistenk.,
GICKLEORN,J. 1920. Ueber eine neue Euglenacee
-.
1933c. The question of the ingestion of
(Amphitropisaequiciliata nov. gen. et spec.).
solid particles by Euglena. Trans. Amer. micr.
Oesterr.bot.Z. 69: 193-199.
Soc., 52: 220-222.
GIMESI, N. 1930. Die Geburt von Trachelomonas
-.
1934. A note on the flagellarapparatus of
volvocinaEhrbg. Arch.Protistenk.,72: 190-197.
and the status of the
Peranema
trichophorum
and
cell
The
M.
1934.
morphology
GOJDICS,
family Peranemidae Stein. Trans. Amer. micr.
division of Euglena deses Ehrbg. Trans. Amer.
Soc., 53: 237-243.
micr.Soc., 53: 299-310.
270
R. P. 1936. Cytoplasmic
inclusions
ofPhyto- HASSETT,C. C. 1944. Photodynamic
actionin the
mastigoda. Bot.Rev.,2: 85-94.
flagellate Peranema trichoPhorumwith special
. 1937a. A note on behaviorof the chromoreferenceto motor response to light. Physiol.
HALL,
somes in Euglena. Trans. Amer. micr. Soc.,
Zool., 17: 270-277.
1930. Ueber den Exkretionsapparatbei
den Protozoen, nebst Bemerkungenuibereinige
56: 288-290.
. 1937b. Certainculturereactionsot several
HAYE, A.
andere feinereStrukturverhaltnisse
der un-
species of Euglenidae. Trans. Amer. micr. Soc.,
56: 285-287.
. 1937a. Growthof freeliving Protozoa in
tersuchten Arten. Arch. Protistenk.,70: 1-87.
HEIDT,
pure cultures. In CultureMethodsfor Inverte-
K. 1934. Hamatochromwanderung
bei Eu-
glena sanguinea Ehbg., Ber. dtsck. bot. Ges.,
brateAnimals,ed., J.G. Needham. Comstock
52: 607-613.
Pub. Co. Ithaca,N. Y.
. 1937. Form und Strukturder Paramylonkor. 1939. The trophicnatureof the plant-like
ner von Euglena sanguinea (Ehrb.). Arch.
flagellates. Quart. Rev. Biol., 14: 1-12.
Protistenk.,
88: 127-142.
- %
.1941a. Food requirements
and otherfactors HIBBARD, H. 1945. Currentstatusofourknowledge
influencing
growthof Protozoain purecultures.
of the Golgi apparatus in the animal cell. Quart.
In Protozoain Biological Research,eds., Calkins
Rev.Biol., 20: 1-19.
andSummers.Columbia
Univ.Press,NewYork. HIRSCH, G. C. 1939. Form und Stofweckselder
---. 1941b. Populationsof plant-likeflagellates.
Golgi-Kdrper. ProtoplasmaMonog., 18: 394 pp.
Amer.Nat., 75: 419-437.
HOLLANDE, A. 1938. Les dictyosomesdes eugl6n1943. Growth-factors
forProtozoa. In Viiens. C. R. Soc. Biol. Paris, 127: 517-518.
tamins and Hormones,eds., R. S. Harris and
1940. Le chondriomedes Eugleniens et des
K. V. Thimann. AcademicPress,N. Y.
Cryptomonadines. C. R. Acad. Sci., Paris,
HALL, R. P., and JAHN, T. L. 1929a. On the
210: 317-319.
comparativecytology of certain euglenoid HYMAN, L. H. 1936. Observations on protozoa.
flagellatesand the systematicpositionof the
familiesEuglenidaeSteinand AstasiidaeBtits-
-
I. The impermanence
ofthecontractile
vacuole
chli. Trans. Amer. micr. Soc., 48: 388-405.
%
.1929b.
Dispersedstages of the stigmain
Euglena. Science, 69: 522.
HALL,
R. P., and NIGRELLI, R. F. 1937. A note
on the vacuome of Paramecium bursaria and
thecontractile
vacuoleofcertainciliates. Trans.
Amer.mnicr.
Soc., 56:185-190.
R. P., and POWELL, W. N. 1927. A noteon
the morphologyand taxonomicposition of
HALL,
-.
in Amoebavespertilio.
II. Structureand mode of
foodingestionin Peranema. Quart.J. micr.Sci.,
79: 43-56.
1937. Peranema and "Grantia." Science,
85: 454.
1938. Observations
on Protozoa. III. The
vacuolarsystemof the Euglenida. Beik. bot.
Zbl.,58A:379-382.
IVANIc, M. 1935. Zur Kenntnisder rhizopodialen
-.
Nahrungsaufnahmebei Peranema trichiophorum
Stein. Zool. Anz., 109: 19-23.
46: 155-165.
. 1928. Morphologyand binary fissionof JAHN,T. L. 1929. Studies on the physiologyof the
euglenoid flagellates. I. The relation of the
Peranematrichophorum
(Ehrb.) Stein. Biol. Bull.
density of population to the growth rate of
54: 36-64.
Euglena. Biol. Bull., 57: 81-106.
HALL, R. P., and SCHOENBORN,H. W. 1939. Fluct. 1930. Studies on the physiologyof the eugleuationsin growthrate of Euglena anabaena,
E. gracilis, and E. viridis, and their apparent
noidflagellates. II. The autocatalyticequation
relationtoinitialdensity
ofpopulation.Physiol.
and the question of an autocatalyst in the
Zool.,12: 201-208.
growth of Euglena. Biol. Bull., 58: 281-287.
on Euglena leucops -.
HALL, S. R. 1931. Observations
1931. Studies on the physiology of the
n. sp., a parasiteof Stenostomum
withspecial
euglenoid flagellates. III. The effect of hyPeranematrichophorum.Trans.Amer.micr.Soc.,
referenceto nuclear division. Biol. Bull.,
60: 327-334.
HAMBURGER,C. 1911. StudienuberEuglena Ekrenuber die Ki5rperhulle.
bergii,insbesondere
S.
B. heidelberg.
Akad. Wiss., 4:1-22.
on the growthof
drogenion concentration
Euglena gracilis Klebs. Biol. Bull., 61: 387-399.
-. 1933a.-Studies on the physiologyof the
euglenoidflagellates.IV. The thermaldeath
HXRDTL,
time of Euglena gracilis. Arch. Protistenk.,79:
glena Ehrenb. Beih. bot. Zbl., A., 53: 606-619. -.
HARTMANN, M., and CHAGAS, C. 1910. Flagellaten-Studien. Mem. Inst. Osw. Cruz., 2: 64-125.
1933b. On certain parasites of Phacus and
Euglena; Sphaerita phaci, sp. nov. Arch.Protistenk., 79: 349-355.
H. 1935. Einigesuberden Bau und die
rotenEuLebensweiseeinerneustonbildenden
249-262.
1934. Problems of population growthin the
Protozoa. Cold Spring Harbor Symp. Quant.
Biol., 2: 167-180.
-.
1935. Studies on the physiology of the
euglenoid flagellates. VI. The effectsof temperature and of acetate on Euglena gracilis
culturesin the dark. Arch.Protistenk.,86: 251257.
. 1941. Respiratorymetabolism. In Protozoa
in BiologicalResearch,eds., Calkinsand Summers.
Columbia Univ. Press, New York.
JAHN, T. L., and McKIBBEN,
W. R. 1937. A
colorless euglenoid flagellate, Khawkinea halli,
n. gen.,n. sp. Trans. Amer.micr.Soc., 56:48-54.
JANDA, V. and JfROVEC, 0. 1937. Ueber kuinstlich
hervorgerufenen
Parasitismus eines freilebenden
Ciliaten Glaucoma piriformisund Infektionsversuche mitEuglenagracilisund Spinockaetabiflexa.
Mem. Soc. Zool. Tchecoslov.Prague, 5: 24 pp.
JENNINGS, H. S. 1904. Contributionsto the study of
the behavioroflowerorganisms. CarnegieInstit.
Wash. Publ., 16. 256 pp.
JENNINGS, H. S. 1906. Behaviorof thelowerorganssms. Columbia Univ. Press, New York. 366
PP.
0. 1926. Protozoenstudien. I. Arch.
JfRovEC,
Protistenk.,
56: 280-289.
. 1929. Die Silberlinien bei einigen Flagellaten. Arch.Protistenk.,68: 209-214.
1934a. Der Einflussvon ultraviolettenStrahlen auf gruineund farbloseStamme von Euglena
gracilis. Protoplasma,21: 577-587.
. 1934b. VorlaufigeMitteilung uber den Einfluss verschiedener Metalle auf Reinkulturen
von Euglena gracilis. Mem. Soc. Zool. Tcldcoslov.Prague, 2: 6 pp.
JfROVEC,O., and VACHA, K. 1934a. Ueber die
Schutzwirkung von Germanin gegen photodynamischeSchadigung und ultravioletteStrahlen. Mem. Soc. Zool. Tchecoslov. Prague, 2:
11 pp.
-.
1934b. Photodynamische erscheinungenan
grunen und farblosen Stamm von Euglena
gracilis. Protoplasma,22: 203-208.
JOHNSON,D. F. 1934. Morphologyand lifehistory
of Colacium vesiculosumEhrbg. Arch. Protistenk.,83: 241-263.
1939. A study of Euglena rubra
JOHNSON, L. P.
Hardy 1911. Trans. Amer. mnicr.Soc., 58:
42-48.
. 1942. A peculiar stainingreactionin Euglena
rubra Hardy 1911. Proc. Iowa Acad. Sci., 49:
517-519.
. 1944. Euglenae of Iowa. Trans. Amer.
micr.Soc., 63: 97-135.
1942. Cause of the
JOHNSON, L. P., and JAHN, T. L.
green-redcolor change in Eiuglenarubra. Physiol. Zool., 15: 89-94.
-.
JONES,
271
D. T. 1944. Two protozoansfromGreat
Salt Lake.
Bull.
Univ. Utah. (Biol. Ser.),
35: 11 pp.
KIAHL, A. 1928. Die Infusorien(Ciliata) der
OldesloerSalzwasserstellen.Arch. Hydrobiol.,
19: 50-123.
KIDDER,G. W. 1941. The techniqueand significance of controlin protozoan culture. In
Protozoa in Biological Research, eds., Calkins
andSummers.ColumbiaUniv.Press,NewYork.
R. L. 1935. The contractilevacuole of
KING,
Paramecium multimicronucleata.J. Morph., 58:
555-571.
KIRBY,H. 1941a. Relationshipsbetweencertain
Protozoa and other animals. In Protozoain
Biological Research,eds., Calkins and Summers.
ColumbiaUniv.Press,New York.Pp. 890-1008.
. 1941b. Organisms
livingon or in Protozoa.
In Protozoa in Biological Research,eds., Calkins
and Summers. Columbia Univ. Press, New
York.Pp. 1009-1114.
KIRKMAN, H., and SEVERINGHAUS, A. E. 1938.
A reviewof the Golgiapparatus. Anat. Rec.,
70: 413-432,557-573;71: 79-103.
KLEBS, G. 1883. Uber die Organisationeiniger
Flagellatengruppen
und ihre Beziehungenzu
anderen Infusorien. Untersuch.bot.Inst. Tubin-
gen,1: 233-362.
KLEIN, B. M. 1930. Ueberdas Silberliniensystem
einiger Flagellaten. Arch. Protistenk.,72: 404419.
KOL, E. 1929. "Wasserblute" der Sodateiche auf
der Nagy Magyar Alfold (Grossen Ungarischen
Tiefebene). Arch. Protistenk.,66: 515-522.
A. 1923. Ueber den Bau und die
KORSCEIKOW,
Aggregationder Geisselnbei den Volvocales
und den Flagellaten. Arch.Russ. Protist.,2: 195205.
. 1924. Ueberden Bau und die Aggregation
der Geisselnbei den Volvocalesundden Flagel-
laten. Arch. Russ. Protist.,3: 148-205.
1937. Beitrag zur Kenntnis
der Morphologieund Entwicklungsgeschichte
der
Gattung Euglena und Phacus. Arck. Protistenk.,
90: 88-123.
KUDO, R. R. 1946. Protozoology. C. C. Thomas,
KRICHENBAUER, H.
and Baltimore.
778pp.
Springfield
KUTSCHER, F.
1898. Beitrage zur Kenntnis der
Euglena sanguinea. Z. physiol. Chem., 24:
360-363.
KYLIN,
H. 1927. Ueber die karotinoidenFarb-
stoffeder Algen. Hoppe-Seyl. Z., 166: 39-77.
LACKEY, J. B. 1929a. Studies on the life histories
of Euglenida. I. The cytology of Entosiphon
sulcatum (Duj.) Stein. Arch. Protistenk.,66:
176-200.
-.
ofEuglen1929b. Studiesin the lifehistories
ida. II. The life cycles of Entosiphonsulcatum
272
and Peranema trichophorum.Arch. Protistenk.,
67: 128-156.
LACKEY,J. B. 1932. Oxygendeficiencyand sewage
protozoa: with descriptionsof some new species.
Biol. Bull., 63: 287-295.
-.
1933. Studies in the life history of the
Euglenida. III. The morphologyof Peranema
trichophorum
Ehrenberg,with special reference
to its kinetic elementsand the classificationof
the Heteronemidae. Biol. Bull., 65: 238-248.
. 1934a. Studies in the lifehistoriesof Euglenida. IV. A comparison of the structure and
division of Distigma proteus Ehrenberg and
Astasia dangeardiLemm. A studyin phylogeny.
Biol. Bull., 67: 145-161.
. 1934b. Two new species of Euglenidae and
the position of the order. J. Tenn. Acad. Sci.,
9: 31-33.
. 1936. Occurrence and distribution of the
marine protozoan species in the Woods Hole
area. Biol. Bull., 70: 264-278.
-.
1938a. The floraand fauna of surfacewaters
polluted by acid mine drainage. U. S. Pub.
Health Rep., 53: 1499-1507.
. 1938b. A study of some ecologic factors
affecting the distribution of Protozoa. Ecol.
Monog. Durham,8: 501-527.
. 1939a. Notes on plankton flagellates from
the Scioto River (withdescriptionsofnew forms).
Lloydia, Cincinnati,2: 128-143.
. 1939b. Aquatic life in waters polluted by
acid mine waste. U. S. Pub. Health Rep., 54:
740-746.
. 1940. Some new flagellatesfromthe Woods
Hole area. Amer. Midl. Nat., 23: 463-471.
-.
1940b. The microscopic flora and fauna of
treeholes. OhioJ. Sci., 40: 186-192.
. 1942. The effectsof distillery wastes and
waters on the microscopicfloraand fauna of a
small creek. U. S. Pub. HealthRep.,57: 253-260.
LACKEY, J. B., and SmiTH,R. S. 1940. Limitations
of Euglenidae as polluted water indicators.
U. S. Pub. Health.Rep., 55: 268-280.
LEFEiVRE,M. 1931. De la valeur des caracteres
sp6cifiques chez quelques Eugl6niens. Rec.
Trav. Crypt. dedids d L. Mangin, Paris. Pp.
343-354.
-.
1932a. Sur la structurede la membrane des
Euglenes du groupeSpirogyra. C. R. Acad. Sci.
Paris, 195: 1908-1309.
. 1932b. Sur le d6terminismedes variations
morphologique et ornementales chez quelques
Eugleniens. Ann. Protist., Paris, 3: 201-207.
. 1932c. Recherches sur la biologie et la
syst6matique de quelques algues obtenues en
cultures. Rev. Algol., 6: 313-335.
. 1934. Recherches sur la biologie et la sys-
t6matique de quelques Eugleniens. Rev. Algol.
7: 139-148.
LEMMERMANN, E. 1906. Ueber das Vorkommen
von Stisswasserformenin Phytoplankton des
Meeres. Arch. Hydrobiol.,1: 409-427.
-.
1913. Eugleninae. In Die Siisswasserftora
und der Schweiz,Fischer,
Deutschlands,Osterreich
Jena.2:115-174.
LINDEMAN,R. L. 1942. Experimental simulation
of winter anaerobiosis in a senescent lake.
Ecology, 23: 1-13.
LOEFER, J. B. 1931. Morphology and
binary
fissionof Heteronemaacus (Ehrb) Stein. Arch.
Protistenk.,
74: 449-470.
. 1939. Acclimatizationof freshwater ciliates
and flagellates to media of higher osmotic
pressure. Physiol.Zool., 12: 161-172.
LOWNDES, A. G. 1941. On flagellarmovementin
unicellular organisms. Proc. zool. Soc. Lond.,
lllA: 111-134.
. 1944. The swimmingof unicellularflagellate
organisms. Proc. zool. Soc. Lond., 113A; 99-107.
LWOFF, A. 1933. Die Bedeutung des Blutfarbstoffesfur die parasitischen Flagellaten. Zbl.
Bakt. Abt. (Orig.), 130: 498-518.
LWOFF, A., and Dusi, H. 1935. La suppression
experimentale des chloroplastes chez Euglena
mesnili. C. R. Soc. Biol. Paris, 119:1092-1095.
. 1936. La nutrition de l'Euglenien Astasia
chattoni.C. R. Acad. Sci. Paris, 202: 248-250.
LUND, J. W. G. 1942. The marginalalgae of certain ponds, with special referenceto bottomdeposits. J. Ecol. 30: 245-283.
MAcLENNAN, R. F. 1941. Cytoplasmicinclusions.
In Protozoain Biological Research,ed. by Calkins
York. Pp. 111-190.
MAINX, F. 1926. Einige neue Vertreterder GattungEuglenaEhrb. Arch.Protistenk.,
54:150-160.
. 1928. Beitraigezur Morphologieund Physiologie der Engleninen. Arch. Protistenk.,
60: 305414.
MANGENOT,G. 1926. A propos de la signification
du stigma des Englnes. C. R. Soc. Biol. Paris,
94:577.
MAST, S. 0. 1911. Light and tkebehaviorof organisms. New York, 410 pp.
-.
1917. The relation between spectral color
and stimulationin the lower organisms. J. exp.
Zool. 22: 471-528.
. 1927. Structureand functionof the eyespot
in unicellular and colonial organisms. Arch.
Protistenk.,60: 197-220.
1936. Motor responsesto lightin the invertebrate animals. In BiologicalEffectsofRadiation,
ed. by B. M. Duggar. McGraw-Hill Company,
New York.
. 1941. Motor responsein unicellularanimals.
In Protozoa in Biological Research,Calkins and
Summers,eds. Columbia Univ. Press, New York.
Pp. 271-351.
and DOYLE, S. L. 1935. A new type of
-,
cytoplasmic structure in the flagellate Chilo85: 145monas paramecium. Arch. Protistentk.,
149.
-,
and GOVER, MARY. 1922. Relation between
intensity of light and rate of locomotion in
Phacus pleuronectesand Euglena gracilisand its
bearingon orientation. Biol. Bull., 43: 203-209.
, and PACE, D. M. 1933. Synthesisfrominorganic compounds of starch, fats, proteinsand
protoplasm in the colorless animal Chilomonas
paramecium. Protoplasma,20: 326-358.
MOLISCH, H. 1923. Mikrochemieder Pjlanze. 3rd
Ed. Jena.
NASSONOV,D. 1924. DerExkretionsapparat (kontractileVacuole) der Protozoa als Homologondes
GolgischenApparats der Metazoazellen. Arch.
mikr.Anat., 103: 437-482.
des StisNAUMANN, E. 1922. Die Sestonfarbungen
swassers,etc. Arch.Hydrobiol.,13: 647-692.
VAN OYE, PAUL. 1926. Flagellates du Congo Belge.
Bull. Soc. roy.Bot. Belg., 58: 11-19.
A. 1927. Neue oder wenig bekannte
PASCHER,
Flagellaten XVIII. Arch. Protistenk.,58: 577598.
und phototak1930. Eine neue,stigmatisierte
tische Am6be. Biol. Zbl., 50: 1-7.
1931. Ueber die Verfestigungdes Protoplasten im Gehause einer neuen Euglenine (Kleb73: 315-322.
siella). Arch.Protistenk.,
PATTEN, RUTH, and BEAMS, H. W. 1936. Observaon some
tionson the effectof the ultra-centrifuge
free-livingflagellates. Quart. J. micr. Sci., 78:
615-635.
PETERSEN, J. B. 1929. Beitrage zur Kenntnis der
Flagellatengeisseln. Bot. Tidsskr.,40: 373-389.
POCHMANN,A. 1942. Synopsisder GattungPhacus.
Arck. Protistenk,95: 81-252.
PRINGSIEIM, E. G. 1926. Ueber das Ca-Bedurfnis
einigerAlgen. Planta, 2: 555-568.
. 1935. Ueber Azetatflagellaten. Naturwiss.,
23: 110-114.
-.
1936. Zur Kenntnis saprotroperAlgen und
polyFlagellaten. I. Ueber Anhiaufungskulturen
saprober Flagellaten. Arch.Protistenk.,87: 4396.
. 1937. Ueber das Stigma bei farblosenFlagellaten. Cytologia,Fujii-Festschrift,pp. 324-255.
. 1941. The interrelationshipsof pigmented
and colourless Flagellata. Biol. Rev., 16: 191204.
. 1942. Contributionsto our knowledgeof saprophyticalgae and flagellata. III. Astasia, Dis-
273
tigma,Menoidium,and Rhabdomonas. New Phytol.,41: 171-205.
RATCLIFFE, H. 1927. Mitosis and cell division in
Euglena spirogyra. Biol. Bull., 53: 109-122.
REUKAUF, E. 1940. UeberTrichozystenbei Ziliaten
und aihnlicheGebilde bei Flagellaten. Mikrokosmos,33: 77-80.
RHODES,R. C. 1926. Mouth and feedinghabits of
Heteronemaacus. Anat. Rec., 34 (Suppl.): 152-
153.
RYBINSKY,S. B., and ZRYKINA,L. M. 1935. Ueber
Kernverainderung
bei Euglena gracilis(Ehrbg) bei
chroniicherArsenvergiftung.Arch. Protistenk.,
85: 334-340.
SANDON,H. 1927. The compositionand distribution
of the protozoanfauna of the soil. Oliver and
Boyd, London, xv + 237 pp.
SANDS, W. N. 1934. The coloured scums of padi
fields. Malay. agric.1., 22: 484.
SAUER, M. E. 1935a. The cytotoxic principle in
anti-euglena rabbit serum. J. Immunol., 29:
157-164.
. 1935b. Correlation of immunologic and
physiologic types of Euglena gracilis Klebs.
Arch. Protistenk.,85: 412-415.
SCMLLER,
J. 1925. Die planktonischen Vegetationen des adriatischenMeeres. B. Chrysomonadina, Heterokontae,Cryptomonadina,Eugleniae, Volvocales. Arch. Protistenk.,53: 49-123.
H. W. 1936. Growthof two species
SCHO,NBORN,
ofAstasia in relationto pH ofthemedium. Anal.
Rec., 67 (Suppl.): 121.
. 1940. Studies on the nutritionof colorless
euglenoid flagellates. I. Utilization of inorganic nitrogenby Astasia in pure cultures. Ann.
N. Y. Acad. Sci., 40:1-36.
. 1942. Studies on the nutritionalrequirements
of Euglena gracilis in darkness. Physiol. Zool.,
15:325-332.
SCHRODER, V. N. 1927. Influence of electrolytes
of potentialof the cell wall in
upon the difference
Euglena ehrenbergii.(In Russian). Proc. 2nd
Cong. Zool. Anat. Histol. U.S.S.R., 167-168.
SENIOR-WHITE,R. 1928. Physical factorsin mosquito ecology. II. Ind. J. med. Res., 16: 11-30.
SENN,G. 1900. Eugleninae,in Naturl.Pftanzenfam.
1st ed. 1, la, pp. 173-185.
F. M., and JAHN,T. L. 1946. A studyof
SHAWHAN,
the genus Petalomonas. (In press)
SHORTESS,G. S. 1942. The relation between temperature, light, and rate of locomotion in Peranema trichopkorum
and response to changes in
temperature. Physiol. Zool., 15: 184-195.
SIGOT,A. 1931. Existencede plaquettesosmiophiles
periflagellaireschez Euglena gracilis Klebs; leur
valeur cytologique. C. R. Soc. Biol. Paris, 106:
1069-1072.
274
SINGE,J. 1941. Soil algae ofLahore. Current
Sci.,
TANZER, C. 1941. Serologicalstudieswith free10:29-30.
Bangalore,
42: 291-312.
livingProtista. J. Immunol.,
SKVORTZOW, B. W. 1925. Die EuglenaceengattungTCEAKHOTINE,S. 1936a. La fonctiondu stigma
Ehrenberg.Eine systematische
Trachelomonas
Euglena,etudi6eau moyende la
chezle flagell6
Reck.Biol. Sta., 1:
Ubersicht.Tr. Sungariiskoe
ultraviolette.C. R. Soc. Biol.
micropuncture
1-101.
Paris,121: 1162-1165.
. 1926. Ueberneue und wenigbekannteForobjetsd'experiences
. 1936b. Les Protozoaires,
EhTrachelomonas
menderEuglenaceengattung
faites
en Cytologieexperimentale.(Recherches
renb.II. Ber.dtsch.bot.Ges.,44: 603-621.
ultraviolette).Ann.Proavec la micropuncture
PhacusDu. 1928. Die Englenaceeangattung
tist.,5: 1-57.
jardin. Ber. dtsch.bot.Ges.,46: 105-125.
TERNETZ,CHARLOTTE. 1912. Beitragezur Morphoalgae of the
G. M. 1933. The fresh-water
SmiTHr,
logie und Physiologieder Euglena gracilis. Jb.
NewYork. 716pp.
States. McGraw-Hill,
United
wiss. Bot., 51: 435-514.
J.D. 1943. Golgiapparatusin Astasiahar- TISCHER, J. 1936. Ueberdas Euglenarhodon
SMYTHI,
und
risii. Nature,Lond.,151: 110.
einerrotenEuglene. HoppeandereCarotinoide
. 1944. The Golgi apparatus of Protozoa.
Seyl.Z., 239: 257-269.
Biol. Rev.,19: 94-104.
beiEuglena
B. 1916. Die Kernteilung
TSCHENZOFF,
SOKOLOFF, D. 1933. Algunas nuevas formasde
36: 137-173.
viridisEhrbg. Arch.Protistenk.,
del Vallede Mexico. Ann.Inst.Biol. VALKANOV,
flagelados
IX. EinerhizA. 1934. Protistenstudien
Mex.,4:197-206.
83: 367-370.
opodialeEuglena? Arch.Protistenk.,
de la VLK, W. 1938. Ueberden Bau derGeissel. Arch.
al conocimiento
. 1935a. Contribucion
estructuradel estigmatade los Euglenoidina.
90: 448-488.
Protistenk.,
Ann.Inst.Biol. Mex.,6: 71-78.
in
WAGER,H. 1899. On the eyspotand flagellum
lumin. 1935b. El organoidede percepciones
Euglenaviridis. J. Linn. Soc. Zool. Lond.,27:
osas de los Euglenoidina.Ann.Inst.Biol. Mex.,
463-481.
6:189-192.
ofOhio. Ohio
WALTON,L. B. 1915. Euglenoidina
SPARROW, F. K. 1943. Aquatic Phycomycetes.
Biol. Surv.Bull.,4: 341-459.
Univ.ofMich.Press,Lansing. 785pp.
WARDEN,C. F., JENKINS,T. N., and WARNER,L. H.
der Algen
STEINECKE, F. 1925. Der Stammbaum
1940. Comparative
Vol. II. Ronald
Psychology,
darUntersuchungen
nach sero-diagnostischen
Press, New York. 1070 pp.
gestellt. Bot.Arch.,10:82-205.
vacuole.
WEATHERBY,J. H. 1941. The contractile
NotizenII. HIeterodendron In Protozoain BiologicalResearch,
- . 1932. Algologische
eds. Calkins
ceraStylodinium
ochracea,
Euglenocapsa
Pascheri,
76: 589-594.
siforme.Arch.Protistenk.,
York. Pp. 404-447.
STEUER, A. 1904. Ueber eine Euglenoide (Eutreptia)aus dem Canale Grande von Triest. WENRICH, D. H. 1924. Studies on Euglenamorpha
hegneri,
n.g.,n. sp. Biol.Bull.,47: 149-175.
3: 126-137.
Arch.Protistenk.,
. 1935. Host-parasite relations between parazooSTRAID,E. 1928. Miscellaneanomenclatorica
sitic Protozoa and theirhosts. Proc. Amer.phil.
I-II. Arch.Naturgsch.,
logicaet palaeontologica
Soc., 75: 605-650.
A., 92: 30-75.
C. 1931. The WERMEL, E. 1924a. Zur Biologie der Flagellaten
SWANN,W. F. G., andDEL RosARio,
eines Moortumpels. Arch. Protistenk.,48: 207ofradioactive
radiations
uponEuglena. J.
effect
Inst.,211:303-317.
212.
Franklin
. 1932. The effectof certainmonochromatic
. 1924b. Neue oder wenigbekannte Protisten.
on Euglenacells. J. Frankradiation
ultraviolet
48: 204-206.
XII. Arch.Protistenk.,
linInst.,213: 549-560.
DE WILDE1MAN,E. 1894. Sur le thermotaxismedes
studyof
SWEET, H. E. 1939. A micropopulation
euglenes. Bull.Soc.belg.Micr.,20: 245-258.
Euglena gracilis Klebs in sterile,autotrophic
. 1928. A propos du thermatoxismedes Eugmedia and in bacterialsuspensions.Physiol.
lenes. Ann. Protist.,Paris, 1: 127-136.
Zool.,12: 173-200.
WILSON, C. N. 1928. The cytology and reproofEuglenaceae
SWIRENKO, D. K. 1927. Systematics
duction of the flagellateTrackelomonasvolvocina.
(Russ.withFr. summary).Arch.russ.Protist.,
Trans.Amer.micr.Soc.,47: 434-443.
6:195-207.
VON
WITTICH. 1863. Ueber den Farbstoffder EugSZABADOs, M. 1936. Euglena Untersuchungen.
lena
Arch.,27: 573-575.
sanguinea. Virchows
4: 45-95.
(Ger. summary).ActaBiol.Szeged.,
and repro- ZUMSTEIN,H. 1900. Zur Morphologieund PhysioTANNREUTHER, G. W. 1923. Nutrition
logiederEuglenagracilis. Jb.wiss.Bot..34: 149ductionofEuglena. Arch.Entw.Mech.Org.,52:
198.
367-383.

The Euglenoid Flagellates

Transcription

Similar documents

Amoeba, Paramecium, Euglena, and Volvox

Freshwater Microorganisms

Work at the Gateway Arch This Summer!

The Euglena - Lisle CUSD 202

Cysts and their formation in some neustonic Euglena species

protists

The leggiest animal known on Earth

Rental Items

trUpoint ARCH Technical Data Sheet.indd