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Tic  Lo7i'C}'  Fitiif/i —  Phycouivccfcs.  Harry 
Morton  Fitzpntrick.  ^31  i)p.  (Illustrated).  AIc- 
Graw-Hill  Book  Co.  $4.00. 

This  book  will  be  heartily  welcomed  by  students 
and  resenrch  wo'-kers  in  mycology  and  ])lant  path- 
ology. The  author  has  recognized  and  attempt- 
ed to  fill  the  need  of  a  complete  and  detailed 
treatment  of  the  taxonomy  and  morphology  of 

the  phycomycetes.  In  his  classification  of  the 
Phycomycetes  into  the  eight  orders,  namely; 
Chytridiales,  Ancylistales,  Blastocladiales,  Mon- 
oblepharidales,  Saprolegniales,  Peronosporales, 
Mucorales,  and  Entomophthorales,  the  author 
does  not  depart  far  from  the  older  classifications. 
Where  changes  are  made,  adequate  explanation  is 
given  for  the  reason  of  the  change.  The  inclusion 
of  the  Plasmodiophoracae  in  the  Chytridiales  and 
the  establishment  of  the  order  Blastocladiales  are 
examples  of  this.  Keys  are  provided  for  all  gen- 
era. A  complete  discussion  of  the  work  done  on 
various  species  of  a  genus  follows  with  citations 
to  literature.  Doul)tful  or  excluded  genera  of  an 
order  are  treated  at  the  end  of  the  order.  In  con- 
clusion a  brief  and  concise  survey  of  the  various 
views  of  the  origin  of  the  Phycomycetes  as  well 
as  Hemiascomycetous  affinities  is  given  by  the 
author. 

Technical  terms  are  printed  in  boldface  type 
in  the  text  at  the  point  at  which  they  are  defined^ 
or  explained.  Especiall\  desirable  is  the  bibli- 
ography found  at  the  end  of  each  chapter. 

— Ruth  I.  Walker. 


"(^<y^^^^^^   ^ 


f  93/ 


nj 


THE  LOWER  FUNGI 
PHYCOMYCETES 


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ology 


THE  LOWER  FUNGI 


PHYCOMYCETES 


BY 
HARRY  MORTON  FITZPATRICK 

Professor  of  Mycology,  Department  of  Plant  Pathology, 
Cornell  University 


First  Edition 


McGRAW-HILL  BOOK  COMPANY,  Inc. 
NEW  YORK:  370  SEVENTH  AVENUE 

LONDON:  6  &  8  BOUVERIE  ST.,  E.  C.  4 
1930 


^        ^~  / 


Copyright,  1930,  by  the 
McGraw-Hill  Book  Company,  Inc. 

printed  in  the  united  states  of  america 

All  rights  reserved.  This  book,  or 

parts  thereof,  may  not  be  reproduced 

in  any  form  without  permission  of 

the  publishers. 


THE    MAPLE   PRESS   COMPANY,   YORK,   PA- 


luj    L  I  8  «  A  R  Y 

^%v  — 

PREFACE 

This  book  is  intended  by  the  author  to  serve  a  two-fold  pur- 
pose. The  urgent  need  of  the  research  worker  in  mycology 
and  plant  pathology  for  an  adequate  treatment  of  the  taxonomy 
and  morphology  of  the  fungi  is  generally  recognized.  Though 
it  is  clearly  impossible  to  provide  this  for  the  whole  group  within 
the  limits  of  a  single  volume,  the  attempt  is  made  here  to  meet 
the  need  for  the  Phycomycetes.  No  effort  has  been  spared 
in  the  endeavor  to  have  the  taxonomic  presentation  thoroughly 
modern  and  complete.  Keys  are  provided  to  all  genera,  and 
citations  are  given  to  much  of  the  outstanding  literature.  At 
the  same  time  the  author  has  tried  to  present  the  subject  matter 
in  such  a  fashion  that  the  book  would  serve  in  college  and  uni- 
versity classrooms  as  a  text  or  reference  work  for  beginning  and 
advanced  students. 

In  formal  courses  in  mycology  time  is  usually  so  limited  that 
it  is  impossible  to  cover  the  entire  field  of  the  fungi  in  other 
than  a  hurried  and  superficial  manner.  Some  teachers  avoid 
this  difficulty  by  confining  the  laboratory  studies  to  one  of  the 
larger  subdivisions  of  the  group.  This  permits  the  student 
to  concentrate  his  efforts  and  to  obtain  a  type  of  intensive  train- 
ing which  fits  him  to  proceed  on  his  own  resources  in  the  remain- 
der of  the  field.  For  a  course  of  this  character  no  group  of  the 
fungi  serves  the  teacher's  purpose  better  than  do  the  Phycomy- 
cetes. Their  diversity  of  form  makes  them  especially  suitable 
from  the  point  of  view  of  comparative  morphology,  and  in  many 
genera  the  species  lend  themselves  readily  to  cytological,  bio- 
logical, cultural,  and  taxonomic  studies.  It  is  hoped  that  this 
book  will  be  found  useful  as  a  text  in  connection  with  laboratory 
courses  of  this  type.  In  any  case  it  will  afford  a  basis  for 
systematic  collateral  reading  on  the  lower  fungi  and  related 
groups  of  organisms. 

Over  a  period  of  years  it  has  been  the  author's  practice  to 
provide  his  classes  with  a  mimeographed  syllabus,  outlining  the 
classification  of  the  fungi  and  introducing  the  student  to  the 
various  phases  of  the  broad  field  of  mycology.     This  syllabus, 


vi  PREFACE 

occasionally  revised  nnd  amplified,  has  served  essentially  as  a 
text,  and  its  presentation  in  book  form  has  long  been  contem- 
plated. The  present  volume  represents  the  outcome  of  that 
plan  in  so  far  as  the  lower  fungi  are  concerned.  It  is,  thus, 
the  natural  outgrowth  of  the  author's  experience  as  a  teacher, 
and  is  in  a  large  part  a  compilation  based  on  the  literature.  No 
claim  is  made  that  it  embodies  to  any  noteworthy  extent  knowl- 
edge gained  from  personal  research  throughout  the  group. 

In  even  a  cursory  examination  of  the  following  pages  the 
reader  will  note  that  the  treatment  given  the  various  families 
and  genera  is  not  uniformly  detailed.  Some  groups  demand  a 
fuller  discussion  on  account  of  their  exceptional  scientific  interest ; 
others  have  received  it  because  of  their  outstanding  economic 
importance.  Though  the  author  has  allowed  himself  consider- 
able latitude  in  this  regard,  the  effort  has  been  made  to  stress 
the  material  which  contributes  most  to  the  usefulness  of  the 
book. 

The  plan  of  providing  a  separate  bibliography  at  the  close 
of  each  chapter  has  been  followed  from  the  conviction  that  the 
segregation  of  the  references  in  this  manner  aids  the  student 
in  gaining  a  general  knowledge  of  the  literature.  It  makes 
easier  also  the  selection  of  papers  for  supplementary  reading. 
The  bibliographies  have  been  carefully  prepared.  Every 
reference  included  serves  a  definite  purpose,  and  is  cited  in  the 
text.  If  errors  in  these  citations  are  discovered  the  author  will 
appreciate  having  them  called  to  his  attention.  Though  it  is 
not  possible  to  state  with  assurance  that  all  the  literature  pub- 
lished prior  to  any  given  date  has  been  incorporated,  a  deter- 
mined attempt  has  been  made  to  keep  the  manuscript  up-to-date 
during  the  process  of  its  preparation. 

The  omission  of  a  glossary  has  been  deliberate.  Terms  are 
printed  in  boldface  type  at  the  points  in  the  text  at  which  they 
are  defined  or  their  use  definitely  indicated.  This  explanatory 
matter  is  available  through  the  index. 

For  pennission  to  reproduce  illustrations  from  the  works  of 
others  the  author  is  under  deep  obligation  to  a  large  number  of 
individuals  and  institutions  in  this  country  and  abroad.  Though 
the  hst  is  so  long  that  detailed  enumeration  here  seems  inadvis- 
able, full  credit  is  given  in  the  legends  accompanying  the  figures. 
A  unifonn  spirit  of  courtesy  and  generosity  has  been  encountered 
in  every  direction  in  this  connection. 


PREFACE 


Vll 


In  conclusion  the  author  wishes  to  express  his  gratitude  for 
the  continued  support  and  encouragement  given  his  efforts  by 
his  colleagues  and  students,  and  by  his  friends  in  other  institu- 
tions. Without  this  cooperation  the  laborious  undertaking 
would  not  have  been  begun  and  hardly  could  have  been  completed 

H.  M.  FiTZPATRICK. 


Cornell  University, 
Ithaca,  New  York, 
Jubj,  1930. 


(uj    L  I  B  :^  A  R  Y 


\< 


.Qt 


CONTENTS 

Page 

Preface v 

CHAPTER  I 

Introduction   . 1 

Thallophyta 1 

Algae 2 

Bacteria 4 

Lichens 4 

Myxothallophyta •.   •    •  5 

Myxom>-cetes 6 

Acrasieae 9 

Labyrinthuleae 11 

Fungi.    " 12 

Pliycomycetes 15 

Ascomycetes 16 

Basidiomycetes 17 

Bibliography :  Introduction 18 

CHAPTER  II 

Phycomycetes 21 

Origin  of  the  Phycomycetes 21 

Thallus 23 

Asexual  Reproduction 24 

Sexual  Reproduction 27 

Classification 37 

Key  to  Orders 39 

Bibliography:  Phycomycetes 41 

CHAPTER  III 

Chytridiales 43 

Key  to  Families 47 

Plasmodiophoraceae 48 

Woroninaceae 66 

Olpidiaceae 71 

Synchytriaceae 80 

Rhizidiaceae 88 

Cladochytriaceae 100 

Doubtful  Chytridiales 107 

Bibliography:  Chytridiales 110 

ix 


M 


iN 


X  CONTENTS 

Page 

CHAPTER  IV 

Ancylistales 117 

Key  to  Genera 118 

Doubtful  or  Excluded  Genera 126 

Bibliography:  Ancylistales 128 

CHAPTER  V 

Blastocladiales 130 

Key  to  Genera 133 

Bibliography:  Blastocladiales 136 

CHAPTER  VI 

MONOBLEPHARIDALES 138 

Key  to  Species  of  Monoblepharis 142 

Bibliography:  Monoblepharidales 145 

CHAPTER  VII 

Saprolegniales 146 

Key  to  Families 147 

Saprolegniaceae 148 

Key  to  Genera 156 

Doubtful  Genus 171 

Leptomitaceae 171 

Key  to  Genera 172 

Bibliography:  Saprolegniales 181 

CHAPTER  VIII 

Peronosporales 185 

Key  to  Families 186 

Albuginaceae 186 

Pythiaceae 193 

Key  to  Genera 194 

Peronosporaceae 210 

Key  to  Genera 211 

Bibliography:  Peronosporales 223 

CHAPTER  IX 

MUCORALES 234 

Key  to  Famihes 241 

Mucoraceae 242 

Pilobolaceae 251 

Thamnidiaceae 253 

Chactocladiaceae 257 

Choanephoraceac 258 

Mortierellaceae • 264 


CONTENTS  XI 

Page 

Piptocephalaceae 270 

Bibliography:  Mucorales 275 

CHAPTER  X 

Entomophthorales   281 

Key  to  Genera 283 

Bibliography:  Entomophthorales 298 

CHAPTER  XI 

PHTCOMyCETOUS  AFFINITIES  OF  THE  HeMIASCOMYCETES .    301 

Euascomycetes 302 

Protoascomycetes 302 

Hemiascomycetes 303 

Thelebolacese 303 

Monascacea; 303 

Protomycetaceaj 304 

Ascoideaceai •    307 

Bibliography:  Hemiascomycetes 313 

Index 317 


THE  LOWER  EUNGl 


PHYCOMYCETES 


CHAPTER  I 
INTRODUCTION 

As  botanists  are  not  yet  in  complete  agreement  with  respect 
to  the  Hmits  and  interrelationships  of  the  various  groups  of 
primitive  plant  life,  it  is  necessary  that  the  extent  of  the  lower 
fungi  as  here  understood  be  indicated.  It  is  desirable  also  that 
at  least  brief  consideration  be  given  to  the  groups  of  organisms 
which  lie  near  them  in  the  classification. 

Thallophytes. — The  plant  kingdom  is  divided  by  systematists 
into  several  large  primary  subdivisions.  The  lowest  of  these 
embraces  all  the  primitive  forms  of  plant  life,  and  is  named  by 
most  writers  the  Thallophyta.  In  this  large  and  diverse  assem- 
blage the  vegetative  portion  of  the  plant  is  usually  very  simple  in 
type,  and  in  general  lacks  the  definite  differentiation  into  root, 
stem,  and  leaf  which  characterizes  higher  plants.  This  simple 
vegetative  plant  body  has  been  termed  the  thallus;  hence  the 
name  Thallophyta  meaning  thallus  plants.  In  the  group  as  a 
whole  the  thallus  is  extremely  simple,  and  in  many  of  the  lower 
forms  consists  of  only  a  single  cell.  Among  the  higher  forms  't 
sometimes  shows  considerable  differentiation.  Moreover,  in 
some  groups  of  plants  above  the  Thallophyta  the  vegetative 
body  is  simple  and  has  been  called  the  thallus.  In  such  cases 
the  relative  simplicity  of  the  reproductive  processes  serves  to 
separate  the  Thallophyta  from  higher  forms. 

Although  no  two  of  the  various  standard  classifications  of 
lower  plants  agree  in  detail,  the  following  brief  outline  of  the 
major  subdivisions  of  the  Thallophyta  represents  in  the  main  the 
most  generally  accepted  arrangement,  and  will,  in  any  case, 

1 


2  THE  LOWER  FUNGI— PHYCOMYCETES 

serve  as  a  basis  for  discussion.     Names  included  in  parentheses 
are  regarded  here  as  synonyms. 

Thallophyta 

1.  Myxothallophyta  (slime  thallophytes) 

A.  Acrasieae 

B.  Labyrinthuleae 

C.  Myxomycetes  (Mycetozoa,  slime  moulds) 

1.  Exosporeae,  i.e.,  Ceratiomyxa 

2.  Endosporeae  (Myxogastres) 
II.  Euthallophyta 

A.  Bacteria  (Schizomycetes,  fission  fvmgi) 

B.  Fungi  (Eumycetes) 

1.  Phj-comycetes  (lower  fungi) 

2.  Ascomycetes 

3.  Basidiomycetes 

4.  Fungi  Imperfecti 

C.  Lichens  (Lichenes) 

D.  Algae 

1.  Cyanophyceae  (Schizophyceae,  blue-green  algae,  fission  algae) 

2.  Chlorophyceae  (green  algae) 

3.  Phaeophyceae  (brown  algae) 

4.  Rhodophyceae  (red  algae) 

The  green  coloring  matter,  chlorophyll,  which  occurs  in  practi- 
cally all  higher  plants,  is  absent  in  several  of  the  groups  of  the 
Thallophyta.  It  is  present  in  at  least  the  majority  of  the  algae, 
and  in  a  restricted  sense  perhaps  may  be  said  to  occur  in  the 
lichens.  It  is  wholly  absent  in  the  Myxothallophyta,  bacteria, 
and  fungi. 

In  the  presence  of  sunhght,  plants  containing  chlorophyll 
are  able  to  synthesize  the  carbohydrates  necessary  to  their  metab- 
olism from  the  carbon  dioxide  of  the  air  and  from  water.  Forms 
of  life  lacking  it  are  dependent  on  green  plants  for  the  elabora- 
tion of  their  carbohydrate  food.  All  non-chlorophyll  containing 
organisms  (animals,  slime  thallophytes,  bacteria,  fungi)  must 
lead,  consequently,  a  dependent  existence,  either  as  parasites 
in  hving  plants  or  animals,  or  as  saprophytes  in  dead  or  dis- 
organizing plant  or  animal  remains. 

Algae. — In  their  possession  of  chlorophyll  and  in  their  con- 
sequent ability  to  lead  an  independent  existence  the  algae  are 
strikingly  different  from  the  colorless  thallophytes.  It  may  be 
assumed  that  they  represent  the  primitive  type  from  which  the 
higher  green  plants  arose.  In  the  morphology  of  the  thallus 
and  organs  of  reproduction  the  group  exhibits  great  diversity. 


INTRODUCTION  3 

At  one  extreme  it  is  represented  by  unicellular  microscopic  forms, 
and  at  the  other  by  species  of  complex  structure,  some  of  which 
are  of  great  size.  The  members  of  the  group  are  chiefly  aquatic, 
and  include  the  pond  scums  and  sea  weeds  familiar  to  all  students 
of  nature. 

Though  chlorophyll  occurs  in  general  throughout  the  algae 
the  thallus  is  distinctly  green  only  in  the  Chlorophyceae.  In 
the  Cyanophyceae,  Phaeophyceae,  and  Rhodophyceae  other  color- 
ing matter  is  present  in  sufficient  amount  to  obscure  the  green, 
and  give  the  thallus  another  characteristic  color.  Older  algolo- 
gists  used  the  color  of  the  thallus  as  a  basis  for  the  primary  sepa- 
ration of  the  group,  and  recognized  as  major  subdivisions, 
blue-green  algae,  green  algae,  brown  algae,  and  red  algae. 
Though  these  groups  are  still  recognized  as  constituting  in  a 
broad  way  a  convenient  separation,  there  is  a  pronounced 
tendency  in  modern  classification  toward  basing  separations 
wholly  on  morphology  {e.g.,  West  and  Fritsch  1927).  Where 
color  fails  to  coincide  completely  with  morphology  rearrangement 
has  occurred.  It  is  to  be  expected  that  future  research  will 
result  in  even  more  extensive  revision  and  the  disappearance 
of  the  old  absolute  separation  based  on  color. 

In  some  of  the  more  recent  treatments,  the  blue-green  algae 
(Cyanophyceae)  are  removed  from  the  algae,  are  renamed  the 
Schizophyceae,  and  together  with  the  Schizomycetes  (bacteria) 
are  made  to  comprise  a  lower  primary  subdivision  of  the  Thallo- 
phyta  termed  the  Schizophyta.  The  group  thus  constituted  is 
regarded  as  occupying  an  isolated  position  in  the  phylogenetic 
arrangement,  and  its  members  are  believed  to  be  very  primitive. 
Both  in  the  bacteria  (fission  fungi)  and  blue-green  algae 
(fission  algae)  reproduction  is  accomplished  almost  exclusively 
by  means  of  simple  vegetative  cell  cleavage  or  fission.  Though 
spores  of  a  simple  type  occur  in  both  groups,  complicated  repro- 
ductive structures  and  processes,  comparable  to  those  of  other 
thallophytes,  are'  lacking.  The  nucleus,  if  not  actually  absent, 
is  at  least  far  less  definitely  organized  than  in  other  plants. 

The  blue-green  color  of  the  Cyanophyceae  is  believed  to  be 
due  to  the  presence  in  the  protoplasm  of  two  associated  pigments, 
one  blue,  the  other  green.  The  blue  coloring  matter  has  been 
named  phycocyanin.  That  the  green  is  chlorophyll  seems  not 
entirely  certain.  It  does  not  occur  in  distinct  chloroplasts, 
and  may  be  in  chemical  combination  with  the  blue  pigment. 


4  THE  LOWER  FUNGI— PHYCOMYCETES 

Although  the  bacteria  lack  the  blue-green  color  their  resemblance 
to  the  Cyanophyceae  in  other  respects  is  certainly  striking. 

Bacteria. — The  absence  of  chlorophyll  in  the  bacteria  has 
influenced  most  students  to  place  these  forms  near  the  fungi. 
In  some  earlier  classifications  the  two  groups  were  merged. 
Even  de  Bary  (1887)  treated  them  side  by  side.  It  is  true  that, 
lacking  chlorophyll,  they  have  a  type  of  physiology  similar  to 
that  of  the  fungi,  but  differences  in  morphology  are  marked  and 
indicate  clearly  that  the  two  groups  are  at  best  only  remotely 
related.  Among  the  lower  fungi  there  seem  to  be  no  forms 
through  which  a  connection  with  the  bacteria  may  be  logically 
indicated.  In  the  fungi  the  nucleus  is  highly  organized  and 
evident,  the  cell  wall  is  of  a  different  composition  from  that  of 
the  bacteria,  and  organs  of  locomotion  are  wholly  dissimilar. 

Although  the  bacteria  constitute  a  very  large  and  extremely 
important  group  of  colorless  lower  forms,  it  is  neither  possible 
nor  appropriate  to  incorporate  in  a  book  on  lower  fungi  any 
detailed  statement  concerning  them.  Instead,  the  student  is 
referred  to  the  many  reference  works  which  have  appeared  in  the 
broad  field  of  bacteriology. 

Lichens. — In  the  above  outline  of  the  major  subdivisions  of 
the  Thallophyta  the  lichens  (Lichenes)  are  listed  as  a  separate  class 
coordinate  in  rank  with  the  fungi.  This  disposition  of  the  group 
is  made  chiefly  with  the  idea  of  isolating  these  forms  for  the 
purpose  of  discussion.  The  actual  position  of  the  group  in  a 
phylogenetic  arrangement  is  somewhat  uncertain  and  debatable. 
The  thallus  of  the  lichens  is  clearly  fungous  in  character,  and 
the  fruiting  structures  are  essentially  identical  with  those  of  the 
true  fungi.  In  fact,  the  lichens  differ  from  the  fungi  only 
in  one  important  respect.  Their  thallus,  in  a  very  early  stage 
of  development,  incorporates  within  itself  algae  encountered  on 
the  substratum,  and  these  exist  throughout  its  life  in  the  inter- 
stices between  its  hyphae.  The  two  organisms,  thus  brought 
together,  considered  as  a  unit,  constitute  a  Hchen.  They  main- 
tain an  intimate  food  relationship,  which  has  been  assumed  by 
many  workers  to  be  mutually  advantageous,  and  has  long  been 
called  symbiosis.  Experiments  have  demonstrated  that  the 
algal  constituent  of  this  dual  combination  is  capable  of  existing 
free  in  nature,  and  indeed  has  its  own  proper  place  in  the  classi- 
fication of  the  algae.  In  any  given  genus  of  lichens  the  alga  is 
usually  a  single  definite  species.     In  the  group  as  a  whole  many 


INTRODUCTION  5 

genera  of  algae  (Cyanophyceae  and  Chlorophyceae)  are  repre- 
sented. Though  the  alga  within  the  thallus  is  sometimes 
abnormal  as  compared  with  its  condition  when  living  free,  usually 
no  malformation  occurs.  The  thallus  does  not  develop  in  nature 
when  the  proper  alga  is  lacking,  and  attempts  in  the  laboratory 
to  induce  the  formation  of  normal  thalli  in  the  total  absence  of 
algae  have  met  with  only  indifferent  success.  It  is  evident  that 
ordinarily  at  least  the  fungous  hyphae  develop  at  the  expense 
of  the  alga,  and  there  seems  to  be  httle  basis  for  the  belief  that 
a  mutually  advantageous  food  relation  exists.  In  fact  the 
phenomenon  appears  to  be  clearly  of  the  nature  of  parasitism, 
rather  than  of  symbiosis.  This  fact  has  led  many  workers  to 
feel  that  the  lichens  are  merely  fungi,  which  have  become  special- 
ized in  their  parasitism  on  algae.  Some  students  who  hold  this 
point  of  view  favor  interpolation  of  the  lichens  among  the  fungi. 
Others,  with  an  interest  or  knowledge  more  pronounced  in  one 
group  than  in  the  other,  prefer,  for  the  sake  of  convenience,  to 
keep  the  two  apart.  Still  other  workers  believe  that  the  peculiar 
association  of  fungus  and  alga  existing  here  indicates  that  the 
group  is  an  ancient  one  with  a  more  or  less  independent  origin. 
The  older  belief  that  the  lichen  is  a  single  organism,  of  which 
the  green  cells  are  an  .integral  part,  has  now  largely  disappeared. 
A  good  general  presentation  of  the  present  day  situation  is  given 
by  Smith  (1921). 

In  the  majority  of  lichens  the  fruitbodies  are  ascomycetous 
in  type,  some  being  discomycetous  and  others  pyrenomycetous. 
A  few  lichens  are  basidiomycetous.  Since  none  are  phycomy- 
cetous  the  group  has  relatively  little  interest  in  connection  with  a 
consideration  of  the  lower  fungi. 

Myxothallophyta. — At  the  lowermost  limit  of  the  Thallophyta 
there  exist  several  groups  of  very  primitive  organisms  which  may 
be  conveniently  discussed  under  the  common  heading  of  Myxo- 
thallophyta. This  name,  first  proposed  in  Engler  und  Prantl's 
Die  NatiirUche  Pflanzenfamilien,  means  slime  thallophytes 
and  alludes  to  the  slimy  aspect  of  the  thallus,  which  is  composed 
of  naked  protoplasm.  In  this  group  are  included  the  Acrasieae, 
Lab5rrinthuleae,  and  Myxomycetes.  Though  clearly  not  closely 
related,  these  forms  agree  in  that  the  thallus  is  naked  and  more 
or  less  amoeboid  throughout  at  least  a  portion  of  its  existence. 
In  this  respect  they  show  a  pronounced  similarity  to  some  of 
the  simplest  forms  of  the  animal  world.     In  fact  many  zoologists 


6  THE  LOWER  FUNGI— PHYCOMYCETES 

include  them  in  the  Protozoa.  In  some  modern  classifications 
no  attempt  is  made  to  maintain  a  definite  line  of  separation 
between  the  plant  and  animal  kingdoms  at  their  lower  levels. 
Instead  the  group  Protista  is  used  to  include  the  primitive 
forms  of  life  which  lie  on  the  borderline.  This  is  indicative 
of  the  general  state  of  uncertainty  concerning  the  interrelation- 
ships of  these  various  simple  forms,  but  should  not  be 
assumed  to  have  resulted  from  ignorance  of  the  various  individual 
groups. 

Myxomycetes. — Knowledge  of  the  taxonomy  of  the  Myxomy- 
cetes  (Mycetozoa,  shme  moulds)  has  reached  a  high  plane,  the 
group  having  been  long  known  and  critically  studied.  The 
monographic  treatises  of  Lister  (1925)  and  Macbride  (1922)  are 
excellent  and  comprehensive.  Moreover,  investigations  by 
Jahn  (1907,  1908,  1911),  Harper  (1900,  1914),  Harper  and 
Dodge  (1914),  Strasburger  (1884),  Bisby  (1914),  Olive  (1907), 
Skupienski  (1918,  1927,  1928),  Gilbert  (1927,  1928  a,  h,  c), 
Elliott  (1916),  Sanderson  (1922),  and  others  on  the  morphology, 
life  history,  and  nuclear  phenomena  in  these  forms  have  given 
us  a  resonably  intimate  knowledge  of  the  group. 

The  Myxomycetes  correspond  with  the  Acrasieae  and  Labyrin- 
thuleae  in  that  in  all  three,  a  vegetative,  phase,  in  which  the 
organism  moves  and  feeds,  alternates  with  a  fruiting  phase  in 
which  it  is  quiescent.  The  Myxomycetes  in  the  fruiting  phase 
form  definite  spores,  the  walls  of  which  have  been  found  in  some 
genera  at  least  to  be  composed  of  cellulose.  In  germination  the 
spore  frees  one  or  more  naked  uninucleate  protoplasts.  The  num- 
ber is  usually  one,  but  in  several  species  (Gilbert,  1928  6 :  350)  is 
variable  (1-4),  and  in  Ceratiomyxa  is  said  to  be  eight.  These 
protoplasts  emerge  as  swarmspores.  Though  naked,  and  to  a 
degree  amoeboid,  especially  at  the  posterior  end,  they  are  provided 
with  a  cilium  (flagellum)  at  the  anterior  end  which  lashes  about 
and  gives  the  cell  a  peculiar,  whirling,  dancing  motion.  In  a  few 
cases  cells  are  found  to  be  provided  with  a  pair  of  cilia  at  the 
forward  end  (Gilbert  1927).  After  swimming  for  a  time  as 
swarmspores  the  cells  usually  lose  their  cilia  and  crawl  about 
by  amoeboid  movements.  They  are  then  termed  myxamoebae. 
Both  in  the  ciliate  and  amoeboid  states  the  cell  is  capable  of 
ingesting  solid  food  (Gilbert  1928  a,  c),  and  in  either  state  a 
temporary  encystment  of  the  individual  to  form  a  microcyst 
may  result  from   drying  out  in  an  unfavorable  environment. 


INTRODUCTION  7 

These  microcysts  lack  a  definite  wall,  and,  on  the  return  of 
satisfactory  conditions,  revive  and  resume  their  activity. 

Both  the  swarmspores  and  myxamoebae,  as  they  feed  and 
grow,  normally  multiply  by  repeated  divisions.  Finally  they 
are  attracted  toward  each  other,  and  tend  to  coalesce.  In  the 
older  literature  multiple  fusion  of  many  such  cells  to  form  a 
multinucleate  mass  is  described.  Cienkowski  first  applied  the 
term  Plasmodium  to  the  multinucleate  naked  thallus  thus 
formed.  The  character  of  the  impulse  which  draws  the  cells 
together  was  not  understood,  but  the  coalescence  was  believed  to 
be  vegetative  in  character. 

Recently  certain  workers  (Gilbert  1928  a,  in  Dictydiaethalium; 
Skupienski  1928,  in  Didrjmium;  Wilson  and  Cadman  1928, 
in  Reticularia)  have  regarded  the  fusion  as  in  part  sexual,  and 
have  reported  fusion  of  uninucleate  cells  (gametes)  in  pairs  to 
form  zygotes  as  the  first  step  in  Plasmodium  formation.  After 
the  zygote  is  formed  it  may  fuse  with  other  gametes,  with  zoo- 
spores, or  with  other  zygotes.  According  to  Gilbert  and  Skupien- 
ski a  plurinucleate  thallus  thus  results.  In  Reticularia,  according 
to  Wilson  and  Cadman,  ciliate  gametes  fuse  in  pairs,  myxamoe- 
bae being  unknown.  The  zygote  thus  formed  acts  as  a  center  of 
attraction  toward  which  other  ciliate  haploid  cells  (gametes  or 
swarmspores)  are  drawn.  These  incoming  cells  enter  the  cy1;o- 
plasm  of  the  zygote  and  are  completely  digested  there,  the  phenom- 
enon being  regarded  as  of  the  nature  of  ingestion  rather  than 
coalescence.  Finally  the  original  pair  of  gametic  nuclei  fuse  to 
form  the  nucleus  of  the  zygote,  and  it  by  repeated  divisions 
furnishes  the  nuclei  for  the  growing  thallus.  If  this  account  is 
correct  the  mature  thallus  of  this  species  is  hardly  a  Plasmodium 
in  the  sense  of  Cienkowski.  Since  the  Plasmodium  has,  however, 
so  long  been  regarded  as  distinctive  of  the  Myxomycetes  veri- 
fication of  the  account  must  precede  its  general  acceptance. 
Much  additional  work  on  the  nuclear  history  of  the  group  is 
desirable.  In  any  case,  the  plasmodium  is  characteristic  in 
aspect,  and  the  phenomenon  of  multiple  fusion,  however  inter- 
preted, is  admittedly  confined  to  the  slime  moulds. 

The  Plasmodium  may  multiply  by  fragmentation,  or  may 
increase  in  size  by  fusion  with  other  plasmodia  or  myxamoebae. 
If  conditions  are  unfavorable  it  may  encyst  temporarily  to  form 
a  sclerotium.  Normally  the  plasmodium  is  an  actively  growing 
body  with  the  power  of  amoeboid  movement.     It  is  multinucle- 


8  THE  LOWER  FUNGI— PHYCOMYCETES 

ate  and  its  nuclei  increase  in  number  by  mitosis  as  it  feeds  and 
enlarges.  As  it  passes  over  or  through  the  substratum  it  ingests 
particles  of  bark,  bits  of  dead  leaves,  and  other  debris  often  in 
sufficient  amount  to  cause  a  change  in  its  color.  These  are 
taken  in,  the  available  food  assimilated,  and  the  refuse  material 
usually  ejected  in  the  wake  of  the  moving  Plasmodium.  Practi- 
cally all  the  species  live  a  purely  saprophytic  existence,  but  some 
are  capable  of  enveloping  and  dissolving  living  materials  such  as 
the  fruit  bodies  of  higher  fungi.  The  growing  plasmodium  has 
a  consistency  similar  to  that  of  egg  albumen.  In  color  it  ranges 
from  pearly  white  through  shades  of  cream,  yellow,  and  orange, 
to  red,  brown,  or  violet.  The  color  is  to  a  degree  definite  in  a 
given  species,  but  it  changes  from  day  to  day  due  to  metabolic 
processes  and  is  dependent  somewhat  on  the  amount  of  unassim- 
ilated  materials  present  in  the  cytoplasm.  When  the  Plas- 
modium Hes  on  the  surface  of  the  substratum  it  may  form  a  thin 
film  of  irregular  outline,  but  when  permeating  the  crevices  of  a 
decaying  log  it  becomes  a  much  branched  network  of  strands. 

After  an  extended  period  of  vegetative  activity  the  plasmodium 
flows  out  upon  an  exposed  surface,  and  contracts  into  a  cushion- 
shaped  mass.  It  is  then  ready  for  transformation  into  the 
fruiting  phase.  The  Myxomycetes  are  split  into  two  primary  sub- 
divisions on  the  basis  of  the  character  of  the  fructification  which 
is  then  formed.  In  the  Exosporeae,  including  only  the  genus 
Ceratiormjxa,  the  fruiting  structure  is  columnar  and  bears  spores 
over  its  outer  surface,  each  at  the  end  of  a  minute  sterigma. 
In  the  Myxogastres  the  spores  are  borne  inside  the  fructification. 
It  is  usually  then  called  the  sporangium.  If  the  sporangium  is 
irregular  or  sinuous  in  form  it  is  termed  a  plasmodiocarp.  If 
several  imperfectly  delimited  sporangia  become  partially  fused 
and  develop  into  a  compound  fructification  it  is  called  an 
aethalium.  It  will  be  sufficient  here  to  describe  the  development 
of  the  typical  sporangium. 

Over  the  surface  of  the  cushion-shaped  plasmodium  the 
protoplasm  is  pushed  up  at  numerous  points  to  form  definite 
papillae.  These  soon  elongate  into  tiny  columns,  each  of  which 
develops  into  a  sporangium.  The  base  of  each  column  contracts, 
and,  in  species  having  stipitatc  sporangia,  forms  a  slender  tubular 
stalk  through  which  the  protoplasm  passes  upward  into  an 
enlarging  inflated  terminal  vesicle  that  later  contains  the  spores. 
As  the  protoplasm  advances  refuse  material  is  thrown  out,  and 


INTRODUCTION  9 

is  used  to  form  a  membrane,  the  peridium,  over  the  surface  of 
the  sporangium.  Similarly,  as  the  protoplasm  passes  into  the 
sporangia  other  waste  materials  are  often  left  behind  on  the 
substratum  and  may  form  a  glistening  film,  termed  the  hypo- 
thallus.  Within  the  sporangium  Unes  of  cleavage  cut  the  proto- 
plasm into  progressively  smaller  portions  until  finally  uninucleate 
bits  are  delimited.  Each  of  these  secretes  a  definite  wall,  and 
develops  into  a  globose  spore.  During  the  process  of  protoplasmic 
cleavage,  waste  materials  not  used  in  the  formation  of  the 
peridium  are  deposited  in  elongate  vacuoles,  and  form  there 
cylindrical  threads  called  capillitium.  These  threads  are  often 
ornamented  with  beautiful  surface  markings,  spiral  thickenings, 
spines,  etc.,  which  afford  characters  of  diagnostic  value  useful  in 
generic  separation.  At  maturity  the  peridium  bursts  or  disinte- 
grates, and  the  mass  of  capillitium  and  spores  is  exposed.  The 
spores  then  fall  out  and  are  disseminated  by  the  wind. 

The  name  Myxogastres  was  selected  as  indicative  of  the 
marked  resemblance  which  certain  of  these  organisms  show  to 
the  Gastromycetes.  The  similarity  is,  however,  only  superficial. 
The  capilUtium  and  peridium  in  the  Gastromycetes  are  formed 
from  hyphae,  made  up  of  living  cells,  and  are  consequently  wholly 
unlike  the  structures  bearing  the  same  names  in  this  group. 

Nuclear  division  in  the  Myxomycetes  has  been  studied  in 
various  genera,  and  seems  to  be  essentially  a  typical  mitosis. 
No  evidence  of  the  existence  in  the  group  of  a  primitive  type  of 
mitosis  resembling  that  of  the  Plasmodiophoraceae  has  been 
found.  In  Ceratiomyxa,  sole  representative  of  the  Exosporeae, 
OHve  (1907)  states  that  a  sexual  fusion  of  nuclei  in  pairs  occurs 
just  preceding  the  cutting  out  of  the  young  uninucleate  spores. 
He  says  that  this  is  followed  immediately  by  synapsis  and  the 
reduction  divisions,  the  matures  pores  being  quadrinucleate. 
Jahn  (1907)  in  a  study  of  the  same  species  found  fusion  and 
reduction  at  a  much  earlier  stage.  A  reinvestigation  of  this 
form  and  a  comparison  of  the  nuclear  history  here  with  that 
in  various  members  of  the  Myxogastres  is  desirable.  Until  we 
know  more  concerning  sexuality  and  nuclear  phenomena  in  the 
group  we  cannot  arrive  at  any  safe  conclusion  concerning  its 
relationships  with  other  lower  forms. 

Acrasieae. — The  Acrasieae  comprise  a  small  group  of  sapro- 
phytic, and  for  the  most  part  coprophilous  organisms,  lying 
apparently  at  the  extreme  lower  Umit  of  the  plant  world.     They 


10  THE  LOWER  FUNGI— PHYCOMYCETES 

have  been  regarded  by  van  Tieghem,  de  Bary,  Zopf,  Harper, 
Olive,  and  others  as  belonging  near  the  Myxomycetes,  and  are 
here  so  treated,  though  the  differences  between  the  two  groups 
are  at  least  as  pronounced  as  their  points  of  similarity. 

In  the  Acrasieae  the  organism  exists  during  the  vegetative 
phase  in  the  form  of  naked  amoeboid  cells  (myxamoebae). 
These  never  pass  into  the  ciliate  swarmspore  condition  which, 
at  certain  periods,  characterizes  the  motile  cells  of  the  Myxo- 
mycetes. They  crawl  about  over  the  substratum,  ingesting  and 
feeding  on  solid  materials,  and  increase  greatly  in  number  by 
repeated  divisions.  At  the  close  of  the  vegetative  period  under 
the  influence  of  some  unexplained  impulse,  they  move  toward 
common  centers  and  collect  into  definite  colonies  which  have  been 
termed  by  some  writers  pseudoplasmodia  or  aggregation-plas- 
modia.  The  myxamoebae  composing  these  colonies  do  not 
fuse.  Each  cell  retains  its  individuality  throughout  the  further 
development  of  the  colony  and  the  subsequent  formation  of 
the  mature  fructification.  The  myxamoebae  crawl  over  one 
another  and  become  heaped  up  to  form  sessile  or  stalked  masses 
of  definite  form,  which  in  some  species  exhibit  considerable  com- 
plexity. Each  cell  then  usually  assumes  a  cellulose  wall  and 
becomes  a  spore.  In  two  genera  {Sappinia,  Guttulinopsis)  a 
wall  is  not  formed,  but  the  peripheral  protoplasm  is  hardened 
into  a  protective  layer.  The  cell  in  such  cases  is  called  a  pseudo- 
spore.  These  spores  or  pseudospores  lie  in  a  definite  mass, 
being  held  together  by  a  mucous  substance,  and  constitute  the 
fructification.  These  masses  have  a  superficial  resemblance  to 
the  colonies  of  bacterial  cells  formed  in  the  Myxobacteriaceae. 
At  the  close  of  a  period  of  rest  the  spores  germinate  by  cracking 
open,  and  the  content  of  each  escapes  as  a  vegetative  myxamoeba. 
The  pseudospores  pass  into  the  vegetative  phase  gradually  with- 
out casting  off  a  membrane  of  any  sort.  Under  unfavorable 
environmental  conditions  myxamoebae  may  enter  the  resting 
condition  isolated  from  one  another  as  microcysts. 

Though  the  Acrasieae  resemble  the  Myxomycetes  in  possessing 
a  naked  amoeboid  phase,  their  vegetative  period  includes 
neither  the  swarmspores  nor  the  true  plasmodium  of  that  group. 
Moreover,  there  is  no  condition  which  shows  any  resemblance  to 
the  net-plasmodium  of  the  Labyrinthuleae.  In  the  Acrasieae 
the  vegetative  stage  ends  when  formation  of  the  pseudoplas- 
modium  begins.     The  latter  is,  therefore,  a  structure  connected 


INTRODUCTION  11 

with  the  phenomenon  of  fructification,  and  cannot  be  regarded  as 
homologous  with  either  the  true  Plasmodium  of  the  Myxomycetes 
or  the  net-plasmodium  of  the  LabyrinthuUae. 

For  details  of  the  taxonomy  of  the  group  the  student  is  referred 
to  the  papers  of  Olive  (1901:  1902).  The  families  and  genera 
recognized  by  him  as  comprising  the  group  are  as  follows: 

Acrasieae  van  Tieghem,  1880. 
Sappiniaceae 

Sappinia  Dangeard,  1896. 
Guttulinaceae 

Guttulinopsis  Olive,  1901. 

GuUulina  Cienkovvski,  1873. 
Dictyosteliaceae 

Acrasis  van  Tieghem,  1880. 

Dictyostelium  Brefeld,  1869. 

Polysphondylium  Brefeld,  1884. 

Coenonia  van  Tieghem,  1884. 

The  group  as  treated  by  Olive  contains  about  twenty  species. 
Prior  to  the  appearance  of  his  papers  only  one  species  had  been 
reported  for  North  America.  He  grew  a  number  of  forms  in  pure 
culture  on  solid  media  and  in  nutrient  decoctions.  He  also 
studied  stained  preparations,  and  figures  nuclei.  No  indication 
of  nuclear  fusion  was  observed.  If  sexuaHty  exists  in  the  group 
it  is  as  yet  undiscovered. 

Labyrinthuleae. — This  group,  founded  by  Cienkowski  (1867), 
is  composed  of  a  small  number  of  very  primitive  and  imperfectly 
known  organisms  characterized  by  the  presence  in  the  vegetative 
phase  of  a  peculiar  structure  termed  a  net-plasmodium.  This 
was  thought  by  Zopf  (1892)  to  constitute  a  vegetative  condition 
intermediate  in  character  between  the  aggregation-plasmodium 
of  the  Acrasieae  and  the  true  Plasmodium  of  the  Myxomycetes. 
He  erected  the  group  Sorophoreae  to  include  the  Acrasieae  and 
Labyrinthuleae.  As  now  understood  the  Labyrinthuleae  embrace 
two  genera,  Lahyrinthula  Cienkowski  (1867)  with  three  species 
parasitic  on  algae,  and  Diplophrys  Barker  (1868)  with  one 
coprophilous  species  and  another  doubtful  form  said  to  be 
aquatic. 

In  the  beginning  of  the  vegetative  phase  the  Labyrinthuleae 
exist  as  motile  fusiform  (spindle-shaped)  cells,  each  of  which 
is  provided  with  two  radiating  tufts  of  delicate  pseudopodia 
situated  at  the  opposite  poles.  These  cells  may  remain  separate, 
but  when  they  come  in  contact  their  pseudopodia  usually  fuse. 


12  THE  LOWER  FUNGI— PHYCOMYCETES 

Anastomosis  of  several  individuals  in  this  fashion  results  in 
the  formation  of  the  characteristic  net-Hke  structure  designated 
by  Zopf  the  net-plasmodium.  The  fusiform  individuals  possess 
a  limited  degree  of  contractiUty,  but  retain  their  individuality. 
They  appear  to  ghde  along  the  threads  of  the  net,  and  are  thus 
Umited  in  their  wanderings.  During  this  period  of  activity 
they  feed,  increase  in  size,  and  undergo  repeated  division. 
In  division  the  cell  elongates,  is  constricted  at  the  middle,  and 
is  finally  pulled  apart  into  two  new  individuals  held  together  by 
a  plasma  strand.  The  research  of  Zopf  on  Lahyrinthula  indi- 
cated that  food  is  obtained  in  solution  rather  than  in  the  solid 
condition. 

At  the  close  of  the  vegetative  period  the  wandering  cells 
collect  into  sessile  or  stalked  masses,  and  pass  into  an  encysted 
state  which  may  be  termed  the  fructification.  The  individual 
cells  in  Lahyrinthula  assume  definite  walls  and  are  termed  spores. 
The  chemical  composition  of  the  wall  is  apparently  unknown.  In 
Diplophrys  a  wall  is  absent,  and  the  cell  is  called  by  Ohve 
(1901)  a  pseudospore.  After  a  period  of  rest,  the  organism 
passes  again  into  the  vegetative  phase,  the  spores  in  germination 
freeing  one  to  four  of  the  fusiform  cells  provided  with  polar 
pseudopodia. 

The  Labyrinthuleae  are  far  less  well  known  than  the  Acrasieae. 
The  species  of  Lahyrinthula  have  been  observed  only  by  their 
authors  Cienkowski  and  Zopf,  while  those  of  Diplophrys  have 
been  very  inadequately  studied.  The  position  of  the  group  in 
the  classification  is  extremely  doubtful.  Many  zoologists 
include  it  in  the  Protozoa.  The  type  of  cell  division  seems  to 
indicate  a  relationship  with  the  Monadineae  of  that  group.  The 
net-plasmodium  has  only  a  superficial  resemblance  to  the  true 
Plasmodium  of  the  Myxomycetes,  and  it  is  unlikely  that  the 
Labyrinthuleae  are  more  than  remotely  related  to  them. 

Fungi. — The  essential  characters  of  the  other  groups  of  the 
Thallophyta  having  been  indicated  above,  the  field  is  now 
cleared  for  a  general  consideration  of  the  fungi.  This  must 
of  necessity  be  somewhat  more  brief  than  would  seem  from 
certain  points  of  view  desirable. 

The  fungi  constitute  by  far  the  largest  and  most  diverse 
group  of  non-chlorophyll  containing  thallophytes.  In  general 
they  may  be  said  to  differ  from  other  colorless  forms  in  the 
possession  of  the  filamentous  vegetative  structure  known  as 


INTRODUCTION  13 

mycelium.  The  spores  of  the  fungi  are  of  many  t3'^pes,  but  in 
practically  all  cases  in  germination  they  put  out  one  or  more 
small  protuberances  which  elongate  and  assume  the  form  of 
more  or  less  cyHndrical  threads.  These  are  termed  germ  tubes. 
As  they  increase  in  length  they  tend  to  branch,  and  soon  a  much 
branched  complex  of  threads  constituting  the  vegetative  plant 
body  or  thallus  is  formed.  On  account  of  its  mould-like  aspect 
in  some  groups  this  structure  received  the  name  mj^celium.  A 
single  thread  or  branch  is  termed  a  hypha  (plur.  hyphae).  In 
some  fungi  the  development  of  mycelium  is  very  limited  {e.g., 
Saccharomycetaceae)  and  in  a  few  groups  (Olpidiaccae,  Woronin- 
aceae,  Synchytriaceae,  Ancylistaceae)  the  thallus  may  fail  com- 
pletely to  assume  the  filamentous  form.  In  such  cases  mycelium 
is  said  to  be  absent.  In  some  of  the  algae,  threads  comparable 
to  mycelium  are  present.  In  certain  bacteria,  moreover,  the 
cells  remain  together  in  chains  forming  long  threads  which  are 
analogous  to  mycelium.  The  fungi  which  lack  mycelium  resem- 
ble the  other  members  of  the  group  in  the  characters  of  their 
reproductive  processes,  and  in  general  are  not  easily  confused 
with  other  lower  thallophytes.  A  few  (Plasmodiophoraceae, 
Woroninaceae)  approach  the  Myxomycetes,  and  correspond  with 
them  in  that  the  thallus  is  a  naked  protoplast  at  least  in  early 
stages.  In  the  higher  fungi  a  cell  wall  is  always  present,  and 
is  composed  of  a  modification  of  cellulose,  termed  fungus  cellulose, 
which  in  composition  is  akin  to  chitin.  In  the  lower  fungi  the 
wall  in  many  forms  gives  the  reaction  for  true  cellulose.  Though 
green  plants  in  general  store  their  food  reserve  in  the  form  of 
starch  this  substance  is  unknown  in  the  fungi.  Instead,  the 
soluble  food  is  transformed  into  an  oil,  glycogen,  and  is  stored  in 
the  vacuoles.  In  this  connection  a  consideration  of  the  taxo- 
nomic  position  of  the  genus  RhodochT/triumJjSigerheim,  containing 
a  single  species  R.  spilanthidis  parasitic  on  ragweed  {Ambrosia 
spp.),  is  of  interest.  This  organism  lacks  chlorophyll  but  stores 
as  starch  the  food  obtained  in  soluble  form  from  the  host.  In 
morphology  it  corresponds  closely  with  the  algal  genus  Phyllo- 
hium  Klebs  (1881).  Because  it  lacks  chlorophyll  Lindau  (1899) 
places  it  in  the  fungi.  Other  students  (Lagerheim  1893 ;  Atkinson 
1908  a,  h)  incorporate  it  in  the  algae.  This  difference  in  point  of 
view  illustrates  the  difficulty  of  drawing  a  sharp  line  between 
the  two  groups.  The  green  algal  genus  Chlamydomonas,  which 
in  certain  classifications  embraces  some  non-chlorophyll  con- 


14  THE  LOWER  FUNGI— PHYCOMYCETES 

taining  saprophytic  forms,  constitutes  another  illustration  of 
the  point.  Such  border  line  cases  make  difficult  precise  gener- 
alizations concerning  the  limits  of  the  fungi. 

The  reproductive  processes  of  most  of  the  fungi  are  far  more 
highly  developed  than  those  of  any  of  the  bacteria  or  slime  thallo- 
phytes.  They  are  approximated  in  complexity  in  some  of  the  algae. 
Many  of  the  fungi,  apparently  the  majority,  are  polymorphic, 
i.e.,  form  two  or  more  kinds  of  spores  in  the  life  cycle.  These 
different  spore  forms  are  designated  either  as  perfect  or  imperfect. 
The  perfect  spore  form  occurs  more  or  less  definitely  in  connection 
with  the  sexual  process,  and  is  often  called  the  sexual  spore. 
The  imperfect  spore  form  is  asexual.  More  than  one  type  of 
asexual  spore  may  be  developed  in  a  single  species.  The  sexual 
and  asexual  spores  are  often  borne  together  or  in  succession  on 
the  same  thallus,  but  in  some  cases  occur  on  different  thalli. 
Unless  borne  together  the  genetic  connection  between  the  two 
may  remain  for  a  long  time  unsuspected.  The  phase  of  the  life 
cycle  in  which  the  perfect  spore  form  occurs  is  termed  the  perfect 
or  sexual  stage.  That  in  which  the  imperfect  spore  form  is 
developed  is  called  the  imperfect  or  asexual  stage.  In  both 
cases,  especially  in  the  higher  fungi,  the  spores  are  often  borne 
in  definite  aggregations  or  conceptacles  termed  in  general 
fruit  bodies. 

In  as  far  as  possible,  the  classification  of  the  fungi  is  based  on 
the  characters  of  the  perfect  stage.  In  practically  all  modern 
systems  of  classification  the  fungi  are  subdivided  on  this  basis 
into  three  major  natural  groups, — Phycomycetes,  Ascomycetes, 
and  Basidiomycetes.  These  subdivisions  usually  rank  as 
classes,  are  coordinate,  are  treated  as  units  in  the  phylogenetic 
arrangement,  and  are  separated  rather  sharply  from  one  another. 
In  these  respects  they  differ  essentially  from  the  group  Fungi 
Imperfecti,  which  is  usually  appended  to  them  as  a  fourth  major 
subdivision  of  the  fungi.  This  group  was  erected  for  the  temporary 
accommodation  of  the  imperfect  stages  of  fungi  which  have  not 
yet  been  identified  in  connection  with  their  perfect  stages.  There 
are  many  hundreds  of  them.  They  are  believed  to  be,  in  most 
cases,  imperfect  stages  of  Ascomycetes.  A  smaller  number 
probably  belong  with  Phycomycetes  or  Basidiomycetes.  The 
perfect  stages  of  some  of  them  may  no  longer  occur  in  nature,  or 
possibly  may  never  have  been  developed.  The  group  as  a  whole 
has  no  unity  and  consequently  no  proper  place  in  a  natural 


INTRODUCTION  15 

system.  The  imperfect  forms  of  which  it  consists  are  separated 
by  an  artificial  classification  based  largely  on  spore  characters. 
When  one  of  them  is  proved  to  be  the  imperfect  stage  of  a  known 
member  of  the  Phycomycetes,  Ascomycetes,  or  Basidiomycetes  it 
passes  automatically  to  that  group,  and  bears  thereafter  the 
name  apphed  to  the  perfect  stage.  It  is  to  be  expected  that 
in  time  hundreds  of  such  transfers  will  be  made.  Certain  forms, 
which  are  properly  speaking  Fungi  Imperfecti,  have  never  been 
included  in  the  group  because  their  characters  are  such  as  to 
indicate  clearly  their  actual  relationships.  Members  of  the 
Mucorales  known  only  in  the  asexual  (sporangial)  condition, 
and  unconnected  stages  of  rusts  (Uredinales)  belonging  to  the 
form  genera  Aecidium,  Caeoma,Peridermium,Roestelia,  and  Uredo 
fall  in  this  category. 

The  outstanding  characters  of  the  Phycomycetes,  Ascomycetes, 
and  Basidiomycetes  will  now  be  indicated  briefly.  The  Phycomy- 
cetes embrace  the  lower  fungi  treated  in  this  book.  A  general 
discussion  of  the  group  is  given  in  the  following  chapter.  The 
Ascomycetes  and  Basidiomycetes  are  called  the  higher  fungi. 
Certain  authors  restrict  the  name  Eumycetes  to  them. 

The  Phycomycetes  viewed  in  their  entirety  are  a  diverse  group. 
The  primitive  members  of  the  class  are  chiefly  aquatic,  while  the 
more  recent  are  terrestrial.  The  thallus  in  the  lower  forms  is 
characteristically  simple  and  inconspicuous.  In  the  higher  it 
develops  as  a  profusely  branching  mycelium,  which  is  usually 
more  evident  than  the  reproductive  bodies.  The  mycelium  is 
usually  coenocytic  (non-septate  and  plurinucleate),  but  in  some 
forms,  chiefly  the  highest,  tends  to  develop  septa  in  age  or  may 
even  be  normally  septate  from  the  beginning.  In  practically  all 
cases  septa  are  formed  in  the  delimitation  of  the  reproductive 
cells.  Sexual  organs  are  commonly  present  and  usually  func- 
tional. The  product  of  sexuahty  is  usually  a  spore  (oospore  or 
zygospore).  In  a  few  known  cases  motile  sex  cells  (gametes) 
fuse  in  pairs  to  form  motile  zygotes.  In  a  single  genus,  Mono- 
blepharis,  ciliated  antherozoids  fertilize  the  female  cell.  In 
some  species  the  sexual  cells  are  no  longer  functional.  In  others, 
one  or  both  cells  have  been  suppressed.  Asexual  reproduction 
occurs  typically  by  means  of  spores  (sporangiospores)  borne  in 
a  sac  called  the  sporangium.  The  sporangiospores  in  the  lower 
forms  are  usually  motile  (zoospores,  swarmspores),  but  in  the 
higher  are  usually  non-motile  (aplanospores) .     In  many  cases, 


16  THE  LOWER  FUNGI— PHYCOMYCETES 

especially  in  higher  groups,  the  sporangium  germinates  directly 
by  one  or  more  germ  tubes,  functioning  thus  in  its  entirety  as  a 
spore.  It  is  then  called  by  many  writers  a  conidium.  The 
most  characteristic  structures  of  the  group  as  a  whole  are  the 
sporangium,  coenocytic  mycehum,  and  zoospores. 

In  the  Ascomycetes  the  mycelium  is  well  developed  in  most 
cases,  and  is  typically  septate.     It  is  usually  less  conspicuous, 
however,  than  the  reproductive  bodies,  the  condition  in  this 
respect  being  the  reverse  of  that  in  the  Phycomycetes.     Motile 
cells  are  never  formed.     The  group  is  distinguished  by  the  ascus, 
which  is  a  sac  forming  endogenous  spores,  usually  in  small  and 
definite  number  (typically  eight,  but  less  frequently  some  other 
number  which  is  usually  a  multiple  of  two).     Though  a  sac 
forming  endogenous  spores,  the  ascus  is  not  homologous  with 
the  sporangium,  and  differs  from  it  in  several  important  respects. 
It  is  sexual  in  character,  in  it  two  nuclei,  usually  regarded  as 
sexually   different,    fuse,    and  in  it  reduction  division  occurs. 
Following  the  reduction  process  the  ascospores  are  cut  out  by 
means  of  the  astral  rays  in  a  peculiar  process  known  as  free  cell 
formation.     The  spores  thus  delimited  are  surrounded  by  unused 
cytoplasm  termed  epiplasm.     In  the  sporangium,  epiplasm  is 
absent,  and  the  process  of  progressive  cytoplasmic  cleavage, 
which  accomplishes  spore  formation  there,  is  a  wholly  different 
phenomenon.     In  the  lower  Ascomycetes  the  asci  are  formed 
without  order  throughout  a  mould-like  mycelium,  or  exist  as 
isolated  cells  as  in  the  yeasts.     In  the  great  majority  of  higher 
forms  they  are  collected  into  a  more  or  less  spherical,  flask- 
shaped,  cup-shaped  or  disc-shaped  fruit  body,  usually  conspic- 
uous   and    termed    the    ascocarp    (apothecium,    perithecium). 
Asexual  reproduction  takes  place  by  means  of  spores  termed 
conidia.     Conidia  are  exogenous  and  are  adjointed  at  the  ends 
of  more  or  less  specialized  hyphae  called  conidiophores.     The 
conidium  of  the  Ascomycetes  and  Basidiomycetes  is  regarded 
as  homologous  with  that  of  the  Phycomycetes  and  hence  with 
the  sporangium.     The  conidiophores  in  some  forms  are  scattered 
over  the  mycelium.     In  others,  they  are  aggregated  into  definite 
sori  or  fruit  bodies  (acervuli,  sporodochia,  coremia,  pycnidia). 
In  some  forms  the  hyphae  break  apart  at  the  septa  to  form 
unicellular  asexual  spores  termed  oidia.     The  group  as  a  whole 
may  be  roughly  split  into  the  Discomycetes  and  Pyrenomycetes. 
It  contains  the  yeasts,  morels,  cup  fungi,  truffles,  and  many  forms 


INTRODUCTION  17 

with  minute  fruit  bodies.     It  is  the  largest  of  the  three  major 
subdivisions  of  the  fungi,  and  contains  about  twenty  orders. 

In  the  Basidiomycetes  the  thalhis  exists  as  a  well  developed 
mycelium.  The  individual  hyphae  often  lie  close  together  and 
run  more  or  less  in  parallel  forming  heavy  strands  or  cords  termed 
rhizomorphs.  The  fruit  body  usually  results  from  differentiation 
at  the  tip  of  a  rhizomorph.  The  hyphae  are  septate  and  are 
often  provided  at  the  septa  with  peculiar  structures  termed 
clamp  connections.  The  clamp  is  of  the  nature  of  a  curved 
lateral  branch  connecting  the  two  cells  otherwise  separated  by 
the  septum,  and  is  probably  homologous  with  the  ascus  hook 
developed  in  crozier  formation  in  the  Ascomycetes.  The 
Basidiomycetes  are  distinguished  by  the  basidium,  an  organ 
similar  to  the  ascus  and  probably  homologous  with  it,  but  differ- 
ing in  that  the  spores  are  formed  exogenously  (outside)  rather 
than  endogenously  (inside).  The  sexual  nuclei  fuse  in  the 
basidium  and  reduction  occurs  there.  The  resulting  nuclei 
pass  out  of  the  basidium  through  minute  sterigmata  into  vesicular 
enlargements  at  their  tips,  which  then  mature  into  spores 
(basidiospores)  and  are  ejected  into  the  air.  Usually  four 
spores  are  formed.  The  basidia  usually  arise  in  or  on  special- 
ized fruit  bodies  and  commonly  stand  side  by  side  forming  a 
paUsade  layer  termed  the  hymenium.  Asexual  reproduction 
by  means  of  conidia  of  various  types  commonly  occurs.  The 
group  may  be  divided  roughly  into  smuts,  rusts,  Hymenomycetes 
and  Gastromycetes.  It  contains  the  mushrooms,  bracket  fungi, 
coral  fungi,  gelatinous  fungi,  stink-horns,  puff-balls,  bird's  nest 
fungi  and  other  prominent  forms.  It  is  a  large  group  but  has 
been  more  thoroughly  studied  than  have  the  Ascomycetes. 
Sexual  organs,  present  in  many  Phycomycetes  and  numerous 
Ascomycetes,  are  apparently  absent  in  the  Basidiomycetes.  The 
group  is  characterized  by  a  distinct  alternation  of  generations 
in  which  a  mycehum  composed  of  uninucleate  cells  alternates 
with  mycehum  in  which  the  cells  are  binucleate.  The  same 
type  of  cycle  somewhat  less  sharply  marked  occurs  in  the 
Ascomycetes. 

For  a  more  detailed  treatment  of  the  Ascomycetes  and  Basidio- 
mycetes, especially  with  regard  to  the  problems  of  comparative 
morphology  and  cytology,  the  student  is  referred  to  the  recently 
published  books  of  Gwynne-Vaughan  (1922)  and  Gaumann 
and  Dodge  (1928).     The  taxonomic  hterature  is  extensive  and 


18  THE  LOWER  FUNGI— PHYCOMYCETES 

widely  scattered,  and  the  systematist  is  dependent  to  a  large 
degree  on  the  Sylloge  Fungorum  of  Saccardo  and  the  various 
lists  and  abstracting  journals  which  lead  him  to  the  original 
papers. 

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INTRODUCTION  19 

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Gesell,  29:  231-247,  pi.  11,  1911. 
Klebs,  G.,  Beitrage  zur  Kenntniss  niederer  Algenformen.     Botan.  Zeittmg, 

39 :  249-336,  1881. 
Lagerheim,  G.,  Rhodochytrium  nov.  gen.  eine  Uebergangsform  von  den 

Protococcaceae  zu  den  Chytridiaceen.     Botan.  Zeilung,  51 :  43-53,  1893. 
Lindau,  G.,  Nachtrage.    Die  Naturliche  Pfianzenfamilien  {Engler  und  Pratitl), 

P:  528,  1899. 
Lister,  Arthur  and  Gulielma  Lister,  The  Mycetozoa.  3d  Edit.  296  pp., 

222  pi,  1925. 
Macbride,   Thomas  H.,   The  North   American   Shme-moulds.   2nd   Edit. 

299  pp.,  23  pi.  New  York  (Macmillan),  1922. 
Olive,  E.  W.,  A  preliminary  enumeration  of  the  Sorophoreae.     Proc.  Amer. 

Acad.  Arts  &  ScL,  37:  333-344,  1901. 
,  Monograph  of  the  Acrasieae.     Proc.  Bost.  Soc.  Nat.  Hist.,  30:  451- 

513,  pi  6-8,  1902. 
-,  Cytological  studies  on  Ceratiomyxa.     Trans.  Wise.  Acad.  Sci.,  15: 


753-774,  pi  47,  1907. 
Oltmanns,  F.,  Morphologie  und  Biologie  der  Algen.  2nd  Edit.  Jena.,  1922. 
RosTAFiNSKi,  J.  T.,  SUizowce  (Mycetozoa)  Monografia.     432  pp.,  13  pi, 

Paris  (in  PoUsh),  1876. 
Sanderson,  A.  R.,  On  the  parasitic  habits  of  the  plasmodium  of  Physarum 

viride  var.  rigidum  Lister.      Trans.  Brit.  Mycol  Soc,  7  :  299,  300,  1922. 
Skupienski,  F.  X.,  Sur  la  sexualite  chez  les  Champignons  Myxomycetes. 

CompL  Rend.  Ac.  Sci.  Paris.,  167:  31-33,  1918. 
,  Sur  le  cycle  evolutif  chez  une  espece  de  Myxomycete  endospore, 

Didymium  difTorme  (Duby).     Etude  cytologique.     Compt.  Rend.   Ac. 

Sci.  Paris.,  184:  1341-1344,  fig.  1,   1927.      (Abstr.  in  Biol  Abstr.,  2: 

6923.) 
— ;   Badania   Bio-cytologiczne  nad  Didymium    difforme  Duby,  czesc 

pierwsza.     Acta  Soc.   Botan.   Poloniae,   5:   255-336,    pi    12-18,    1928, 

(French  resume). 
Smith,  A.  L.,  Lichens.  464  pp.,  Cambridge,  1921. 
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fallax.     Botan.  Zeilung,  42:  305-316,  321-323,  1884. 
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534  pp.,  207  fig.,  Cambridge,  1927. 


20  THE  LOWER  FUNGI— PHYCOMYCETES 

Wilson,  Malcolm  and  Elsie  J.  Cadman,  The  life  history  and  cytology  of 

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pi.  1-6,  1928. 
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Beitrage  zur  Physiol,   u.  Morphol.  niederer  Organismen.,  2:  36-48,  pi. 

4,  5,  1892. 


CHAPTER  II 
PHYCOMYCETES 

The  name  Phycomycetes,  translated  literally,  means  algal 
fungi.  It  was  first  applied  by  early  investigators,  who  recognized 
that  members  of  the  group  resemble  strikingly  in  essential 
features  of  morphology  certain  of  the  green  algae. 

Origin  of  the  Phycomycetes. — Several  prominent  early  mycolo- 
gists and  algologists  believed  that  the  Phycomycetes  are  merely 
degenerate  algae,  which,  coincident  with  the  assumption  of  the 
parasitic  or  saprophytic  habit,  have  lost  their  ability  to  form 
chlorophyll.  Pringsheim  (1858),  one  of  the  first  students  of 
note  on  aquatic  Phycomycetes,  interpolated  the  genera  of  the 
Saprolegniales  among  those  of  the  siphonaceous  green  algae. 
Following  his  lead  Cohn  (1872)  and  Sachs  (1874)  proposed 
classifications  in  which  all  the  known  families  of  the  fungi  are 
scattered  among  those  of  the  algae.  In  the  arrangement  pre- 
sented by  Sachs,  the  Chytridiales  are  grouped  with  the  Protococ- 
coideae,  the  Oomycetes  with  the  Oosporeae,  the  Zygomycetes 
with  the  Conjugatae,  and  the  Ascomycetes  and  Basidiomycetes 
with  the  Florideae  (red  algae) .  These  writers  felt  that  the  change 
to  the  parasitic  or  saprophytic  mode  of  hfe,  accompanied  by 
the  loss  of  ability  to  form  chlorophyll,  had  occurred  at  various 
points  along  the  algal  line.  They  beheved  that  several  series 
of  non-chlorophyll  bearing  forms  had  been  thus  initiated.  Con- 
sequently, to  them  there  seemed  to  be  no  logical  basis  in  a  phy- 
logenetic  arrangement  for  segregation  of  the  colorless  forms  as 
a  separate  group.  This  point  of  view  was  generally  accepted  at 
the  time,  and  is  still  held  by  some  students.  Its  correctness  was 
first  seriously  questioned  by  de  Bary  (1881).  That  great  student 
of  mycology  agreed  that,  by  interpolation  of  the  colorless  forms 
among  the  green,  a  usable  arrangement  had  been  devised,  but 
he  doubted  that  it  constitutes  a  natural  system.  He  believed 
that  each  of  the  principal  subdivisions  of  both  the  fungi  and 
algae  has  its  own  lower  and  higher  forms,  and  argued  that  the 

21 


22  THE  LOWER  FUNGI— PHYCOMYCETES 

higher  members  of  any  one  group  show  relationship  with  the 
lower  members  of  the  groups  above.  He  felt  that  any  attempt 
to  merge  the  two  series  would  necessarily  result  in  the  dismember- 
ment of  both.  Since  the  physiological  processes  of  organisms 
possessing  chlorophyll  are  very  different  from  those  of  forms  in 
which  it  is  lacking,  it  seemed  highly  unlikely  to  him  that  the 
change  from  one  type  of  metabolism  to  the  other  had  occurred 
at  a  number  of  different  points  along  the  algal  line.  He  con- 
cluded finally  that  the  algae  and  fungi  probably  arose  as  separate 
groups  very  early  from  unicellular  chlorophyll  bearing  and  non- 
chlorophyll  bearing  organisms  respectively,  and  have  subse- 
quently evolved  along  more  or  less  parallel  lines.  The  rather 
constant  environmental  conditions  characterizing  the  aquatic 
habit  has  been  offered  in  explanation  of  the  development  of 
similar  structures  in  the  two  series. 

The  two  opposing  points  of  view  have  persisted  with  minor 
alterations  to  the  present  day.  In  most  standard  taxonomic 
works  the  ideas  of  de  Bary  have  prevailed,  and  the  algae  and  fungi 
are  treated  as  separate  groups.  In  America,  the  teachings  of 
Sachs  were  elaborated  by  one  of  his  students,  Charles  Bessey 
(1907;  1914),  at  the  University  of  Nebraska,  and  the  interpolation 
of  the  fungi  in  the  algal  series  constitutes  an  outstanding  feature 
of  the  system  of  classification  used  by  the  Bessey  school  of 
botanists  (Ernst  Bessey  1913).  Certain  other  students  of  the 
cryptogams  who  agree  in  regarding  the  fungi  as  degenerate 
algae  are  content  for  convenience  sake  to  have  the  two  groups 
treated  taxonomically  as  distinct. 

In  recent  years  de  Bary's  suggestion  that  the  two  series  have 
evolved  in  parallel  has  been  championed  by  various  students 
(Vuillemin,  1912).  In  America  this  point  of  view  was  given 
prominence  by  Atkinson  (1909;  1915).  He  presents  the  evidence 
indicating  that  the  fungi  have  in  fact  no  connection  with  the 
algal  line,  but  instead  have  been  derived  from  primitive  colorless 
organisms  below  the  level  of  the  existing  Chytridiales.  He 
emphasizes  the  fact  that  in  a  number  of  points  of  morphology 
and  behavior  the  lower  fungi  resemble  the  higher,  and  differ 
from  the  algae.  He  contrasts  the  zoospores  of  the  fungi  with 
those  of  the  algae,  finds  in  the  Chytridiales  the  origin  of  the 
phenomena  of  diplanetism  of  swarmspores  and  proliferation  of 
sporangia  characteristic  of  some  of  the  Saprolegniales,  sees  in 
certain  of  the  Chytridiales  and  Ancylistales  the  origin  of  the 


PHYCOMYCETES  23 

peculiar  type  of  sporangial  germination  present  in  Pythium, 
emphasizes  the  fact  that  the  sexual  organs  of  the  Oomycetes 
in  general  function  quite  differently  from  those  of  the  siphon- 
aceous  green  algae,  argues  that  the  Ascomycetes  and  Basidio- 
mycetes  are  connected  with  the  higher  Phycomycetes  through 
such  forms  as  Endogone  and  Dipodascus,  and  combats  the  point 
of  view  that  the  higher  fungi  arose  from  the  red  algae.  The 
student  interested  in  the  detailed  argument  is  referred  to  the 
papers  of  Atkinson  and  to  others  cited  in  his  bibliographies. 
An  adequate  elaboration  of  the  subject  here  does  not  seem  desir- 
able. The  writer,  who  was  a  student  under  Atkinson,  is  incHned 
to  accept  in  the  main  his  point  of  view  on  the  phylogeny  of  the 
fungi,  and  feels,  moreover,  that,  as  more  critical  and  comprehen- 
sive work  is  done  on  the  various  groups  of  lower  organisms,  a 
greater  body  of  evidence  will  be  assembled  justifying  it. 

Thallus. — GeneraHzations  concerning  the  morphology  of  the 
Phycomycetes  are  difficult  on  account  of  the  great  diversity  of 
the  group.  The  vegetative  portion  of  the  plant  in  the  primitive 
members  of  the  class  is  inconspicuous  and  simple.  In  the 
higher  forms  it  develops  into  a  profusely  branching  and  extensive 
mycelium.  Though  the  mycelium  in  the  group  as  a  whole  is 
characteristically  coenocytic  (i.e.,  non-septate  and  plurinucleate), 
in  some  of  the  higher  families  septa  are  commonly  present.  In 
the  Mucorales  they  are  found  usually  only  in  old  hyphae.  In 
the  Entomophthorales  their  formation  occurs  in  most  forms 
rather  early.  Even  in  typically  coenocytic  thalh  septa  are 
almost  invariably  formed  in  the  delimitation  of  the  reproductive 
cells  (sporangia,  antheridia,  and  oogonia).  In  certain  lower 
groups  {e.g.,  Cladochytriaceae)  the  mycehum  is  often  evanescent. 
In  the  Entomophthorales  it  commonly  falls  apart  at  the  septa 
into  the  component  cells. 

When  the  mycelium  is  coenocytic  it  is  considered  by  many 
writers  to  be  a  single  cell  regardless  of  its  extent  or  the  profusion 
of  its  branching.  Others  regard  each  nucleus  with  the  immedi- 
ately adjacent  enveloping  cytoplasm  as  constituting  a  cell.  An 
interesting  application  of  the  latter  point  of  view  is  seen  in  the 
use  of  the  term  gametes  for  the  nuclei  of  the  plurinucleate 
sexual  organs  (coenogametes)  of  this  group.  Regardless  of 
the  interpretation  accepted,  it  is  known  that  the  cytoplasm  and 
nuclei  commonly  flow  throughout  the  thallus,  and  there  is 
apparently  no  basis  for  an  assumption  that  definite  portions  of 


24  THE  LOWER  FUNGI— PHYCOMYCETES 

the  cytoplasm   maintain   a  constant  and   intimate  association 
with  individual  nuclei. 

The  thallus  of  the  Phycomycetes  is  usually  provided  with  a 
membrane  or  wall,  but  in  some  of  the  lower  groups  (Plasmodi- 
ophoraceae,  Woroninaceae)  it  is  naked  throughout  all  or  the 
major  portion  of  its  existence.  Although  the  wall  in  the  majority 
of  the  fungi  is  composed  of  fungus  cellulose  (a  substance  resem- 
bling chitin),  in  certain  members  of  the  Phycomycetes  it  gives 
the  reaction  for  pure  cellulose. 

In  some  of  the  lower  families  the  entire  thallus  is  transformed 
at  maturity  into  a  single  reproductive  organ  (Olpidiaceae)  or 
group  (sorus)  of  them  (Synchytriaceae).  In  such  cases  the 
organism  is  said  to  be  holocarpic.  In  the  higher  famihes,  only  a 
portion  of  the  thallus  is  transformed  for  purposes  of  reproduction, 
and  the  remainder  continues  to  function  vegetatively.  Such 
organisms  are  termed  eucarpic.  In  species  developing  abundant 
mycelium  the  reproductive  bodies  are  relatively  less  conspicuous 
than  the  thallus.  Prominent  compound  fructifications,  compara- 
ble to  those  of  the  Ascomycetes  and  Basidiomycetes,  are  almost 
wholly  absent.  A  tendency  toward  the  formation  of  such  struc- 
tures is  present  in  the  INIucorales  in  Endogone  and  to  a  lesser 
degree  in  Mortierella. 

Asexual  Reproduction.— In  the  Phycomycetes  asexual  repro- 
duction occurs  in  most  cases  by  means  of  spores  (sporangio- 
spores)  borne  in  unicellular  sacs  called  sporangia.  In  the 
lower  orders,  the  sporangiospores  are  usually  naked  and  motile 
and  are  termed  zoospores.  In  the  higher,  they  are  non-motile, 
have  definite  membranes,  and  may  be  designated  as  aplanospores. 
Though  in  a  few  of  the  lowest  forms  the  zoospores  arc  amoeboid, 
they  are  usually  ciliate  and  may  then  be  called  swarmspores. 
In  most  of  the  famihes  of  the  lowest  order  (Chytridiales)  they 
are  unicihate,  but  in  the  single  family  Woroninaceae  of  that  order 
and  in  almost  all  cases  in  higher  groups  they  are  biciUate.  When 
biciliate,  the  two  ciha  arise  from  the  same  point  on  the  swarm- 
spore.  In  some  genera,  one  cilium  is  markedly  longer  than  the 
other.  The  swarmspore  is  usually  either  pyriform  (pear-shaped) 
or  reniform  (bean-shaped),  the  ciha  being  attached  at  the  nar- 
rowed end  in  the  former  case  and  at  the  lateral  depression  (hilum) 
in  the  latter.  Zoospores  are  characteristic  of  the  more  primitive 
genera,  and  are  indicative  of  an  aquatic  or  semi-aquatic  habit. 
When  present  in  terrestrial  forms  they  swim  in  soil  water  or  on 


PHYCOMYCETES  25 

the  surfaces  of  hosts  wet  with  rain  or  dew.  Zoospores  are  not 
found  in  groups  above  the  level  of  the  Peronosporales.  They 
are  wholly  absent  in  the  Zygomycetes,  Ascomycetes,  and 
Basidiomycetes. 

The  number  of  spores  formed  in  the  sporangium  is  almost 
universally  indefinite,  but  in  a  few  genera  is  characteristically 
one  or  two.  In  the  group  as  a  whole  it  is  extremely  various 
(often  several  hundred),  and  is  chiefly  dependent  upon  the 
number  of  nuclei  which  chance  to  flow  in  from  the  thallus  below. 
The  sporangium  in  its  asexual  character,  and  in  the  indefinite 
number  of  its  spores  differs  strikingly  from  the  ascus.  Moreover, 
while  in  the  ascus  the  spores  are  delimited  by  the  astral 
rays,  in  the  sporangium  successive  cleavage  planes  traverse  the 
cytoplasm  and  in  a  wholly  indefinite  fashion  finally  cut  it  into 
bits  which  are  usually  uninucleate.  These  then  round  up  into 
spores.  There  remains  no  intersporal  cytoplasm  such  as  charac- 
terizes the  ascus.  The  essential  differences  between  spore  for- 
mation in  sporangium  and  ascus  are  indicated  by  Harper  (1899) 
and  Swingb  (1903). 

The  hypha  on  which  the  sporangium  is  borne  is  differentiated 
in  many  genera  as  a  definite  stalk  termed  the  sporangiophore.  In 
some  groups,  it  is  speciaUzed  in  form  and  may  be  characteristically 
branched. 

If  the  sporangium  forms  zoospores,  it  is  called  a  zoospor- 
angium.  If  the  spores  are  ciliated,  it  may  be  called  a  swarm- 
sporangium.  Zoospores  in  some  forms  escape  from  the 
sporangium  through  a  pore  or  exit  tube  of  definite  form  and  posi- 
tion. In  others,  the  sporangial  wall  disintegrates  or  bursts  in 
an  indefinite  fashion.  After  a  period  of  motihty  the  zoospores 
commonly  assume  the  spherical  form  and  become  enveloped  in  a 
definite  membrane.  Usually  they  then  put  out  one  or  more 
germ  tubes  and  germinate  directly  into  mycelium.  In  those 
lower  forms  in  which  mycelium  is  absent,  the  zoospore  merely 
enlarges  and  with  or  without  the  assumption  of  a  membrane 
develops  directly  into  the  thallus.  Aplanospores  are  chiefly 
wind  borne.  They  escape  from  the  sporangium  usually  by 
the  disintegration  of  its  wall  and  in  germination  form  germ 
tubes. 

In  many  cases  in  the  Phycomycetes,  especially  in  the  higher 
groups,  there  are  found  asexual  reproductive  cells  which  corre- 
spond in  size  and  form  with  the  sporangia,  are  unquestionably 


26  THE  LOWER  FUNGI— PHYCOMYCETES 

homologous  with  them,  and  differ  only  in  failing  to  develop 
endogenous  spores.  These  cells  function  at  maturity  in  their 
entirety  as  single  spores  and  germinate  by  one  or  more  germ 
tubes.  Such  reproductive  cells  correspond  morphologically  to 
the  conidia  of  the  higher  fungi  and  this  term  is  often  appHed 
to  them. 

The  conidium  of  the  higher  fungi  is  an  asexual  spore.  It  is 
usually  cut  off  from  a  definite  conidiophore,  is  deciduous, 
is  typically  wind  borne,  and  germinates  by  one  or  more  germ 
tubes,  never  by  endogenous  spores.  In  many  of  the  higher 
Phycomycetes  (e.g.,  Peronospora,  Cunninghamella,  Empusa) 
the  asexual  reproductive  cells  have  all  of  these  features.  In 
other  forms  (e.g.,  Saprolegnia,  Mucor)  they  have  the  charac- 
teristics of  the  typical  sporangium,  being  persistent  instead  of 
deciduous  and  germinating  by  endogenous  spores  instead  of  by 
germ  tubes.  In  intermediate  types  they  are  deciduous  but 
germinate  by  endogenous  spores  (e.g.,  Phytophthora,  Piloholus), 
or  are  persistent  but  germinate  by  germ  tube,  as  in  some  cases 
in  Pythium.  Furthermore,  forms  exist  (e.g.,  Phijiophthora, 
Plasmopara)  in  which  the  type  of  germination  is  unstable  and 
dependent  on  environmental  factors.  In  such  forms  two  asexual 
cells  identical  in  aspect  and  borne  on  the  same  hypha  may  be 
induced  to  germinate  differently  (one  by  germ  tube,  the  other 
by  endogenous  spores)  in  an  experiment  in  which  different 
temperatures  are  provided.  Consideration  of  these  facts  make 
it  evident  that  precision  in  the  application  of  the  terms  sporan- 
gium and  conidium  in  the  Phycomycetes  is  extremely  difficult 
of  attainment.  In  species  in  which  the  type  of  germination  is 
fixed  the  terms  may  be  used  without  ambiguity,  if  their  Hmits 
be  first  arbitrarily  defined,  though  all  writers  will  not  agree  as  to 
their  limits.  In  cases  in  which  the  method  of  germination  is 
dependent  on  environmental  factors  selection  of  the  name  must 
be  deferred  until  germination  has  actually  occurred.  Even  then 
it  is  sometimes  necessary  to  designate  either  as  sporangiophore 
or  conidiophore,  a  structure  on  which  both  sporangia  and 
conidia  have  been  borne. 

In  the  present  volume,  the  writer  has  attempted  to  avoid 
confusion  by  restricting  application  of  the  term  conidium  in 
the  Phycomycetes  to  the  Zygomycetes.  This  procedure  is 
purely  arbitrary.  The  border  Hne  conditions  which  exist  in 
the  Zygomycetes  are  less  confusing  than  those  in  the  lower  groups. 


PHYCOMYCETES  27 

and  it  is  possible  to  use  the  terms  sporangium  and  conidium 
together  there  with  less  difficulty. 

The  transition  from  the  typical  persistent  sporangium  of  the 
lower  Phy corny cetes  to  the  deciduous  conidium  of  the  higher 
has  been  accompHshed  in  various  ways  in  different  groups. 
While  in  the  Peronosporales  the  transition  has  been  marked 
by  a  rather  abrupt  change  from  the  swarmspore  type  of  germina- 
tion to  the  germ  tube  type,  in  the  Mucorales  gradual  and  pro- 
nounced changes  in  morphology  have  occurred.  In  the  latter 
order  the  sporangium  has  tended  to  decrease  in  size,  to  become 
few-spored,  and  to  fall  away.  The  small  few-spored  sporangia 
thus  resulting  have  been  termed  sporangiola.  In  some  cases 
they  are  monosporic,  the  wall  of  the  spore  being  clearly  discerni- 
ble within  that  of  the  sporangiolum.  In  their  highest  develop- 
ment, the  spore  wall  fails  to  form,  and  the  whole  cell  is  then 
termed  a  conidium. 

In  various  genera  of  the  Phycomycetes  {e.g.,  Saproleg?iia, 
Miicor)  an  additional  asexual  spore  form  is  present,  which  cannot 
be  clearly  homologized  with  the  sporangium.  These  spores 
have  been  termed  chlamydospores  or  gemmae.  They  occur 
chiefly  on  old  thalli,  and  are  essentially  merely  vegetative  cells 
with  thickened  walls.  Similar  spores  are  not  uncommon  among 
the  higher  fungi.  They  function  as  resting  spores  and  germinate 
by  germ  tube.  They  are  more  often  intercalary  than  terminal, 
and  usually  are  not  deciduous. 

Sexual  Reproduction. — A  comprehensive  general  discussion 
of  the  phenomena  of  sexuality  in  the  Phycomycetes  must  of 
necessity  be  somewhat  detailed.  Broad  general  statements  are 
impossible  on  account  of  the  great  variation  within  the  group. 
Several  distinct  types  of  sexuahty  occur,  and  a  consideration  of 
their  relationships  is  important  in  connection  with  questions  of 
phylogeny  and  classification. 

The  simplest  form  of  sexuality  represented  is  that  in  which 
swarmspore-like  cells,  called  gametes,  fuse  in  pairs  to  form 
motile  zygotes.  Because  the  fusing  cells  are  motile  the  process  is 
termed  planogamic  copulation.  As  they  are  morphologically 
indistinguishable  it  may  be  called  also  isogamy.  This  is  probably 
the  ancestral  type  of  sexuahty  in  the  group.  It  persists  today  in 
a  few  known  cases,  e.g.,  Olpidium  viciae  (p.  75)  and  Syncluj- 
trium  endobioticum  (p.  82),  and  perhaps  is  present  in  a  consider- 
able number  of  other  incompletely  investigated  members  of  the 


28  THE  LOWER  FUNGI— PHYCOMYCETES 

Chytridiales,  especially  those  having  resting  spores  of  unknown 
origin.  This  type  of  sexual  process  probably  originated  very 
early  in  the  copulation  of  swarm  cells  in  species  in  which  such 
cells  had  functioned  previously  only  asexually  as  swarmspores. 
In  the  relatively  few  present-day  Phycomycetes  in  which  such 
swarm  cells  fuse  as  gametes,  there  occur  in  the  life  cycle  other 
cells  of  identical  aspect  which  still  function  as  swarmspores.  The 
rather  meager  data  gained  from  observations  indicate  that  the 
three  sorts*  of  swarm  cells  (swarmspores,  male  gametes,  and 
female  gametes)  are  delimited  in  different  parent  cells.  The  cell 
in  which  the  swarmspores  are  borne  is  called  the  sporangium. 
Those  in  which  the  gametes  are  formed  are  termed  respectively 
the  male  and  female  gametangia.  The  three  sorts  of  parent 
cells  are  morphologically  indistinguishable.  Considerable  evi- 
dence indicates  that  during  the  period  of  active  growth  while 
the  food  supply  is  abundant  and  other  conditions  favorable  the 
fungus  forms  several  successive  generations  of  swarmspores,  and 
that  when  conditions  become  unfavorable  and  the  rest  period  is 
approached  gametes  are  produced  instead.  In  parasitic  species, 
infection  of  the  host  is  accomplished  by  either  swarmspores  or 
zygotes.  After  the  gametes  fuse  the  zygote  (planozygote)  is 
motile  for  a  time,  but  finally  comes  to  rest,  rounds  up,  increases 
considerably  in  size,  and  at  maturity  develops  into  the  resting 
spore.  As  the  resting  spore  in  germination  frees  swarmspores, 
it  may  be  termed  also  the  resting  sporangium.  The  term 
zygospore,  used  for  similar  structures  in  certain  algae,  is  avoided 
here  since  it  has  become  fixed  in  its  application  in  a  different  sense 
in  the  group  of  higher  Phycomycetes  called  the  Zygomycetes. 

As  has  been  indicated  above  the  species  representative  of  this 
type  of  sexuality  are  termed  isogamic,  because  the  fusing  gametes 
are  alike.  They  may  be  called  also  isogametangic  in  that 
their  gametangia  are  indistinguishable.  Though  no  isogamic 
species  known  at  present  are  heterogametangic  it  is  possible 
that  future  investigations  will  bring  to  light  forms  of  that  type 
also. 

In  those  Phycomycetes  in  which  planogamic  copulation  of  like 
gametes  occurs,  the  fusing  cells  and  the  resultant  zygote  are 
usually  both  ciliate.  However,  in  a  single  imperfectly  known 
species,  described  by  Griggs  (p.  75)  under  the  name  Mono- 
chrjtrium  stevensianum  the  gametes  are  non-ciliate  and  fuse  in 
the  amoeboid  condition.     Moreover,  in  two  species  of  Olpidium, 


PHYCOMYCETES  29 

segregated  long  ago  by  Fisch  (p.  75)  under  the  generic  name 
Reesia,  though  the  gametes  are  cihate,  the  zygote  is  finally  non- 
ciliate  and  amoeboid.  Such  forms  may  be  regarded,  perhaps, 
as  representing  transition  conditions  from  the  more  primitive 
type  of  sexuality  where  the  fusing  cells  are  ciliate  to  the  more 
recent  types  in  which  they  are  wholly  non-motile. 

Planogamic  copulation  between  cells  dissimilar  in  size  and 
shape  was  unknown  in  the  fungi  until  very  recently,  when  it  was 
discovered  by  Kniep   (p.    132)   in  Allomyces  javanicus  of  the 
Blastocladiaceae.     In  this  species  unicihate  gametes,  differing 
considerably  and  constantly  in  size,  fuse  to  form  a  biciliate 
zygote.     The  zygote  swims  for  a  time,  but  soon  invests  itself  in 
a  membrane,  and  puts  out  a  germ  tube  which  develops  directly 
into  the  rhizoid  system  comprising  the  young  thallus.     This 
species  in  addition  to  being  heterogamic   (anisogamic)  is  also 
heterogametangic.     The  gametangia,  though  of  essentially  the 
same  form,  are  of  two  sizes.     The  smaller  always  contains  the 
smaller   gametes,    while   the   larger   contains   the   larger   ones. 
Influenced    by   the    situation   in   other   higher    Phycomycetes, 
Kniep  regards  the  smaller  gametangium  as  male  and  the  larger 
as  female,  and  designates  the  two  as  antheridium  and  oogonium 
respectively.     As  the  larger  gametes  are  formed  in  the  larger 
gametangium,  it  must  be  admitted  that  the  only  criteria  avail- 
able for  a  determination  of  the  sexual  identity  of  these  structures 
indicate    that   they  are  female.     Nevertheless,  the  possibility 
remains  that  they  are  not.     Though  isogamic-heterogametangic 
or  heterogamic-isogametangic   members  of  the   Phycomycetes 
with  planogamic  copulation  have  not  been  discovered,  it  is  clear 
that  the  determination  of  sexual  identity  on  the  basis  of  size 
alone  would  be  even  more  questionable  in  such  cases.     It  is 
possible,  moreover,  that  heterogamic-heterogametangic  species 
with  planogamic  copulation  may  be  found  in  which  the  smaller 
gametes  are  borne  in  the  larger  gametangium  and  the  larger 
gametes  in  the  smaller.     Even  admitting  that  these  hypothetical 
types  may  be,  in  fact,  wholly  absent  in  the  group  it  will  be 
agreed  that  every  effort  should  be  made  to  attain  uniformity 
and  precision  in  the  application  of  terms.     To  this  end  the 
writer  prefers  to  avoid  the  use  of  the  names  oogonium  and 
antheridium  in  this  lower  form  in  which  both  gametes  are  motile. 
If  the  larger  gamete  in  Allomyces  javanicus  be  admitted  to  be  the 
female  then  the  type  of  sexuality  existing  in  this  isolated  case 


30  THE  LOWER  FUNGI—PHYCOMYCETES 

may  fairly  be  regarded  as  intermediate  between  the  planogamic 
copulation  of  isogametes  in  Olpidium  or  Synchytrium,  and 
heterogamic  copulation  as  it  exists  in  Monohlepharis  where  the 
female  gamete  is  practically  non-motile  and  spherical.  Since 
in  other  respects  the  Blastocladiaceae  and  Monoblepharidaceae 
are  clearly  closely  related  a  similarity  in  their  sexual  process  is 
not  surprising. 

The  type  of  heterogamic  copulation  represented  by  Mono- 
hlepharis  is  clearly  higher  than  that  in  Allomyces  in  that  the 
gametes  are  easily  distinguishable  as  male  and  female  respec- 
tively. They  are  not  merely  dissimilar  in  size.  They  differ 
in  other  respects  as  well.  From  the  beginning  the  female  game- 
tangium  is  uninucleate.  Finally  its  contents  contract  to  form 
a  single,  large,  spherical,  naked,  non-ciliate  and  practically  non- 
motile  gamete,  which  is  here  called  the  oosphere.  The  male 
gametangium  is  smaller  than  the  female  and  of  a  somewhat 
different  shape.  At  maturity  it  frees  several  uninucleate, 
unicihate  gametes.  These  swim  about  actively  and  are  attracted 
to  the  oosphere.  They  are  termed  antherozoids  (sperms, 
spermatozoids).  An  anthcrozoid,  on  coming  in  contact  with 
the  oosphere,  fuses  with  it,  and  its  nucleus  approaches  and 
unites  with  the  female  nucleus.  This  fusion  of  the  sexual  nuclei 
is  termed  fertilization,  and  the  female  nucleus  is  said  to  have 
been  fertilized.  Following  fertilization  the  oosphere  assumes 
a  wall,  and  thereafter  is  called  the  oospore.  The  oospore 
functions  as  a  resting  spore,  and,  after  a  period  of  quiescence, 
puts  out  a  germ  tube  which  develops  into  a  new  thallus. 

The  female  character  of  the  oosphere  is  evident  in  that  it 
is  functionally  the  receiving  cell,  remaining  passive  until  ap- 
proached and  fertilized  by  the  male  gamete,  and  in  that  it 
has,  thereafter,  the  capacity  for  developing  into  the  new  plant. 
The  gametangium  which  bears  the  oosphere  is  from  that  fact 
alone  clearly  the  female,  and  may  be  called  without  hesitation 
the  oogonium.  The  antherozoids  are  surely  male  in  that  they 
effect  fertilization  of  the  oospheres.  The  gametangium  in 
which  they  are  formed  is  consequently  male  and  is  termed 
the  antheridium.  The  larger  size  of  the  female  gamete  and 
gametangium  is  pronounced  and  corresponds  in  general  with 
the  situation  in  all  higher  oospore-forming  Phycomycetes. 
Monoblepharis  is  noteworthy  in  that  it  is  the  only  genus  of  the 
known   Phycomycetes  in   which   ciliate  male  gametes  fertilize 


PHYCOMYCETES  31 

the  oosphere.  It  is  unique  also  in  that  the  terms  oosphere  and 
female  gamete  may  be  apphed  here  with  complete  justification 
to  the  same  body. 

In  many  other  genera  of  the  Phycomycetcs  fertilization  is 
immediately  preceded  or  accompanied  by  a  differentiation  of 
the  contents  of  the  female  gametangium  to  form  one  or  more 
spherical  masses  of  protoplasm.  Though  these  are  commonly 
called  oospheres  they  are  not  completely  homologous  with  the 
oosphere  of  Monohlepharis,  since  they  are  in  the  beginning 
multinucleate.  Phycomycetes  having  oospheres  of  this  sort 
include  such  genera  as  Achlya,  Didyuchus,  Pythium,  Albugo, 
and  Peronospora.  In  no  case  of  this  type  does  the  male  game- 
tangium form  antherozoids.  Instead  it  pushes  out  a  branch, 
called  the  fertilization  tube,  which  pierces  the  wall  of  the  female 
gametangium  and  penetrates  to  the  oosphere  before  rupturing 
and  discharging  a  part  or  all  of  its  contents.  When  the  oogonium 
contains  several  oospheres  the  tube  branches,  or  several  anther- 
idia  may  send  tubes  into  a  single  oogonium.  In  all  such  cases 
the  male  and  female  gametangia  are  both  plurinucleate  from  the 
first.  In  the  more  primitive  genera  (e.g.,  Achlya  and  Didyuchus) 
the  entire  content  of  the  oogonium  is  used  in  the  formation 
of  the  oospheres,  whether  there  be  one  or  more.  In  higher 
forms  (e.g.,  Albugo,  Pythium,  Araiospora,  and  Peronospora) 
differentiation  of  the  protoplasm  into  periplasm  and  ooplasm 
occurs,  and  only  the  ooplasm  is  incorporated  in  the  single 
oosphere  formed  in  these  genera.  The  oosphere  in  the  begin- 
ning is  plurinucleate.  Later  it  usually  becomes  uninucleate, 
through  disintegration  of  the  extra  (supernumerary)  nuclei, 
before  fertilization  occurs.  In  a  few  species  (e.g.,  Albugo  bliii) 
the  oosphere  remains  plurinucleate  and,  when  fully  formed,  is 
fertilized  by  a  number  of  male  nuclei  which  are  discharged 
from  the  fertihzation  tube  and  fuse  in  pairs  with  the  female 
nuclei.  Even  in  the  forms  in  which  the  plurinucleate  oosphere 
becomes  uninucleate  before  fertihzation  the  body  may  not  be 
correctly  termed  a  gamete  except  with  respect  to  function  since 
in  the  morphological  and  phylogenetic  senses  several  potential 
gametes  contribute  to  the  formation  of  each  oosphere.  In 
species  in  which  the  oosphere  remains  plurinucleate  to  maturity 
the  terms  compound  oosphere  and  coenogamete  have  been 
applied  by  various  authors.  To  the  student  of  comparative 
morphology  the  latter  name  seems  especially  unfortunate.     The 


32  THE  LOWER  FUNGI— PHYCOMYCETES 

nuclei  which  fuse  here  are  clearly  in  their  homologies  the  gametic 
nuclei,  and  it  may  well  be  said  that  here  fusion  of  undifferenti- 
ated gametes  occurs.  The  oosphere  in  such  cases  is  thus  not 
comparable  morphologically  to  the  gamete  in  Monohlepharis 
but  is  instead  an  aggregation  of  non-individualized  gametes 
functioning  in  its  entirety  as  a  single  gamete. 

The  same  situation  exists  in  the  case  of  the  antheridium.  In 
species  in  which  the  oosphere  remains  plurinucleate  to  maturity 
numerous  antheridial  nuclei  function.  In  species  in  which  the 
mature  oosphere  is  uninucleate  conditions  are  various.  In  some 
cases  only  a  single  male  nucleus  passes  through  the  fertilization 
tube.  In  others  supernumerary  antheridial  nuclei  enter  the 
oosphere,  and,  on  failing  to  find  mates,  disintegrate.  In  some 
of  the  higher  genera  (Peronosporales)  the  content  of  the  anther- 
idium is  differentiated  into  a  central  mass  of  functional  gonoplasm 
which  passes  through  the  tube,  and  a  layer  of  periplasm  which 
remains  in  the  antheridium.  In  these  various  cases,  the  anther- 
idial nuclei,  whether  functional  or  not,  are  termed  gametes  or 
gametic  nuclei  by  many  writers.  The  term  coenogamete  is 
used  by  other  authors,  and  is  applied  to  the  content  of  the  anther- 
idium considered  as  a  unit.  After  fertilization  has  been  effected, 
the  antheridium  tends  to  collapse,  and  is  of  no  further  significance 
in  the  Ufe  cycle.  Meanwhile  in  the  oogonium,  the  oosphere 
assumes  a  wall,  and  thereby  becomes  the  oospore.  The  oospore 
functions  as  a  resting  spore,  and  finally  germinates  to  form  the 
thallus  of  the  succeeding  generation. 

The  fungi  which  form  oospheres  were  called  Oomycetes  (egg- 
forming  moulds)  by  early  students.  The  name  has  persisted, 
and,  in  most  modern  classifications,  is  appHed  to  one  of 
the  primary  subdivisions  of  the  Phycomycetes.  The  type  of 
sexual  reproduction  characterized  by  oosphere  formation  is 
termed  oomycetous.  The  term  oospore  is  used  correctly  only 
for  the  spore  which  results  directly  from  the  maturation  of  the 
oosphere. 

Though  the  delimitation  of  the  oosphere  and  its  transforma- 
tion into  the  oospore  are  the  most  essential  characteristics  of 
oomycetous  reproduction  several  other  features  of  this  type  of 
sexuality  are  commonly  present  and  should  be  indicated.  The 
sexual  identity  of  the  male  and  female  gametangia  is  evident. 
They  differ  in  size  and  shape,  the  female  being  the  larger  and 
typically  the  more  nearly  globose.     They  differ  also  in  function, 


PHYCOMYCETES  33 

the  male  cell  being  more  active,  and  contributing  to  the  more  pas- 
sive and  receptive  female  cell  which  then  matures  the  oosphere. 
The  fertihzation  tube,  present  in  all  forms  but  Monohlepharis, 
does  not  function  as  a  conjugation  tube.  Instead  of  copulating 
with  the  oogonium,  it  pierces  the  oogonial  wall  and  penetrates 
to  the  oosphere.  Properly  speaking,  therefore,  copulation 
between  the  gametangia  does  not  take  place,  and  as  they  do  not 
merge  to  form  a  common  cell  their  individuality  is  retained  even 
after  fertilization. 

Contrasting  in  the  higher  Phycomycetes  with  oomycetous 
reproduction  is  a  wholly  different  type  of  sexuality  termed 
zygomycetous.  It  is  present  in  many  genera,  and  these  con- 
sidered as  a  group  are  called  the  Zygomycetes,  In  these  forms 
differentiation  of  the  female  gametangium  to  form  oospheres 
does  not  occur,  and  the  end  product  of  the  sexual  process  is 
termed  the  zygospore.  The  male  and  female  gametangia  are 
usually  morphologically  identical,  and  are  not  designated  by  the 
names  antheridium  and  oogonium.  In  a  few  genera  (e.g., 
Zygorhynchus)  they  show  a  pronounced  and  constant  difference 
in  size  and  shape,  but  the  character  of  the  sexual  process  is  such 
that  the  larger  cell  may  not  be  regarded  with  certainty  as  the 
female.  Direct  copulation  of  the  gametangia  takes  place  in  all 
cases,  the  contiguous  walls  of  the  two  sexual  organs  are  absorbed, 
and  a  common  cell  results  in  which  the  two  protoplasts  are  com- 
pletely merged.  In  many  genera  the  fusion  cell  then  enlarges 
and  the  individuahty  of  the  copulating  gametangia  is  completely 
obliterated.  In  other  cases  only  a  pore  is  formed  between  the 
two  cells,  and,  though  a  fusion  cell  thus  results,  the  identity  of 
the  gametangia  is  retained.  Finally,  the  fusion  protoplast 
rounds  up,  assumes  a  wall,  and  matures  into  the  zygospore.  In 
some  species  one  gametangium  or  the  other  forms  the  zygospore. 
In  others  it  fills  the  common  cavity  resulting  from  their  complete 
fusion.  In  still  others  it  exists  as  a  globose  bud  protruding  from 
one  of  the  gametangia  or  from  their  point  of  union.  It  is  not 
clearly  an  endogenous  spore.  The  gametangial  wall  enveloping 
the  fusion  protoplast  becomes  greatly  thickened  and  when  thus 
transformed  serves  as  the  wall  of  the  spore.  The  zygospore 
differs  from  the  oospore  is  not  lying  free  in  the  gametangium. 
Fusion  of  one  or  more  pairs  of  sexually  different  nuclei  occurs 
in  the  zygospore,  nuclear  conditions  varying  apparently  in 
different  species.     Functionally  the  zygospore  corresponds  with 


34  THE  LOWER  FUNGI— PHYCOMYCETES 

the  oospore  in  being  a  resting  spore.  After  a  period  of  quiescence 
it  germinates  by  a  germ  tube. 

It  is  evident  that  the  zygomycetous  type  of  reproduction 
differs  from  the  oomycetous  essentially  in  that  the  oosphere  is 
lacking,  and  the  sexual  identity  of  the  interacting  gametangia 
is  in  doubt.  It  differs  also  in  that  true  gametangial  copulation 
occurs.  As  there  is  no  oosphere  the  fertilization  tube  is  unneces- 
sary and  is  lacking,  and  the  resting  spore  tends  to  fill  the  cell 
instead  of  lying  free  as  in  the  Oomycetes. 

These  various  features  of  dissimilarity  considered  together 
indicate  clearly  that  the  Oomycetes  and  Zygomycetes  are  not 
closely  related.  Though  presumably  at  a  remote  period  they 
had  a  common  ancestry,  it  is  evident  that  they  represent  two 
series  of  genera  which  have  arisen  in  parallel  from  still  lower 
forms.  The  probable  line  of  development  of  the  Oomycetes 
from  primitive  aquatic  forms  with  planogamic  copulation  has 
been  indicated  above.  The  origin  of  the  Zygomycete  line  is 
somewhat  more  obscure,  though  forms  possessing  one  or  more 
undoubted  zygomycetous  characters  exist  among  the  Ancylistales 
and  Chytridiales. 

In  certain  of  these  lower  Phycomycetes  primitive  types  of 
sexuality  exist  in  which  oomycetous  and  zygomycetous  charac- 
ters are  found  associated  in  the  same  species.  These  cases  have 
been  inadequately  studied,  and  knowledge  of  them  is  too  frag- 
mentary to  justify  conclusions  as  to  their  relationships.  It 
has  long  been  known  that  in  some  of  the  Chytridiales  (e.g., 
Olpidiopsis  and  Pseudolpidiopsis)  the  resting  spore  is  accom- 
panied at  maturity  by  one  or  more  small  empty  appendages. 
Early  investigators,  ignorant  of  the  real  nature  of  these  struc- 
tures, called  them  companion  cells.  Now  they  are  known  to 
be  emptied  male  cells.  Though  few  Chytridiales  having  com- 
panion cells  have  been  studied  critically  they  are  apparently  all 
endophytic  parasites,  and  their  life  history  is  believed  to  be 
essentially  as  follows.  Ciliated,  free-swimming  swarm  cells 
exist  in  the  water  outside  the  host,  and  in  all  cases  function  as 
swarmspores.  There  'is  no  basis  for  an  assumption  that  any 
of  them  ever  act  as  gametes,  as  in  Olpidium  viciae.  All  are 
apparently  capable  of  accompHshing  infection.  On  coming  in 
contact  with  the  host  the  swarmspore  rounds  up,  effects  pene- 
tration, and  comes  to  lie  within  the  host  cell,  where,  for  a  brief 
period  at  least,  it  exists  as  a  naked  protoplast.     It  gradually 


PHYCOMYCETES  35 

increases  in  size  at  the  expense  of  the  host  protoplasm  and  during 
the  period  of  vegetative  growth  is  termed  the  thallus.  At 
maturity  it  possesses  a  membrane  and  functions  as  a  sporangium, 
freeing  swarmspores  which  pass  to  the  outside  of  the  host  through 
a  more  or  less  elongate  exit  tube.  When  two  or  more  swarm- 
spores enter  the  same  host  cell  the  resultant  thalli  sometimes 
copulate.  Though  the  details  of  the  sexual  process  in  such 
cases  are  not  well  known  and  may  differ  in  different  species,  there 
always  exists  in  later  stages  a  larger  thallus  united  with  one  or 
more  smaller  thalli  by  open  pore  connections.  The  whole  content 
of  the  smaller  cell  or  cells  enters  the  larger  cell,  and  it  then 
assumes  a  thick  wall  and  matures  into  the  resting  spore.  Pre- 
sumably, therefore,  the  larger  cell  is  female  and  the  smaller  cells 
are  male.  At  least  in  some  species  {e.g.,  Olpidiopsis  vexans)  it 
is  known  (Barrett  1912)  that  both  the  male  and  female  cells  have 
become  plurinucleate,  through  division  of  the  primary  swarm- 
spore  nuclei,  before  the  male  cells  have  discharged  their  contents 
into  the  female.  Whether  at  the  moment  of  their  initial  contact 
the  copulating  cells  are  already  provided  with  thin  membranes 
is  not  certainly  known,  but  seems  likely.  If  they  were  then  still 
naked  protoplasts  their  complete  merging  to  form  a  fusion  cell, 
as  in  Monochytrium,  would  probably  occur.  The  very  early 
stages  in  the  process  are  unknown.  Though  the  copulating 
cells  differ  in  size  from  an  early  period,  it  is  possible  that  at  the 
beginning  of  their  association  they  are  morphologically  equiv- 
alent. When  the  male  nuclei  enter  the  female  cell  they  appear 
to  fuse  in  pairs  with  the  female  nuclei.  The  female  cell  finally 
assumes  a  thick  wall,  and  is  transformed  directly  into  the  resting 
spore.  The  use  of  the  term  oospore  or  zygospore  in  such  cases 
results  only  in  indefiniteness.  The  .sexual  process  is  clearly 
neither  typically  oomycetous  nor  typically  zygomycetous.  In 
the  Ancylistales  other  intermediate  types  occur,  and,  though 
that  group  as  a  whole  is  placed  by  some  students  in  the  Oomy- 
cetes,  zygomycetous  tendencies  in  some  of  the  genera  at  least 
{e.g.,  Ancylistes)  are  seen  in  the  absence  of  the  oosphere  and  the 
direct  copulation  of  the  gametangia.  In  this  order  copulation 
is  effected  in  some  cases  by  means  of  a  conjugation  tube.  In 
Zygorhizidium  willei  and  Polyphagus  euglenae  of  the  Chytridiales 
uninucleate  thalli  copulate  in  similar  fashion  by  means  of  a 
conjugation  tube.  The  individual  putting  out  the  tube  is  usually 
considered  to  be  from  that  fact  alone  clearly  the  male.     It  is  of 


36  THE  LOWER  FUNGI— PHYCOMYCETES 

interest,  nevertheless,  to  note  that  the  resting  spore  in  Poly^ 
phagus  is  formed  in  the  tube  rather  than  in  the  so  called  female 
individual. 

A  consideration  of  these  variations  in  the  sexual  process  as 
exhibited  in  the  lower  Phycomycetes  indicates  clearly  that 
various  primitive  types  of  sexuality  exist  here  which  are,  strictly 
speaking,  neither  oomycetous  nor  zygomycetous.  Some  of  these 
probably  represent  lateral  lines  of  development  or  terminations 
of  series  having  little  if  any  connection  with  the  two  main  lines 
ending  in  the  higher  Oomycetes  and  Zygomycetes.  Until  these 
lower  forms  have  been  studied  much  more  thoroughly  the  solu- 
tion of  the  problem  of  their  interrelationships  cannot  be  reached. 

In  numerous  genera  of  the  Phycomycetes,  species  have  been 
described  in  which  a  sexual  stage  is  not  as  yet  known  to  occur. 
In  primitive  members  of  the  group,  such  as  the  lower  Chytrid- 
iales,  it  is  possible  that  some  of  these  are  forms  in  which  sex- 
uality has  not  yet  arisen.  In  the  higher  Phycomycetes  absence 
of  a  known  sexual  stage  may  be  due  to  the  existence  in  the  species 
of  a  heterothallic  condition,  i.e.,  segregation  of  sex  in  such  a 
fashion-  that  constantly  some  thalli  are  wholly  male  while  others 
are  wholly  female.  In  such  heterothallic  species  the  presence 
of  both  sorts  of  thalli,  and  in  most  cases  their  actual  contact,  is 
necessary  before  a  sexual  union  can  be  effected.  It  is  possible 
that  in  some  species  one  of  the  two  sorts  of  thalli  has  died  out 
completely,  leaving  the  species  unisexual.  When  both  sexes 
occur  in  the  same  thallus  the  species  is  termed  homothallic. 
Failure  of  a  homothallic  species  to  form  sexual  spores  is  usually 
attributed  to  unfavorable  features  of  nutrition  or  other  environ- 
mental factors.  These  factors  are  as  yet  only  imperfectly 
understood. 

The  gametangia  of  the  Phycomycetes  are  usually  functional. 
However,  in  several  families  (e.g.,  Saprolegniaceae,  Mucoraceae, 
Entomophthoraceae)  sexual  organs  of  normal  aspect  may  fail  to 
react  sexually.  In  these  cases  spores  morphologically  equiva- 
lent to  the  sexual  spores  are  formed  parthenogenetically.  In 
the  Zygomycetes  such  spores  have  long  been  termed  azygospores. 
In  the  Oomycetes  they  may  well  be  called  aboospores.  They  are 
capable  of  germination  and  the  production  of  normal  thalli. 
Though  the  chromosome  condition  in  such  cases  has  not  been 
compared  with  that  in  normally  sexual  species  it  is  probably 
unchanged  throughout  the  entire  hfe  cycle.     Since  the  fusion 


PHYCOMYCETES  37 

nucleus  of  the  mature  oosphere  is  normally  the  only  nucleus 
with  the  double  chromosome  number  it  is  usual  to  regard  the 
oospore  as  sporophytic,  and  since  the  fusion  nucleus  is  thought 
to  undergo  immediate  reduction  in  all  members  of  the  group  the 
remainder  .of  the  cycle  is  termed  gametophytic.  Consequently 
forms  which  mature  the  oospore  without  fertilization  are  regarded 
as  apogamous.  Oomycetes  in  which  oospores  form  in  the  com- 
plete absence  of  the  antheridium  are  termed  apandrous. 

Classification. — The  taxonomic  study  of  the  fungi  has  engaged 
the  attention  of  mycologists  for  two  hundred  years.  During 
this  period  various  systems  of  classification  have  been  proposed. 
Early  students  were  content  with  any  orderly  arrangement  of 
genera  which  placed  together  fungi  of  similar  morphology. 
Modern  workers  have  sought  to  provide  a  natural  scheme  of 
classification  representing  phylogenetic  relationships. 

At  the  beginning  of  this  chapter,  it  has  been  shown  that  two 
outstanding  points  of  view  exist  with  respect  to  the  origin  of 
the  fungi.  Some  students  regard  the  group  as  monophyletic. 
Others  look  upon  it  as  merely  an  assemblage  of  relatively  unre- 
lated forms,  which  have  degenerated  along  several  different 
lines  from  the  algae.  Until  general  agreement  is  reached  as  to  the 
origin  of  the  group,  it  is  evident  that  no  one  system  of  classifica- 
tion will  receive  the  unqualified  endorsement  of  all  authorities. 
It  is  true,  also,  that  even  an  admittedly  excellent  classification 
has  only  temporary  value.  Investigation  is  constantly  bringing 
to  light  new  facts,  and  these  at  times  change  points  of  view  and 
necessitate  alteration  in  the  content  of  groups  and  in  their 
arrangement.  It  is  not  likely  that  any  classification  will  ever 
be  accepted  as  permanent. 

The  Phycomycetes  are  usually  treated  as  a  unit,  and  constitute 
the  lowest  of  the  three  primary  subdivisions  (classes)  into  which 
the  fungi  are  customarily  divided.  The  number  and  content 
of  the  orders  and  families  making  up  the  Phycomycetes  do  not 
differ  greatly  in  the  various  well  known  modern  separations, 
but  no  two  classifications  are  wholly  alike.  No  one  of  them  has 
been  accepted  generally  as  the  standard.  The  best  known 
treatments  are  those  of  Schroter  (1892-1893)  and  Fischer  (1892) 
published  at  practically  the  same  time  nearly  forty  years  ago. 
Though  now  much  out  of  date,  they  are  still  used  by  many 
students.  In  the  classification  of  Schroter  the  Phycomycetes 
are  separated  into  two  sub-classes,  (1)  the  Oomycetes,  embracing 


38  THE  LOWER  FUNGI—PHYCOMYCETES 

the  orders  Chytridineae,  Ancylistineae,  Monoblepharidineae, 
Saprolegnineae,  and  Peronosporineae,  and  (2)  the  Zygomycetes, 
including  the  Mucorineae  and  Entomophthorineae.  Fischer 
recognizes  three  primary  subdivisions,  Archimycetes,  Oomycetes, 
and  Zygomycetes.  In  the  Archimycetes  he  includes  the  genera 
incorporated  by  Schroter  in  the  Chytridineae  and  Ancylistineae. 
In  erecting  this  group  he  emphasizes  the  fact  that  in  these  forms 
mycelium  is  absent  or  poorly  developed  and  sexual  reproduction 
uncommon.  In  both  classifications,  the  separation  of  the 
Oomycetes  and  Zygomycetes  is  based  on  the  essential  difference 
in  the  sexual  process,  oospores  being  characteristic  of  the  former 
and  zygospores  of  the  latter.  The  two  classifications  differ 
further  in  several  minor  respects.  The  Pythiaceae,  included 
in  the  Saprolegnineae  by  Schroter,  are  incorporated  in  the 
Peronosporineae  by  Fischer,  and  the  Monoblepharidineae  of 
Schroter  are  treated  as  a  family  of  the  Saprolegnineae  by  Fischer. 
Generic  limits  in  the  two  separations  are  not  in  all  cases  identical, 
as  will  be  emphasized  in  later  pages. 

In  recent  years,  two  other  taxonomic  treatments  of  the  Phy- 
comycetes  have  appeared,  which  are  sufficiently  outstanding  to 
require  special  consideration.  These  have  been  presented  by 
von  Minden  (1911)  and  Gaumann  (1926).  The  classification  of 
von  Minden  is  intermediate  in  several  respects  between  the 
separations  of  Schroter  and  Fischer.  While  he  does  not  recog- 
nize the  group  Archimycetes,  and  his  ordinal  separations  cor- 
respond essentially  with  those  of  Schroter,  he  includes  the 
Pythiaceae  in  the  Peronosporineae  and  in  numerous  other  details 
follows  Fischer.  His  paper  as  a  whole  is  the  most  modern  of 
the  taxonomic  treatments  providing  keys  to  families  and  genera. 
Gaumann  concerns  himself  chiefly  with  problems  of  comparative 
morphology,  and  does  not  attempt  a  complete  taxonomic  sepa- 
ration. He  removes  the  Olpidiaceae,  Synchytriaceae,  Plas- 
modiophoraceae,  and  Woroninaceae  from  the  Phycomycetes 
and  treats  them  as  a  lower  group  to  which  he  applies  the  name 
Archimycetes.  The  Rhizidiaceae,  Hyphochytriaceae,  and  Clado- 
chytriaceae  comprise  the  Chytridiales  in  his  arrangement. 
He  divides  the  Phycomycetes  into  Chytridiales,  Oomycetes, 
and  Zygomycetes.  The  Oomycetes  include  the  Monoblephari- 
daceae,  Blastocladiaceae,  Ancylistaceae,  Saprolegniaceae,  Lep- 
tomitaceae,  and  Peronosporaceae.  The  Zygomycetes  include 
the  Mucoraceae,  Endogonaceae,  and  Entomophthoraceae.     The 


PHYCOMYCETES  39 

recently  published  book  by  Gaumann  and  Dodge  (1928)  is  a 
translation  of  this  work  of  Gaumann.  No  attempt  will  be 
made  at  this  point  to  criticize  or  explain  the  various  pronounced 
changes  advocated  by  Gaumann.  In  some  cases  this  is  done  on 
the  pages  which  follow  in  connection  with  the  groups  concerned. 

In  presenting  the  ordinal  and  family  separations  which  appear 
in  the  present  work  the  writer  has  tried  to  maintain  a  conserva- 
tive point  of  view.  Changes  from  the  older  established  arrange- 
ments have  been  made  only  when  they  were  clearly  unavoidable. 
In  such  cases  adequate  explanations  have  been  given.  The 
inclusion  of  the  Plasmodiophoraceae  in  the  Chytridialcs  and 
the  recognition  of  the  order  Blastocladiales  constitute  instances 
of  this  sort.  On  the  whole  the  classification  does  not  depart 
far  from  the  older  established  points  of  view.  The  terminations 
-ales  and  -aceae  for  ordinal  and  family  names  respectively  are 
those  recommended  by  the  International  Rules  of  Botanical 
Nomenclature  (Briquet  1912).  They  are  now  generally  used 
in  the  taxonomic  literature. 

Though  the  eight  orders  into  which  the  Phycomycetes  are 
separated  in  the  following  key  constitute  rather  definitely 
delimited  groups,  they  tend  to  merge  somewhat  at  their  border 
lines.  This  is  to  be  expected  in  any  natural  system.  If  the 
sum  total  of  the  characters  of  each  group  be  taken  into  consid- 
eration the  lines  of  separation  will  appear  more  sharp. 

Key  to  Orders  of  Phycomycetes 

I.  Mycelium  wholly  absent  in  several  families,  in  others  present  but  poorly 
developed  or  evanescent;  thallus  at  maturity  functioning  in  large  part 
or  in  its  entirety  in  reproduction;  sexual  reproduction  often  unknown, 
when  present  of  various  kinds  but  not  typically  oomycetous  or 
zygomycetous. 

A.  Thallus  in  most  forms  functioning  essentially  in  its  entirety  in  one 

capacity,  at  maturity  usually  acting  as  a  single  sporangium  or 
gametangium  or  by  cleavage  becoming  a  sorus  of  like  sporangia ; 
resting  spore  not  lying  free  in  the  gametangium. 

1.  Chytridiales,  p.  43 

B.  Thallus  at  maturity  divided  by  transverse  septa  into  a  chain  of 

cells  capable  of  functioning  in  various  capacities,  i.e.,  as  sporan- 
gia, male  or  female  gametangia,  or  specialized  vegetative  cells; 
resting  spore  lying  free  in  the  female  gametangium  and  resem- 
bling the  oospore  of  higher  orders;  an  oospliero  apparently  lacking. 

2.  Ancylistales,  p.  117 

II.  Mycelium  well  developed,  not  evanescent;  thallus  at  maturity  function- 
ing in  relatively  small  part  in  reproduction;  specialized  cells  cut  off  by 


40  THE  LOWER  FUNGI— PHYCOMYCETES 

septa  to  function  as  reproductive  organs;  the  remainder  of  the  thalhis 
retaining  its  vegetative  character;  sexual  reproduction  usually  present; 
resting  spores,  identical  in  aspect  with  the  sexual  spores,  developed  in 
some  genera  parthenogenetically. 

A.  Male  and  female  gametangia  freeing  ciliate  gametes  which  fuse  to 

form  zygotes;  zygote  developing  directly  into  the  new  plant 
without  first  becoming  a  resting  spore;  characteristic  thick- 
walled  chlamydospores  formed  asexually. 

3.  Blastocladiales,  p.  130 

B.  Female  gametangium  not  forming  ciliate  gametes;  sexual  fusion 

resulting  in  a  thick-walled  resting  spore. 

1.  Contents  of  female  gametangium  differentiated  at  maturity 

to  form  one  or  more  naked  protoplasmic  spheres  termed 
oospheres;  sexual  identitj^  of  male  and  female  gametangia 
evident;  female  gametangium  (oogonium)  larger  and 
stouter  than  the  male  gametangium  (antheridium);  true 
gametangial  copulation  lacking;  fertilization  accomplished 
by  passage  of  one  or  more  male  nuclei  directly  into  the 
oosphere;  oosphere  maturing  into  a  thick-walled  oospore 
lying  free  in  the  oogonium;  swarmspores  formed  in  most 
genera. — Oomycetes. 
a.  Antheridium  forming  ciliate  cells  (antherozoids)  which 

swim   to   the  oogonium   and  fertilize   the  oosphere; 

fertilization  tube  lacking. 

4.  Monoblepharidales,  p.  138 

6.  Antherozoids  not  formed;  one  or  more  male  nuclei 
discharged  into  the  oosphere  through  a  fertilization 
tube  put  out  by  the  antheridium. 

(1)  Forms  typically  aquatic  and  chiefly  saprophytic; 

sporangia  usually  not  deciduous,  freeing 
endogenous  spores;  asexual  cells  functioning  as 
conidia  uncommon;  oogonium  forming  one  to 
many  oospheres. 

5.  Saprolegniales,  p.  146 

(2)  Forms  typically  terrestrial  and  parasitic,  though 

species  of  aquatic,  semiaquatic,  and  saprophy- 
tic habit  occur;  sporangia  typically  deciduous 
and  wind  disseminated,  commonly  termed 
conidia,  in  some  cases  freeing  endogenous 
spores,  in  others  germinating  directly  by  germ 
tube;  oogonium  forming  a  single  oosphere 

6.  Peronosporales,  p.  185 

2.  Oospheres    lacking;    sexual    identity   of   male    and    female 

gametangia  not  evident;  the  two  cells  usually  indistinguish- 
able in  size  and  shape,  and  functioning  alike;  consequently 
the  terms  antheridium  and  oogonium  not  applicable;  true 
gametangial  copulation  occurring  and  the  merged  proto- 
plasts transformed  into  the  zygospore;  zygospore  not  lying 


PHYCOMYCETES  41 

free;  its  wall  formed  directly  from  that  of  the  sametan- 
gium;  swarmspores  absent  in  the  trroup. — ^Zygomycetes. 
a.  Forms  typically  saprophytic;  zygospores  borne  chiefly 
on  aerial  mycehum;  asexual  reproductive  cells 
extremely  various  and  representing  steps  in  the 
evolution  of  the  unicellular  deciduous  conidium  from 
the  many-spored  persistent  sporangium;  conidia  not 
shot  away. 

7.  Mucorales,  p.  234 

6.  Forms  chiefly  parasitic  and  entomogenous,  a  few  forms 
saprophytic,  a  few  oth  rs  parasitic  on  plants;  zygo- 
spores borne  typically  within  the  host;  asexual  repro- 
duction almost  always  by  conidia  borne  at  the  ends  of 
specialized  conidiophores  and  shot  away  at  maturity. 

8.  Entomophthorales,  p.  281 

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Jena  (Gustav  Fischer),  1926. 
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701  pp.,  406  fig..  New  York  (McGraw-Hill  Book  Company,  Inc.),  1928. 
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CHAPTER  III 
CHYTRIDIALES 

The  members  of  this  order  are  characterized  by  extreme 
simphcity  of  form  and  structure,  and  are  regarded  as  the  lowest 
of  all  the  fungi.     They  are  commonly  termed  chytrids. 

Mycelium  is  either  wholly  wanting  or  only  sHghtly  developed. 
When  present  it  consists  usually  of  delicate  threads,  the  terminal 
branches  of  which  taper  to  sharp-pointed,  almost  invisible  tips. 
In  only  a  few  genera  are  the  threads  of  broad  diameter  and 
definitely  cylindrical  as  in  most  higher  fungi.  Frequently,  the 
thallus  is  so  Umited  in  extent  that  its  branches  are  confined  to 
a  single  host  cell.  It  is  then  said  to  be  monophagus.  In  other 
cases,  the  branches  enter  several  or  many  host  cells,  the  term 
polyphagus  being  appHed.  In  species  in  which  mycehum  is 
wholly  absent  the  thallus  functions  in  its  entirety  at  maturity 
in  reproduction.  A  single  thallus  may  be  transformed  into  a 
sporangium,  a  group  (sorus)  of  sporangia,  a  resting  spore,  or 
a  group  (sorus)  of  resting  spores.  Two  thalh  may  conjugate, 
one  functioning  as  the  male  cell,  the  other  as  the  female.  In 
species  possessing  mycelium  the  reproductive  cells  are  far  more 
prominent  than  the  vegetative  threads. 

The  thallus,  in  the  chytrids,  has  its  beginning  in  almost  all 
cases  as  a  motile  spore,  zoospore,  which  comes  to  rest,  enlarges, 
and  finally  attains  the  form  and  size  characteristic  of  the  mature 
thallus.  Zoospores  are  amoeboid  or  ciliate.  In  the  latter  case, 
they  are  often  called  swarmspores. 

In  asexual  reproduction  zoospores  are  borne  in  indefinite 
number  in  a  unicellular  sac,  called  the  sporangium,  which  may 
or  may  not,  as  indicated  above,  compose  the  entire  thallus. 
During  the  summer  in  temperate  regions  several  generations 
of  the  organism  usually  follow  one  another  rapidly  as  long  as 
a  food  supply  is  available.  The  sporangia  produced  at  this 
period  are  typically  thin-walled  and  may  be  termed  summer 
sporangia,  thin-walled  sporangia,  swarmsporangia  or  merely 
sporangia.     Especially  at  the  close  of  the  season  or  in  periods 

43 


44  THE  LOWER  FUNGI— PHYCOMYCETES 

of  unfavorable  environment  they  may  be  thick-walled,  and  are 
then  termed  resting  sporangia  or  resting  spores.  When  evidence 
is  given  that  a  sexual  fusion  acconipani(>s  their  formation  the 
terms  oosporangium,  oospore,  zygo sporangium  or  zygospore 
are  often  applied. 

When,  in  parasitic  species,  the  summer  sporangia  or  resting 
spores  are  formed  within  the  host  cell  they  are  termed  endobiotic 
(endophytic  when  the  host  is  a  plant,  endozoic  when  it  is  an 
animal).  When  they  stand  on  the  surface  of  the  host,  with  only 
the  nutritive  hyphae  penetrating  into  its  interior,  they  are  said 
to  be  epibiotic  (epiphytic  or  epizoic).  In  saprophytic  species 
thej^  are  either  intramatrical  or  extramatrical  depending  on 
whether  they  lie  in  or  outside  of  the  matrix  or  substratum. 

The  summer  sporangium  is  usually  more  or  less  globose  or 
ovoid,  though  in  some  genera  it  is  considerably  elongated.  At 
maturity  its  contents  form  one  to  many  zoospores.  These  are 
usually  ciliate  and  escape  from  the  sporangium  through  a  definite 
pore,  which  often  terminates  an  elongate  exit  tube.  More  rarely 
the  zoospores  are  non-ciliate  and  amoeboid.  Occasionally, 
zoospores  encyst  in  the  sporangium  and  germinate  by  tubes 
in  situ.  In  some  genera  the  protoplast  passes  from  the  spo- 
rangium into  an  extruded  thin-walled  vesicle,  which  later  bursts 
freeing  the  zoospores.  In  such  cases  the  zoospores  may  or  may 
not  be  completely  delimited  before  passing  into  the  vesicle. 
Since  the  vesicle  functions  as  a  sporangium,  it  is  so  called  by 
many  writers,  while  the  initial  cell,  from  which  it  arises,  is  termed 
the  prosporangium. 

When  the  mature  thallus  divides  to  form  a  group  of  sporangia 
or  resting  spores  the  group  is  termed  a  sorus.  In  some  genera 
the  entire  protoplast  flows  from  the  thallus  into  a  thin-walled 
vesicle  and  there  divides  to  form  the  sorus.  In  such  cases  the 
initial  thallus  cell  is  called  the  prosorus. 

The  resting  spore  corresponds  essentially  in  its  methods  of 
germination  to  the  summer  sporangium  except  that  in  some  cases 
it  functions  as  a  prosorus  and  emits  a  vesicle  in  which  a  sorus 
of  sporangia  are  formed.  It  is  thicker  walled  than  the  summer 
sporangium  and,  though  sometimes  smooth,  is  often  character- 
istically roughened,  being  tuberculate,  echinulate,  or  reticulate. 

In  this  order  the  zoospores  are  usually  ciliate,  and  swim 
actively  for  a  time  before  coming  to  rest  and  retracting  their 
cilia.     In   most   genera  the   zoospore,   on   becoming   quiescent, 


CHYTRIDIALES  45 

envelops  itself  in  a  thin  membrane  and  is  then  said  to  be  encysted. 
Some  writers  term  it  a  cystospore.  In  the  Plasmodiophoraceae 
and  Sjmchytriaceae  a  membrane  is  not  formed,  and  in  these 
groups,  composed  wholly  of  parasites,  the  zoospore  is  capable  of 
passing  directly  through  the  host  cell  wall  into  the  cell  cavity.  In 
the  other  families  the  zoospore  assumes  a  membrane,  and  germina- 
tion is  accomplished  by  the  passage  of  the  protoplast  through  a 
short  exit  tube  or  germ  tube.  In  parasitic  species  this  exit 
tube  functions  as  an  infection  thread  and  penetrates  the  host 
cell  wall.  In  the  Olpidiaceae  and  Woroninaceae  the  protoplast 
of  the  cystospore  then  passes  through  the  tube  into  the  host  and 
there  develops  into  the  mature  thallus.  In  the  typical  epibiotic 
species  (Rhizidiaccae)  the  germ  tube  of  the  cystospore  acts  as 
a  holdfast  and  often  develops  into  a  system  of  delicate  endo- 
biotic  rhizoids,  while  the  spore  itself  enlarges  and  forms  an 
epibiotic  sporangium  or  resting  spore.  In  the  Cladochytriaceae 
epibiotic  sporangia  are  sometimes  formed  in  this  way,  but  more 
often  the  protoplast  of  the  swarmspore  passes  through  the  germ 
tube  into  the  host  and  develops  there  into  an  extensive  mycelium. 
Endobiotic  sporangia  and  resting  spores  then  develop  from  inter- 
calary or  terminal  enlargements  of  this  mycelium. 

Sexual  reproduction  probably  takes  place  in  many  of  the 
genera  of  the  order,  but  its  presence  has  been  satisfactorily 
demonstrated  in  relatively  few  species.  Probably,  subsequent 
investigations  will  show  that  the  resting  spores  throughout  the 
group  are  in  most  cases  at  least  sexually  produced.  They  are 
commonly  termed  resting  spores,  rather  than  oospores  or  zygo- 
spores, because  the  method  of  their  formation  is  usually  in  doubt. 
Even  in  cases  in  which  the  details  of  the  sexual  process  are  com- 
pletely known  the  terms  oospore  and  zygospore  are  avoided 
since  in  these  primitive  forms  sexuality  is  often  intermediate  in 
type  between  typical  oomycetous  and  typical  zygomycetous 
reproduction.  Considerable  variation  in  the  sexual  process  is 
evident  in  the  group,  the  general  situation  having  been  sum- 
marized in  the  preceding  chapter  (p.  34).  The  resting  spore 
in  some  species  {e.g.,  Olpidium  viciae  and  Synchytrium  endo- 
bioticum)  results  from  planogamic  fusion  of  cihate  isogametes. 
In  other  cases  {Monochytrium)  gametes  fuse  in  the  amoeboid 
condition.  Probably  many  species  form  their  resting  spores 
in  this  manner,  the  fusions  not  yet  having  been  observed  due 
to  the  difficulty  of  following  the  activities  of  such  small  motile 


46  THE  LOWER  FUNGI— PHYCOMYCETES 

cells.  In  all  such  cases,  summer  sporangia  result  from  zoospores 
and  resting  spores  from  zygotes.  In  other  species,  young  thalli 
copulate  {e.g.,  Olpidiopsis  spp.  and  Pseudolpidiopsis  spp.)  and 
a  pore  connection  is  formed  between  them.  One  cell  then 
functions  as  the  female  and,  after  receiving  the  contents  of  the 
male  cell,  enlarges  and  is  transformed  by  the  thickening  of  its 
wall  directly  into  the  resting  spore.  The  spore  does  not  lie  free 
in  the  oogonium  as  in  the  Oomycetes.  The  emptied  male  cell 
remains  attached  to  the  spore  even  at  maturity  and  was  termed 
the  companion  cell  by  earlier  mycologists  who  failed  to  appreciate 
its  real  character.  In  some  cases,  several  male  cells  conjugate 
with  a  single  female  cell,  and  the  resting  spore  bears  consequently 
several  companion  cells.  In  Zygorhizidium  a  conjugation  tube 
is  put  out  by  one  individual  and  its  contents  are  discharged 
through  the  tube  into  the  other  which  then  develops  into  the 
resting  spore.  In  Polyphagus  a  similar  tube  is  formed  but  the 
resting  spore  develops  in  the  tube. 

It  is  evident  in  the  light  of  this  great  variation  in  the  sexual 
process  that  the  order  Chytridiales  can  not  be  incorporated  in 
the  old  superordinal  group  Oomycetes,  as  has  been  attempted 
by  Schroter  (1892:  63). 

In  the  separation  of  the  families  of  the  order  the  treatment 
here  adopted  is  not  identical  with  that  of  any  standard  text. 
Except  in  the  incorporation  of  the  Plasmodiophoraceae,  it  agrees 
in  the  main  with  that  of  von  Minden  (1911:  226),  though  his 
recognition  of  the  family  Hyphochytriaceae  is  not  followed. 
His  monograph  of  the  order  is  the  most  recent  general  treatment. 
We  have  not  seen  fit  to  follow  Gaumann  (1926:  15)  in  excluding 
from  the  Phycomycetes  those  lower  families  of  the  present  order 
which  do  not  form  mycelium.  His  limitation  of  the  term  Archi- 
mycetes  to  such  forms  will  prove  confusing  to  all  students  who 
have  applied  it  in  the  sense  of  Fischer  to  the  Chytridiales  and 
Ancylistales. 

Below  in  the  discussion  of  the  Plasmodiophoraceae  the  reasons 
for  the  incorporation  of  this  family  in  the  Chytridiales  are  given. 
The  point  is  stressed  that  the  order  as  here  recognized  is  clearly 
a  polyphyletic  group.  The  inclusion  of  an  additional  border 
line  family  is  consequently  the  more  easily  justified.  The  results 
of  future  investigation  will  doubtless  enable  the  student  of 
phylogeny  to  arrange  the  members  of  the  order  in  several  natural 
lines,  but  at  present  this  does  not  seem  possible.     Consideration 


CHYTRIDIALES  47 

of  the  morphology  of  the  zoospore  will  probably  afford  one  of  the 
more  fundamental  bases  of  separation,  since  this  structure  is 
presumably  primitive.  It  is  of  interest  to  note  in  this  connec- 
tion that  in  the  Woroninaceae  alone  is  this  cell  biciliate  as  in 
the  higher  orders.  The  Chytridiales  are  of  special  interest  to 
that  group  of  students  who  beheve  that  the  higher  fungi  arose 
from  the  lower  (Atkinson  1909  6).  By  other  students  they  are 
regarded  as  degenerate  unicellular  green  algae  or  degenerate 
Oomycetes.  Although  the  writer  is  inclined  to  the  belief  that 
the  fungi  have  arisen  from  unicellular  non-chlorophyll  bearing 
organisms  and  that  the  group  is  phylogenetically  a  unit,  it  seems 
evident  that  certain  lines  of  development  have  progressed  a 
relatively  short  distance.  The  terminations  of  several  such 
lines  apparently  exist  today  in  the  Chytridiales,  while  one  or 
more  other  lines  may  be  assumed  to  have  produced  the  higher 
forms. 

The  order  Chytridiales  embraces  approximately  two  hundred 
known  species.  The  majority  were  described  first  from  Central 
Europe  and  may  not  have  been  encountered  elsewhere.  The 
group  has  been  studied  relatively  httle,  and  numerous  unde- 
scribed  species  doubtless  await  the  attention  of  the  investigator' 
in  all  parts  of  the  world.  Many  are  probably  cosmopohtan. 
Most  of  the  known  species  are  true  parasites  in  plants  or  animals. 
Of  those  in  plants  fully  half  occur  in  fresh-water  algae,  almost 
as  many  Uve  in  higher  plants,  while  the  remainder  occur  in  marine 
algae,  aquatic  fungi,  and  in  pollen  grains,  rust  spores,  and  other 
similar  bodies  which  fall  into  the  water.  A  few  species  are 
parasitic  in  Protozoa,  and  some  are  saprophytic  in  submerged, 
decaying  plant  or  animal  remains.  All  the  species  are  micro- 
scopic, though  in  some  cases  their  presence  stimulates  the  host 
to  form  noticeable  galls,  swellings  or  discolorations.  In  the 
treatment  which  follows,  the  effort  is  made  to  include  all  known 
genera.  The  miscellaneous  character  of  the  literature,  has  made 
this  difficult,  however,  and  it  is  to  be  expected  that  some  forms 
have  been  overlooked. 

Key  to  Families  of  Chytridiales 

I.  Mycelium  wholly  lacking;  thallus  always  intramatrical. 

A.  Thallus  existing,  through  early  stages  at  least,  as  a  naked,  more  or 
less  amoeboid  protoplast,  often  somewhat  obscured  by  the 
protoplasm  of  the  host  cell,  finally  (in  most  cases)  fragmenting 


48  THE  LOWER  FUNGI— PHYCOMYCETES 

into  a  number  of  naked  protoplasts,  each  of  which  tlien  assumes 
a  wall  and  functions  as  a  summer  sporangium  or  resting  spore. 

1.  Thallus  never  functioning  in  its  entirety  as  a  single  sporan- 

gium or  resting  spore,  but  in  some  cases  said  to  form  a  soral 
membrane  before  breaking  up  into  sporangia;  sporangia 
germinating  by  a  small  number  (one  to  eight)  of  amoeboid 
or  uniciliate  zoospores;  cilium  demonstrated  in  but  few 
cases,  where  known  attached  to  the  anterior  end  of  the 
zoospore;  vegetative  mitosis  of  a  peculiar  protomitotic  or 
cruciform  type. 

1.  Plasmodiophoraceae,  p.  48 

2.  Mature  thallus  in  some  genera  forming  a  membrane  and 

functioning  as  a  single  sporangium  or  resting  spore,  in 
others  fragmenting  into  a  number  of  naked  protoplasts 
each  of  which  then  assumes  a  membrane;  a  common  soral 
membrane  never  formed;  sporangia  typically  multispored; 
zoospores  laterally  biciliate. 

2.  Woroninaceae,  p.  66 

B.  Thallus  provided  from  an  early  period  with  a  thin  membrane, 
clearly  discernible  within  the  plasma  of  the  host  cell;  zoospores 
uniciliate;  cilium  attached  at  the  posterior  end  of  the  spore. 

1.  Thallus  at  maturity  functioning  in  its  entirety  as  a  single 

sporangium  or  resting  spore. 

3.  Olpidiaceae,  p.  71 

2.  Thallus  at  maturity  either  developing  a  thick  wall  and  func- 

tioning as  a  resting  spore,  or  its  protoplast  divided  by 
cleavage  planes  to  form  a  sorus  of  sporangia  enclosed  in  a 
common  soral  membrane. 

4.  Synchytriaceae,  p.  80 

II.   Mycelium  present,  though  usually  only  slightly  developed  and  of  delicate 
threads  of  small  diameter;  thallus  intra-  or  extramatrical. 

A.  Mycelium  not  wide-spreading,  usually  confined  to  one  or  two  cells 

of  the  host,  bearing  only  a  single  sporangium,  and  usually  in 
open  connection  with  it  at  maturity;  sporangia  usually  epibiotic. 

5.  Rhizidiaceae,  p.  88 

B.  Mycelium   wide-spreading,   developing  terminal   and   intercalary 

enlargements  which   are   transformed   wholly  or  in   part   into 
sporangia  or  resting  spores. 

6.  Cladochytriaceae,  p.  100 

Plasmodiophoraceae 

Inasmuch  as  the  members  of  this  family  have  long  been 
regarded  by  many  students  as  parasitic  slime  moulds  their 
inclusion  in  the  Chytridiales  necessitates  a  more  lengthy  explana- 
tion that  would  otherwise  be  given.     It  can  best  be  provided  by 


CHYTRIDIALES  49 

a  presentation  in  sequence  of  the  essential  historical  facts  con- 
cerning the  group. 

The  oldest  genus  recognized  at  present  as  a  member  of  the 
family  is  Plasmodiophora.  It  was  founded  by  Woronin  (1878) 
on  the  causal  organism  of  clubroot  of  cabbage,  P.  brassicae  Wor, 
In  his  discussion  of  the  genus,  Woronin  indicates  clearly  that 
he  regarded  the  organism  as  an  undoubted  relative  of  the  Myxo- 
mycetcs.  Incidentally,  he  concluded  that  the  legume  tubercle 
organism,  long  known  and  variously  classified,  should  be  placed 
near  it.  Other  students  of  the  fungi  accepted  his  point  of  view, 
and  a  search  for  additional  "parasitic  slime  moulds"  followed. 
Several  new  species  were  added  to  Plasmodiophora,  and  two  new 
monotypic  genera  Tetramyxa  and  Sorosphaera  were  erected. 
The  legume  tubercle  organism  which  had  already  received  a 
number  of  names  {Schinzia  leguminosarum  Frank,  Bacillus 
radicicola  Beijerinck,  Rhizohium  leguminosarum  Laurent,  Bactri- 
dium  radicicola  Fischer)  was  now  redescribed  asPhytomyxa  legumi- 
nosarum by  Schroter  (1886:134),  and  a  new  order,  Phytomyxini, 
was  erected  for  its  reception.  Because  the  group  (as  Phyto- 
myxinae)  was  incorporated  later  by  Schroter  in  the  standard 
work,  Engler  und  Prantl's,  Die  Nattirhche  Pflanzenfamilien, 
it  was  generally  accepted.  It  includes  there  the  four  genera 
Plasmodiophora,  Phytomyxa,  Tetramyxa,  and  Sorosphaera,  repre- 
sented at  that  time  by  seven  species,  PI.  brassicae  Wor.,  PI.  alni 
(Wor.)  Moll,  PI.  elaeagni  Schroter,  Phy.  leguminosarum  (Frank) 
Schroter,  Phy.  lupini  Schroter,  T.  parasitica  Gobel,  and  S. 
veronicae  Schroter. 

Later,  the  legume  tubercle  organism  was  proved  to  be  beyond 
question  one  of  the  bacteria,  and  more  recent  investigations 
indicate  that  the  root  tubercles  on  Alnus,  Elaeagnus,  Myrica, 
and  certain  other  non-leguminous  plants  are  caused  by  the  same 
species  or  closely  related  ones.  Consequently,  Plasmodiophora 
alni  and  PI.  elaeagni  have  disappeared  from  the  Phytomyxinae 
along  with  Phijtomyxa.  In  a  review  of  this  situation,  Maire 
and  Tison  (1909)  point  out  that,  since  Phytomyxa  has  been 
removed,  the  name  Phytomyxinae  is  no  longer  appropriate. 
They  use  instead  Plasmodiophoraceae,  and  under  this  heading 
list  the  three  remaining  genera.  They  follow  Schroter  in  sepa- 
rating them  on  the  basis  of  the  arrangement  of  the  spores,  i.e., 
Plasmodiophora  (spores  free  from  one  another),  Tetramyxa  (spores 
cUnging  together  in  tetrads),  Sorosphaera  (spores  arranged  to 


50  THE  LOWER  FUNGI— PHYCOMYCETES 

form  a  hollow  sphere).  In  a  later  and  more  extensive  paper 
they  (Maire  and  Tison,  1911)  erect  two  new  genera,  Molliardia 
and  Ligniera,  and  present  a  somewhat  revised  classification  in 
which  they  stress  as  of  primary  significance  the  question  of 
w^hether  a  given  organism  results  in  hypertrophy  of  the  host. 

Although  the  genus  Spongospora  Brunchorst  (1887),  now 
regarded  as  a  member  of  the  group,  was  described  relatively 
early,  its  existence  was  overlooked  or  ignored  by  all  of  these 
later  writers.  It  was  demonstrated  to  be  an  undoubted  member 
of  the  group  by  Osborn  (1911  a)  at  about  the  time  that  Maire 
and  Tison  published  their  second  paper.  Subsequently,  several 
additional  genera  have  been  described  by  other  authors.  These 
are  all  discussed  below  and  in  spite  of  fragmentary  data  in  the 
case  of  some  species,  the  attempt  is  made  to  present  a  complete 
picture  of  the  family  as  it  exists  today. 

The  writer  is  not  the  first  to  incorporate  the  Plasmodi- 
ophoraceae  in  the  fungi.  Gaumann  (1926)  and  Gaumann  and 
Dodge  (1928)  incorporate  the  group  in  the  Archimycetes,  and 
emphasis  has  been  placed  by  various  investigators  on  facts  which 
seemed  to  them  to  justify  the  inclusion  of  the  group  in  the  fungi. 
There  has  been  considerable  diversity  of  opinion  expressed  in  re- 
cent years,  however,  as  to  the  relationships  of  the  group.  Pavil- 
lard  (1910)  concludes  that  these  forms  are  a  branch  of  the 
Myxomycetes  in  which  modifications  have  resulted  from  the 
parasitic  habit.  Schwartz  (1914),  while  admitting  that  they  are 
related  to  the  Myxomycetes,  regards  the  differences  as  so  great 
that  he  treats  them  as  intermediate  between  this  group  and  the 
Chytridiales.  Maire  and  Tison  (1911)  feel  that  they  have  origi- 
nated from  the  Chytridiales,  while  Cook  (1926)  thinks  that  they 
show  relationship  with  the  Protozoa. 

Students  of  the  cytology  of  these  forms  have  been  impressed 
by  the  great  similarity  which  the  various  genera  and  species 
show  in  the  aspects  of  their  nuclear  behavior,  and  by  the  fact 
that  they  differ  from  other  groups  in  exhibiting  in  their  life  cycle 
two  entirely  different  types  of  nuclear  division.  One  type  occurs 
throughout  the  growth  of  the  thallus  or  myxamoeba;  the  other 
immediately  precedes  spore  formation  or  zoospore  delimitation, 
and  consists  of  two  successive  divisions  which  are  believed  to 
constitute  reduction.  The  nuclear  division  which  occurs  during 
the  growth  period  and  which  may  be  termed  somatic  has  been 
commonly    termed   the   "cruciform   division"   or  protomitosis. 


CHYTRIDIALES  51 

Nothing  identical  with  this  type  of  division  has  been  seen  in 
any  other  group  of  organisms,  though  in  some  of  the  most  primi- 
tive Protozoa  (order  Lobosa)  it  is  said  to  be  approximated. 
Several  workers  have  justified  their  inclusion  of  doubtful  species 
in  the  Plasmodiophoraceae  on  the  single  point  of  their  possession 
of  this  type  of  division.  Before  the  two  reducing  divisions 
occur  a  stage  exists  in  the  cycle  in  which  the  stainable  chromatin 
of  each  nucleus  is  extruded  into  the  cytoplasm.  This  is  termed 
the  "akaryote"  stage.  The  two  mitoses  which  immediately 
follow  are  typical,  and  result  in  a  tetrad  of  nuclei.  According 
to  Cook  (1928  b)  these  nuclei  become  in  some  cases  the  centers 
of  spores,  while  in  others  the  primary  nucleus  of  the  spore  is 
diploid  and  reduction  occurs  in  zoospore  formation.  During 
the  cruciform  division  the  nucleolus  divides  and  persists  in  the 
daughter  nuclei.  Since  the  dividing  nucleolus  is  drawn  out 
into  a  dumb-bell  shape,  and  hes  at  right  angles  to  the  chromatin 
gathered  at  the  equatorial  plate,  the  division  figure  as  viewed 
from  the  side  has  the  aspect  of  a  cross.  The  essential  feature 
of  this  mitosis  is  thus  the  persistence  and  division  of  the  nucleolus. 
In  the  reduction  divisions  the  nucleolus  disappears,  as  in  most 
higher  plants,  and  is  re-formed  de  nova  in  the  daughter  nuclei. 
A  nuclear  fusion  (karyogamy)  may  occur  at  some  point  in  the 
cycle,  but,  though  reported  in  one  or  two  cases,  cannot  be  said 
to  have  been  satisfactorily  demonstrated.  Several  workers 
have  expressed  the  opinion  that  it  will  be  found  in  the  pairing 
of  zoospore-like  gametes  when  germinations  are  obtained  in 
satisfactory  quantity.  The  whole  nuclear  situation  is  well 
summarized  in  the  recent  papers  of  Cook  (1926;  1928  h)  on 
Ligniera.  Just  how  much  significance  should  be  attached  to 
the  cruciform  division  is  perhaps  in  question,  and  conclusions 
concerning  the  taxonomic  position  of  the  group  based  on  this 
feature  alone  would  seem  premature  in  the  light  of  our  ignorance 
of  nuclear  division  in  various  lower  groups.  The  spores  have 
been  observed  to  germinate  in  but  few  species  of  the  family 
and  by  but  few  investigators.  In  Plasmodiophora,  according 
to  Woronin  (1878)  and  Chupp  (1917)  the  spore  wall  cracks  open 
and  the  protoplast  emerges  as  a  single  zoospore  which  swims 
for  a  time  with  a  single  cilium  attached  at  the  forward  end.  The 
posterior  end  of  the  zoospore  is  figured  by  Woronin  as  amoeboid. 
If  the  zoospores  could  be  shown  to  be  of  this  type  throughout 
the  group,   a  character  indicating  relationship  of  this  family 


52  THE  LOWER  FUNGI— PHYCOMYCETES 

and  the  Myxomycetes  would  be  provided,  but  the  data  concern- 
ing germination  arc  so  few  and  contradictory  that  conclusions 
may  not  yet  be  safely  drawn.  In  Plasmodiophora  the  amoeboid 
character  described  by  Woronin  was  not  observed  by  Chupp 
(1917).  In  Spongospora  according  to  Johnson  (1908)  eight 
zoospores  are  freed  from  the  spore,  while  Kunkel  (1915)  describes 
but  one.  In  Ligniera  the  number  varies,  according  to  Cook 
(1928  b),  from  four  to  eight.  The  assumption  that  the  zoospore 
penetrates  the  host  directly  without  first  encysting  on  the  surface 
in  an  enveloping  membrane  also  requires  verification.  If  true 
it  may  perhaps  be  regarded  as  evidence  of  relationship  with 
the  Synchytriaceae. 

In  the  host  the  earliest  stages  observed  show  these  parasites 
(except  in  Spongospora  according  to  Kunkel)  as  intracellular, 
uninucleate,  amoeboid  protoplasts,  and  it  may  be  assumed  in 
most  cases  at  least  that  they  penetrate  in  this  form.  In  the 
host  cell  the  protoplast  (myxamoeba)  becomes  multinucleate, 
increases  in  size,  and  absorbs  nutriment  from  the  host.  It  may 
or  may  not  fragment  into  daughter  myxamoebae.  At  maturity 
each  myxamoeba  is  split  by  cleavage  planes  into  uninucleate 
bits,  each  of  which  envelops  itself  in  a  wall  and  assumes  a  more 
or  less  spherical  form.  These  bodies  have  been  termed  spores 
by  all  workers  in  the  group.  After  passing  through  a  period  of 
rest,  however,  they  germinate  by  one  or  more  swarmspores  or 
myxamoebae,  and  seem  to  be  comparable  in  many  respects 
to  the  resting  sporangia  of  other  families  of  the  Chytridiales. 
The  same  is  true  also  of  the  so  called  spores  of  the  Myxomycetes. 
These  "spores"  (resting  sporangia)  may  remain  attached  to 
one  another  forming  groups  of  definite  form,  or  they  may  fall 
apart  and  lie  free  in  the  host  cell. 

The  mature  multinucleate  myxamoeba  which  fragments  to 
form  these  spores  apparently  remains  naked  in  most  cases,  so 
that  the  spores  are  not  enveloped  in  a  common  soral  membrane; 
but  Schwartz  states  clearly  that  such  a  membrane  is  formed  in 
Sorosphaera.  The  papers  of  Borzi  (1884:  6)  and  Nemec  (1911  a; 
1913  a)  on  Rhizomyxa,  Sorolpidium,  and  A  msom?/.ra  lend  support 
to  the  assumption  that  both  types  of  development  exist  in  the 
group.  If  this  is  true  the  group  in  this  respect  is  intermediate 
between  the  Myxomycetes  and  the  Synchytriaceae. 

The  peculiar  phenomenon  of  elimination  which  in  the  Myxo- 
gastres  results  in  the  formation  of  capillitium  threads  and 
"sporangial"  walls  is  wholly  lacking  in  the  Plasmodiophoraceae. 


CHYTRIDIALES  53 

When  several  myxamoebae  exist  together  in  the  same  host  cell, 
and  continue  to  grow,  it  might  be  expected  that  they  will  finally 
come  into  actual  contact,  and  being  naked  fuse.  They  have 
been  stated  to  do  so  in  some  species,  and  certain  writers  have 
termed  the  apparently  united  and  homogeneous  mass,  which 
tends  to  fill  the  host  cell,  the  plasmodium.  Other  investigators 
deny  that  fusion  is  complete,  and  maintain  that  mitosis  is  simul- 
taneous only  in  a  given  myxamoeba,  not  throughout  the  entire 
host  cell.  In  Spongospora  according  to  Kunkel  (1915:  273)  the 
uninucleate  myxamoebae  which  escape  from  the  various  spores 
composing  a  spore  ball  may  lie  in  such  close  contact  that  "they 
seem  to  fuse  and  cannot  be  distinguished  as  separate  bodies." 
He  states  further  that  such  "  baby  plasmodia  "  may  come  together 
to  form  larger  ones,  and  that  infection  of  the  host  is  effected  by 
the  penetration  of  the  multinucleate  "plasmodium"  between 
the  cells  of  the  tuber.  In  the  Myxogastres  where  the  term  Plas- 
modium was  first  used  by  Cienkowski  an  as  yet  unexplained 
phenomenon  of  mutual  attraction  exists  between  the  motile  cells. 
They  are  drawn  together,  and  multiple  cell  fusions  result  in 
the  formation  of  an  enlarging  naked  amoeboid  protoplast.  This 
body  is  termed  a  plasmodium  not  merely  because  it  is  naked  and 
multinucleate,  but  more  essentially  because  it  is  formed  by 
multiple  fusion  of  uninucle'ate  motile  cells  which  are  drawn 
together  by  mutual  attraction.  To  the  writer  it  does  not  seem 
that  such  a  true  plasmodium  has  been  found  in  any  of  the  Plas- 
modiophoraceae.  In  those  species  of  the  family  in  which  a 
fusion  is  conceded  by  all  workers  to  be  lacking,  and  in  which  the 
nuclei  of  the  mature  multinucleate  myxamoeba  clearly  arise 
through  repeated  division  from  the  nucleus  of  the  infecting  zoo- 
spore, the  use  of  the  term  plasmodium  seems  wholly  unjustified. 

In  attempting  to  indicate  the  bases  on  which  it  seems  desirable 
to  incorporate  the  Plasmodiophoraceae  in  the  fungi  rather  than 
in  the  Myxomycetes  it  is  necessary  to  deal  in  generahzations 
on  account  of  inadequate  data.  Enough  is  known  concerning 
the  group,  nevertheless,  to  warrant  the  attempt.  In  the 
character  of  the  zoospore  and  in  the  unusual  type  of  vegetative 
mitosis  the  Plasmodiophoraceae  are  unlike  other  known  fungi. 
The  zoospore  seems  to  resemble  that  of  the  Myxogastres,  the 
nuclear  division  to  some  extent  that  of  certain  Protozoa.  In 
the  absence  of  capillitium  and  so  called  "sporangial"  walls, 
in  the  absence  of  a  true  plasmodium,  and  in  the  presence  of  para- 


54  THE  LOWER  FUNGI— PHYCOMYCETES 

sitism  the  group  differs  strikingly  from  the  Myxogastres  and 
corresponds  with  the  Woroninaceae  and  Synchytriaceae  of  the 
Chytridiales.  In  the  small  and  apparently  rather  definite 
number  (1-8)  of  zoospores  freed  in  the  germination  of  the 
sporangium  ("spore")  the  Plasmodiophoraceae  resemble  the 
Myxogastres  more  than  they  do  the  Woroninaceae  and  Synchy- 
triaceae where  the  number  is  usually  much  larger.  Ignorance 
of  the  facts  concerning  the  position  of  nuclear  fusion  and  reduc- 
tion division  in  the  cycle  of  the  various  groups,  and  conflicting 
evidence  concerning  the  presence  or  absence  of  a  soral  membrane 
render  these  characters  of  little  value  for  purposes  of  contrast. 

In  summarizing  the  available  facts  it  would  seem  that  the 
Plasmodiophoraceae  resemble  the  Myxogastres  less  than  they  do 
the  Woroninaceae  and  Synchytriaceae.  Their  failure  to  form 
a  true  Plasmodium  is  regarded  in  this  connection  as  an  essential 
feature.  However,  in  placing  the  family  in  the  Chytridiales, 
it  should  not  be  assumed  that  the  relationship  to  members  of 
this  order  is  necessarily  close.  It  has  been  pointed  out  above 
in  the  ordinal  diagnosis  that  the  Chytridiales  constitute  a  large 
assemblage  of  forms  which  seem  to  have  been  derived  along  a 
number  of  different  lines.  A  correctly  drawn  phylogenetic 
tree  would  probably  completely  disrupt  the  group.  These 
forms  have  been  treated  together  in  one  order  merely  because 
they  constitute  the  most  primitive  fungi,  not  because  they 
are  regarded  as  a  coherent  group  of  closely  related  genera.  A 
more  natural  arrangement  is  much  to  be  desired,  but  cannot  as  yet 
be  attempted.  This  situation  makes  much  easier  the  inclusion 
of  the  Plasmodiophoraceae  in  the  group,  and  taking  into  con- 
sideration the  striking  difference  in  the  morphology  of  the  swarm- 
spore  in  the  three  families  it  does  not  seem  unreasonable  to 
assume  that  the  Woroninaceae  and  Synchytriaceae  are  as  closely 
related  to  the  Plasmodiophoraceae  as  to  each  other.  To  the 
writer  it  seems  likely  that  these  several  groups  have  arisen  more 
or  less  in  parallel  from  yet  more  primitive  Protozoa,  and  wholly 
independent  of  the  Myxogastres  which  have  arisen  from  the 
same  or  different  Protozoa  along  another  Une.  The  existence 
in  a  limited  section  of  the  Protozoa  of  a  type  of  nuclear  division 
resembling  the  cruciform  division  of  the  Plasmodiophoraceae 
indicates  perhaps  the  origin  of  this  family,  but  does  not  of  neces- 
sity preclude  the  possibility  that  other  families,  which  now  possess 
a  higher  type  of  mitosis,  have  arisen  from  the  same  or  a  closely 


CHYTRIDIALES  55 

related  group.  In  an  interesting  discussion  of  the  "interrela- 
tionships of  the  Protista  and  the  primitive  fungi"  Cavers  (1915: 
168)  expresses  a  similar  point  of  view  but  recognizes  the  Plas- 
modiophorales  as  a  separate  group,  preferring  not  to  include 
them  in  either  the  Myxomycetes  or  Chytridiales.  The  student 
will  find  in  his  article  a  wealth  of  information  concerning  the 
Protozoa  which  is  not  available  in  the  general  mycological 
literature. 

Key  to  Genera  of  Plasmodiophoraceae 

I,  Spores  at  maturity  not  united;  lying  free  in  the  host  cell. 

1.  Plasmodiophora,  p.  55 

II.  Spores  at  maturity  remaining  attached  to  one  another  in  some  definite 
type  of  aggregation. 

A.  Spores  clinging  together  in  tetrads  or  dj-ads. 

2.  Tetramyxa,  p.  59 

B.  Spores  united  in  larger  numbers  to  form  more  or  less  definite  spore 

balls. 

1.  Spore  balls   typically   spherical   to   ellipsoidal,   and   hollow, 

consisting  of  a  peripheral  layer  of  spores  enclosing  a  cen- 
tral cavity. 

3.  Sorosphaera,  p.  60 

2.  Spore  balls  in  the  form  of  flat  two-layered  plates  with   a 

central  cavity  small  or  lacking. 

4.  Sorodiscus,  p.  63 

3.  Spore  balls  sponge-like,  essentially  solid,  lacking  a  central 

cavity  but  traversed  by  prominent  fissures. 

5.  Spongospora,  p.  64 

1.  Plasmodiophora  Woronin  (1878). 

The  genus  Plasmodiophora  was  founded  by  Woronin  on  the 
single  species  PI.  hrassicae  Wor.,  which  he  had  shown  to  be  the 
cause  of  clubroot  of  cabbage  and  other  cruciferous  plants  (Fig.  1). 
Subsequently  a  considerable  number  of  imperfectly  known  organ- 
isms have  been  placed  in  this  genus  by  various  writers,  but  no 
one  of  them  can  be  retained  in  it  with  assurance.  It  seems  best 
for  the  present  to  regard  the  genus  as  monotypic,  and  to  base 
the  discussion  on  the  classical  paper  of  Woronin  and  on  the 
results  of  certain  more  recent  investigations  on  PI.  hrassicae. 

The  disease  caused  by  this  species  is  well  known  on  cabbage, 
and  occurs  less  commonly  on  turnip,  cauliflower,  rutabaga, 
Brussels  sprouts,  and  other  similar  cultivated  and  wild  hosts. 
It   results  in   pronounced  malformation   of  the  roots,   and  has 


56  THE  LOWER  FUNGI— PHYCOMYCETES 


Fig.    1. — Plasmodiophora  brassicae  Woronin.     A  young  cabbaRC  plant  showing 
typical  malformation  of  roots.     (After  Chupp  1017.) 


CHYTRIDIALES 


57 


received  in  consequence  various  common  names  such  as  clubroot, 
and  fingers  and  toes.  The  diseased  roots  are  usually  greatly 
enlarged  locally,  the  swellings  or  galls  varying  in  size  and  shape. 
On  cabbage  especially  they  are 
typically  large  and  fusiform. 

The  organism  gains  entrance 
into  the  roots  from  the  soil 
through  root  hairs  or  other  epi- 
dermal cells.  Inoculation  exper- 
iments performed  by  Kunkel 
(1918:  pZ.  61)  show  that  infection 
may  occur  also  through  the  epi- 
dermal cells  of  the  stem  below 
ground.  The  organism  enters 
as  a  uninucleate  amoeboid  zoo- 
spore (myxamoeba).  In  the 
host  cell  it  increases  in  size, 
becomes  multinucleate  (Fig.  3, 
a) ,  and  fragments  into  a  number 
of  daughter  myxamoebae  (Fig.  3, 
b).  When  the  host  cell  divides 
several  of  these  myxamoebae  are  usually  incorporated  in  each 
of  the  daughter  cells.  Other  cell  divisions  follow  and  soon  a 
group  of  infected  cells  exists.     These  httle  clusters  of  diseased 


Fig.  2. — Planmodiophora  brassicac 
Woronin.  Spores  and  swarmspores. 
{After  Chupp  1917;  fig.  97.) 


Fig.  3.—Plasmodiophora  brassicae  Woronin.  (a)  Multinucleate  myxamoeba 
in  base  of  root  hair  of  oabbage.  (6)  Root  hair  containing  a  number  of  daughter 
myxamoebae  resulting  from  division  of  the  primary  myxamoeba.  {After  Chupp 
1917;  fio.  104.) 

cells  resulting  from  primary  infection  by  a  single  zoospore  were 
termed  by  Woronin  " Krankheitsherde."  Although  Nawaschin 
(1899),  who  first  used  modern  cytological  methods  in  the  study 


58 


THE  LOWER  FUNGI— PHYCOMYCETES 


of  Plasmodiophora,  states  that  the  niyxamoebae  never  migrate 
through  the  host  cell  walls  into  adjacent  cells,  later  workers 
(Lutman,  1913:  3;  Chupp,  1917:  435;  Kunkel,  1918:570)  find  that 
the  organism  spreads  widely  through  the  tissue  by  direct  migra- 
tion. Consequently,  as  Kunkel  points  out,  many  thousands 
of  separate  "  Krankheitsherde"  may  result  from  a  single  primary 
infection.  In  fact,  Kunkel  states  that  the  typical  large  club 
is  the  result  of  a  single  infection. 

In  the  early  stages  of  its  intracellular  existence  the  parasite 
does  not  interfere  sufficiently  with  the  functioning  of  the  host 
cell  to  prevent  its  normal  nuclear  and  cell  division.     Later, 


Fig.    4.- — Plasmodiophora   brassicae    Woronin.     (a)    Formation    of   spores.     (6) 
Mature  spores.      {After  Chupp  1917;  fig.  102.) 


the  host  protoplasm  is  largely  absorbed,  and  the  myxamoebae 
increase  in  size  until  they  practically  fill  the  cell.  This  brings 
them  into  direct  contact  and  they  are  said  by  some  workers  to 
be  completely  merged.  Others  state  that  their  identity  is  never 
lost,  and  that  nuclear  divisions  are  simultaneous  only  in  a  given 
myxamoeba,  not  throughout  the  whole  mass.  In  any  case, 
the  host  cell  is  finally  almost  or  completely  filled  with  the  proto- 
plasm of  the  parasite.  The  two  nuclear  divisions  which  are 
believed  to  constitute  reduction  occur,  and  the  spores  are  cut  out 
about  the  resultant  nuclei  (Fig.  4,  a).  They  are  more  or  less 
spherical  and  are  provided  with  definite  smooth  membranes. 
Although  the  spores  do  not  break  apart  simultaneously  they  lie 


CHYTRIDIALES  59 

at  maturity  entirely  free  from  one  another  and  are  not  aggre- 
gated in  any  manner  (Fig.  4,  h).  They  are  finally  freed  by  the 
disorganization  of  the  host  tissue,  and  are  disseminated  in  the 
soil  water.  Under  favorable  conditions  each  spore  splits  open 
and  germinates  by  a  single  zoospore,  which  swims  for  a  time 
(Chupp  1917:  425)  with  a  single  ciHum  attached  to  the  forward 
end  (Fig.  2).  It  finally  comes  to  rest,  and,  having  penetrated 
the  host,  exists  in  the  cell  in  the  non-ciliate  amoeboid  state. 
Woronin  described  the  free-swimming  spore  as  also  amoeboid. 
Germination  has  been  seen  by  few  investigators  and  the  accounts 
are  contradictory  (see  U.  S.  Dept.  Agr.  Tech.  Bui.  181,  p.  7,  1930). 

An  unconvincing  account  of  the  life  history  of  the  organism, 
widely  at  variance  with  all  previously  published  results,  has  been 
presented  recently  by  Jones  (1928:  313).  He  states  that  the 
spore  in  germination  frees  one  to  twenty  ciHate  cells  and  that 
these  undergo  a  sexual  fusion  in  pairs. 

The  genus  has  been  used  from  the  beginning  as  a  dumping 
ground  for  doubtful  species.  It  is  pointed  out  above  that  PI. 
alni  and  PI.  elaeagni  were  based  on  the  legume  tubercle  organism 
or  related  species.  Several  species,  PI.  tJitis,  PL  californica,  PI. 
theae,  and  PI.  orchidis  are  now  known  to  have  been  founded 
merely  on  the  products  of  cell  disorganization.  More  recently 
PI.  halophilae  Ferdinandsen  &  Winge  (1913)  has  been  described 
from  the  petioles  of  Halophila  ovalis;  a  species  has  been  described 
on  sugar  cane  as  PI.  vascularum  Matz  by  Matz  (1920)  Bourne 
(1922)  and  Cook  (1924;  1929);  PZ.  tabaci  Jones  (1926)  has  been 
discussed  in  connection  with  tobacco  mosaic;  and  at  least  two 
other  species,  PI.  ficus-repentis  Andreucci  (1926)  and  PI.  humuli 
Nicholls  (1924)  have  been  pubhshed.  In  none  of  these  cases 
has  sufficient  detail  of  Ufe  history,  morphology,  and  cytology 
been  provided  to  justify  their  inclusion  in  this  genus  as  more 
than  doubtful  forms. 

2.  Tetramyxa  Gobel  (1884). 

The  genus  was  founded  on  the  single  species  T.  parasitica 
G5bel  parasitic  on  Ruppia  rostellata,  a  member  of  the  pond  weed 
family.  The  organism  causes  the  formation  of  peculiar  whitish 
galls  on  all  parts  of  the  plant  except  the  roots.  The  genus  is 
characterized  by  the  tendency  of  the  spores  to  cling  together  in 
tetrads.  Sometimes  they  are  found  in  dyads,  or  as  single  spores. 
More  rarely  large  binucleate  spores  occur. 


60  THE  LOWER  FUNGI—PIIYCOMYCETES 

The  host  is  infected  by  the  uninucleate  zoospore.  This  becomes 
multinucleate  and  divides,  so  that  the  host  cell  often  contains 
several  multinucleate  myxamoebae.  These  grow  and  may  come 
in  contact  but  are  never  completely  fused.  Each  myxamoeba 
forms  its  spores  independently,  and  they  may  be  in  various 
stages  of  completion  in  the  same  host  cell.  Prior  to  spore 
formation  the  protoplasm  of  each  myxamoeba  segments  into 
uninucleate  spore  mother  cells.  Two  divisions,  believed  to  con- 
stitute reduction,  then  occur,  and  the  spore  mother  cell  is  cut 
by  two  perpendicular  planes  into  four  uninucleate  cells,  each  of 
which  assumes  a  cell  wall  and  becomes  a  spore.  These  four 
spores  tend  to  remain  permanently  united. 

MolUard  (1909)  described  a  second  species,  T.  triglochinis 
Molliard,  on  a  parasite  occurring  on  Triglochin  palustre.  Galls 
are  formed  on  various  parts  of  the  plant  above  ground.  The 
life  history  of  this  organism  is  imperfectly  known.  A  multi- 
nucleate myxamoeba  segments  in  the  host  cell  into  uninucleate  por- 
tions and  these  after  several  nuclear  divisions  again  segment. 
Tetrads  of  globose  bodies,  described  by  Molliard  as  spores,  are  thus 
formed.  Maire  and  Tison  (1911)  state  that  these  lack  a  definite 
cell  wall  and  consequently  are  not  comparable  to  the  spores  of 
other  members  of  the  group.  These  authors  have  seen  fit, 
therefore,  to  erect  a  new  genus  Molliardia  Maire  &  Tison  for 
this  species,  which  they  retain  in  the  Plasmodiophoraceae  only 
provisionally.  Until  the  species  is  better  known  it  seems  more 
logical  to  retain  it  in  Tetramyxa  as  a  doubtful  form. 

8.  Sorosphaera  Schroter  (1886: 135). 

As  founded  by  Schroter  the  genus  Sorosphaera  included  only 
one  species,  8.  veronicae  Schrot.,  occurring  in  Europe  on  various 
species  of  Veronica.  It  causes  the  formation  of  galls  on  various 
parts  of  the  plant,  leaves,  petioles,  stems,  etc.  After  infection 
by  the  uninucleate,  amoeboid  zoospore  the  host  cell  becomes 
greatly  enlarged.  The  parasite  grows,  becomes  multinucleate, 
and  divides,  several  multinucleate  protoplasts  thus  coming  to  exist 
in  the  same  host  cell.  By  host  cell  division  "  Krankheitsherde" 
are  formed  as  described  for  Plas7nodiophora,  but  direct  migration 
through  the  cell  walls  has  not  been  observed.  The  several 
multinucleate  protoplasts  in  a  single  host  cell  increase  in  size, 
but  never  fuse  with  one  another.  Although  the  nuclei  of  each 
myxamoeba    divide    simultaneously,    the    nuclei    of    adjacent 


CHYTRIDIALES  61 

myxamoebac  divide  independently.  Finally,  the  protoplasm 
splits  up  into  uninucleate  bits,  and  each  of  these  rounds  up, 
assumes  a  wall,  and  becomes  a  spore.  The  spores  formed  by 
each  myxamoeba  remain  attached  to  one  another,  the  whole 
being  in  the  form  of  a  hollow  sphere,  which,  according  to  Schroter 
(1899)  and  Schwartz  (1911)  is  enveloped  in  a  very  thin  soral 
membrane.  These  spore  balls  are  later  freed  by  the  disintegra- 
tion of  the  host,  and  each  spore  germinates  b}^  a  single  zoospore. 

Two  other  species,  S.  junci  Schwartz  (1910)  and  S.  graminis 
Schwartz  (1911),  were  later  added  to  the  genus.  These  forms 
correspond  to  *S'.  veronicae  Schrot.  in  all  the  essential  features 
of  the  life  cycle,  though  the  spore  balls  are  much  less  regular 
in  form,  the  spores  sometimes  adhering  merely  in  chains.  The 
host  is  not  stimulated  to  form  galls,  the  attacked  roots  being 
even  thinner  than  the  normal  ones.  When  Maire  and  Tison 
(1911)  founded  their  new  germs  Lignier a,  to  include  all  the  species 
of  the  family  which  do  not  cause  hypertrophy  of  the  host,  they 
transferred  to  it  S.  junci;  and  the  following  year  S.  graminis, 
which  had  meanwhile  been  pubhshed,  was  placed  in  Ligniera  by 
Winge  (1912).  Subsequently,  Cook  (1926)  has  shown  by  inocu- 
lation experiments  that  these  two  species  are  identical,  and  that 
several  other  species  (L.  bellidis  Schwartz,  L.  mcnthae  Schwartz, 
L.  alismatis  Schwartz,  L.  pilorum  Fron  &  Gaillat)  more  recently 
described  were  also  based  on  this  one  species.  The  genus 
Ligniera  contains  several  other  species  (L.  radicalis  Maire  & 
Tison,  L.  verrucosa  Maire  &  Tison,  L.  isoetes  Palm).  Cook 
(1926)  considers  it  highly  probable  that  L.  radicalis  is  also 
identical  with  *S.  junci.  On  the  other  hand,  L.  verrucosa  Maire 
&  Tison  is  clearly  a  distinct  species,  marked  by  its  roughened 
spores  and  thc'r  less  evident  tendency  to  cling  together  in  definite 
masses;  and  L.  isoetes  Palm,  if  in  fact  a  member  of  this  group, 
is  certainly  distinct. 

As  the  genus  Ligniera  Maire  &  Tison  was  based  merely  on 
a  host  reaction  the  writer  is  wholly  disinclined  to  accept  it  as 
valid.  It  is  clear  that  two  hosts  may  react  quite  differently 
to  a  given  parasite,  one  being  stimulated  to  gall  formation,  while 
the  other  is  not.  It  seems  best  for  the  present  to  include  all  of 
the  species  in  Sorosphaera,  even  though  in  some  the  tendency 
to  form  definite  spore  balls  is  much  less  evident  than  in  the  type 
species  S.  veronicae  Schroter.  The  genus  as  thus  reconstituted 
includes  besides  the  type  also  *S.  junci  Schwartz,  and  tentatively 


62 


THE  LOWER  FUNGI— PHYCOMYCETES 


as  doubtful  members  S.  radicalis  (Maire  &  Tison),  S.  verrucosa 
(Maire  &  Tison),  and  S.  isoetes  (Palm).  Further  study  may 
result  in  the  transfer  of  some  of  these  latter  forms  to  other  genera. 
A  discussion  of  the  doubtful  genus  Rhizomyxa  Borzi  (1884) 
may  be  inserted  most  logically  perhaps  at  this  point.  This 
genus  includes  only  the  type  species,  R.  hypogaea  Borzi, 
described  as  parasitic  in  the  roots  of  a  number  of  flowering  plants. 
It  has  been  variously  interpreted  in  the  literature.  Borzi 
pictured  and  discussed  both  asexual  and  an  asexual  stage  (Fig.  5), 


rTH  f'l  I 


Fig.  5. — Rhizomyxa  hypogaea  Borzi.  (a)  Young  thalli  in  cortical  cells  of 
Stellaria  media,  (h)  Formation  of  sporangia,  (c,  d)  Sori  of  sporangia,  that 
at  (c)  in  a  root  hair,  (e,  f)  Zoospores  infecting  host  ceils,  {g)  Swarmspores. 
{h)  Germinating  sporangia  with  exit  tubes,  (s)  Thallus  divided  by  septum 
to  form  oogonium  and  antheridium.  (0  After  fertilization  showing  oospore 
in  oogonium.      {After  Borzi  I884.) 

but  in  the  light  of  later  work  on  other  forms  it  seems  highly  prob- 
able that  he  based  his  description  on  a  mixture  of  two  or  more 
different  organisms.  In  the  sexual  process  as  described  the 
thallus  elongates  and  becomes  septate  into  two  unequal  cells, 
one  of  which  functions  as  an  antheridium  and  the  other  as  an 
oogonium.  In  the  oogonium  a  differentiation  of  the  contents 
into  periplasm  and  ooplasm  precedes  fertilization,  and  at  matur- 
ity a  single  oospore  lies  free  in  the  oogonium.  This  account  was 
accepted  by  Schroter  (1892:  91)  and  he  was  led  by  it  to  place 
the  genus  in  the  Ancylistales.  Fischer  (1892:  69),  von  Minden 
(1911:  278),  and  others  have  excluded  this  stage  from  consider- 
ation.    In  the  asexual  phase,  according  to  Borzi,  the  thallus  is 


CHYTRIDIALES  63 

at  maturity  a  naked,  multinucleate  plasma  which  tends  to  fill 
the  host  cell.  It  may  assume  a  membrane  and  function  directly 
as  a  multispored  sporangium,  or  it  may  break  up  while  yet 
naked  into  a  number  of  uninucleate  bits  each  of  which  becomes 
invested  in  a  wall.  Each  of  these  bits  is  comparable  to  the  spore 
of  Sorosphaera  and  on  germination  frees  two  to  four  zoospores. 
Maire  and  Tison  regard  Rhizomyxa  as  a  complex  of  several  organ- 
isms, and  feel  that  this  phase  is  probably  merely  S.  verrucosa. 
The  multispored  sporangium  may  be  that  of  an  Olpidium. 

More  recently  Nemec  has  described  two  genera,  SoroJpidium 
Nemec  (1911  c)  and  Anisomyxa  Nemec  (1913  a),  which  should  be 
given  consideration  in  connection  with  Rhizomyxa.  In  the 
first,  based  on  S.  hetae  Nemec,  found  in  the  living  cortical  cells 
of  Beta  vulgaris,  the  thallus  persists  to  maturity  as  a  naked 
multinucleate  protoplast,  and  then  is  said  to  become  invested 
in  a  thin  membrane.  Fragmentation  finally  results  in  the  forma- 
tion of  a  sorus  of  spores  each  of  which  later  frees  one  to  several 
zoospores.  (See  Guyot,  A.  L.,  Rev.  Path.  Veg.  et  Ent.  Agric., 
14 :  176-183,  1927.) 

In  Anisomyxa,  based  on  A.  plantaginis  Nemec,  found  in  the 
roots  of  Plantago,  a  similar  situation  exists.  The  individual 
sporangium  may  be  relatively  large,  and  frees  a  considerable 
number  of  spores.  A  common  soral  envelope  was  not  observed. 
Nemec's  accounts  do  not  carry  conviction,  and  leave  us  in  doubt 
concerning  essential  points  in  the  life  cycle  in  both  genera.  If 
he  has  not  misunderstood  his  material  these  forms  seem  to  be 
intermediate  between  Plasmodiophora  and  the  Synchytriaceae. 
They  should  be  studied  further, 

4.  Sorodiscus  Lagerheim  &  Winge  (Winge,  1912). 

In  1870,  Kareltschikoff  and  Rosanoff  described  pecuhar  flat 
plate-hke  bodies  which  they  found  in  the  cells  of  Callitriche 
autumnalis.  These  bodies  were  later  observed  by  Lagerheim  in 
C.  vernalis,  and  were  recognized  by  him  to  be  spore  aggregations 
of  one  of  the  Plasmodiophoraceae.  In  1912,  Winge,  working 
over  Lagerheim's  material,  made  these  the  basis  of  the  new  genus 
Sorodiscus  and  the  new  species  S.  callitrichis  Lagerheim  & 
Winge. 

The  spore  aggregations  are  flattened  plates  of  uniform  thick- 
ness but  of  var>dng  outline  and  diameter  depending  on  the  size 
and  form  of  the  host  cell.     The  plate  consists  of  two  layers  of 


64  THE  LOWER  FUNGI— PHYCOMYCETES 

small  polygonal  cells,  the  spores.  Between  the  two  layers  a 
small  lumen  occasionally  occurs.  This  indicates  that  the  plates 
are  in  reality  much  flattened  hollow  spheres  or  ellipsoids,  and 
the  genus  is  believed  by  Winge  to  be  very  close  to  Sorosphaera. 
Winge  did  not  observe  infection  nor  the  uninucleate  stage  of  the 
myxamoeba.  Later  stages  were  studied,  and  the  form  seems 
to  correspond  in  the  main  to  other  members  of  the  group.  Young 
myxamoebae  and  mature  spore  balls  were  observed  together 
in  the  same  host  cell.  The  individual  spores  are  finally  spherical. 
Spore  germination  was  not  observed. 

5.  Spongospora  Brunchorst  (1887). 

The  spore  balls  of  Spongospora  are,  as  the  name  signifies, 
tiny  sponge-like  aggregations  of  spores.  The  interior  of  the 
ball,  unlike  that  of  Sorosphaera,  is  essentially  solid,  and  is  tra- 
versed by  broad  fissures  which  open  to  the  surface  as  prominent 
lacunae  (Fig.  6).  In  shape  the  ball  is  globose  or 
somewhat  elongated,  and  the  individual  spores, 
while  actually  polyhedral  from  mutual  pressure, 
are  potentially  spherical. 

The  genus  contains  the  single  species,  Spon- 
gospora subterranea  (Wallroth)  Lagerheim,  cause 
of  powdery  scab  of  potatoes.     When  Brunchorst 
Fig.  6.  —  Spongo-  erected  the  genus  he  named  the  organism  S. 
(Waiir^othT  LTger-  i'olani,  not  realizing  that  the  earlier  name  Ery- 
heim.  A  single  spore  sibe  subterrauea  Wallroth  (1842)  had  been  given 
ball.    {Original.)        ^^    .^_     rj.^^   identity   of   the   two   forms   was 

recognized  by  Lagerheim  (1892:  104),  and  the  existence  of  other 
early  synonyms  was  noted.  Martins  (1842:  28)  named  the 
species  Protomyces  tuberum  solani,  and  Berkeley  (1846:  33) 
called  it  Tubercinia  scabies.  The  organism  came  into  prominence 
through  the  papers  of  Massee  (1908)  and  Johnson  (1907;  1908; 
1909)  on  economic  aspects  of  the  potato  disease.  Massee  used 
the  name  Spongospora  scabies  (Berkeley)  Massee.  Later  the 
organism  was  studied  cytologically  by  Osborn  (1911  a,  6) 
and  Home  (1911);  while  Melhus  (1914  h)  and  Kunkel  (1915) 
have  published  on  its  life  history. 

When  Brunchorst  established  the  genus  he  saw  a  plasmodium- 
like  stage  associated  with  the  spore  balls,  and  regarded  the 
organism  as  a  relative  of  the  slime  moulds.  Lagerheim  opposed 
this  point  of  view,  and  Maire  and  Tison  failed  to  include  the  genus 


CHYTRIDIALES  65 

in  the  Plasmodiophoraceae.  Later  workers  have,  however, 
generally  regarded  the  organism  as  a  member  of  this  group. 

Our  knowledge  of  the  life  history  of  the  species  is  consider- 
ably confused  by  contradictions  in  the  accounts  of  Johnson, 
Home,  Osborn,  and  Kunkel.  According  to  Johnson  the  spore 
germinates  by  eight  zoospores,  while  Kunkel  states  that  the 
entire  content  emerges  as  a  single  zoospore.  Kunkel  says  further 
that  the  various  zoospores  which  emerge  from  the  spores  compos- 
ing a  spore  ball  may  coalesce  to  form  a  tiny  plasmodium,  and 
that  this  is  capable  of  infecting  the  host  by  passing  down  into  the 
tuber  between  its  cells.  In  the  host  cell  the  behavior  of  the 
protoplast  of  the  parasite  seems  to  be  much  like  that  of  other 
species  of  the  family.  At  maturity  several  spore  balls  may  exist 
together  in  the  same  cell.  Osborn  states  that  immediately 
preceding  spore  formation  the  nuclei  fuse  in  pairs  throughout 
the  protoplast,  and  that  this  is  followed  by  the  reduction  divi- 
sions. Additional  investigation  of  the  organism  is  desirable  in 
the  light  of  the  evident  contradictions  in  the  published  accounts. 

The  genus  Clathrosorus  Ferdinandsen  and  Winge  (1920)  was 
based  on  the  single  species,-  C.  campatiulae  Ferd.  &  Wge.  col- 
lected in  Denmark  on  the  roots  of  Campanula  rapunculoides. 
The  organism  causes  the  formation  of  small  galls  resembling  the 
legume  tubercles.  Spore  balls  somewhat  resembling  those  of 
Spongospora  were  found,  the  individual  spores  having  a  minutely 
warted  membrane.  The  "cruciform"  type  of  nuclear  division  is 
pictured.  The  account  is  very  brief,  and  knowledge  of  the  life 
cycle  too  inadequate  to  warrant  recognition  of  the  genus.  The 
organism  is  perhaps  a  relative  of  Spongospora. 

Excluded  Genera 

The  following  genera,  which  have  been  incorporated  in  the 
Plasmodiophoraceae  in  certain  recent  treatments,  are  regarded 
as  falling  outside  the  limits  of  the  group  as  here  understood. 

1.  Sporom3rxa  Leger  (1908). 

An  organism  found  in  the  coelomic  cavity  of  the  imago  of 
Scaurus  tristis  was  named  Sporomyxa  scauri  Leger,  and  made  the 
basis  of  this  genus.  Although  Leger  referred  the  species  to  the 
Plasmodiophoraceae  its  incorporation  in  the  family  does  not 
seem  justified.  In  addition  to  the  fact  that  it  occurs  in  an 
animal  host,  its  possession  of  ellipsoidal  spores  indicates  lack  of 


66  THE  LOWER  FUNGI— PHYCOMYCETES 

relationship.     In  any  case  our  knowledge  of  its  life  cycle  and 
cytology  is  insufficient  to  warrant  its  inclusion  here. 

2.  Ostenfeldiella  Ferdinandsen  &  Winge  (1914:  648). 

This  genus  was  based  on  material  collected  by  Ostenfeld  on  the 
coast  of  St.  Croix  (West  Indies)  on  Diplanthera  wrightii  one  of 
the  Potomogetonaceae.  The  organism  was  found  in  the  con- 
spicuously thickened  internodes  of  the  erect  branches,  and  was 
named  0.  diplantherae  Ferd.  &  Wge.  Certain  cells  of  the  host 
were  found  packed  with  brown,  thick-walled  spores.  Uni- 
nucleate amoebae  were  found  in  others.  Although  other  stages 
were  not  observed  the  organism  was  placed  in  the  Plasmodio- 
phoraceae  by  the  authors  of  the  new  genus.  There  seems  to  be 
but  slight  reason  for  including  it  in  the  group,  and  at  best  its 
position  is  doubtful.     The  authors  did  not  see  living  material. 

3.  Cystospora  Elliott  (1916:  15). 

This  genus  was  based  by  Elliott  on  a  single  species,  C.  batata 
Elliott,  which  he  found  to  be  the  cause  of  a  characteristic  disease 
of  the  tubers  of  sweet  potato  called  pox  or  soil-rot.  Although 
he  assigned  the  genus  to  the  Plasmodiophoraceae  there  is  in  fact 
little  in  the  published  account  to  indicate  relationship  with  this 
group. 

Woroninaceae 

Mycelium  wholly  lacking;  thallus  intramatrical,  usually 
occurring  in  water  moulds,  in  early  stages  existing  as  a  naked, 
more  or  less  amoeboid  protoplast,  at  maturity,  in  some  cases, 
forming  a  membrane  and  functioning  as  a  single  sporangium  or 
resting  spore,  in  others,  fragmenting  into  a  number  of  naked 
parts,  each  of  which  then  assumes  a  membrane  and  functions 
as  a  sporangium  or  resting  spore;  the  sorus,  thus  formed,  conse- 
quently never  provided  with  a  soral  envelope ;  sporangia  typically 
multispored;  zoospores  laterally  biciliate,  as  in  the  Oomycetes. 

Key  to  Genera  of  Woroninaceae 

I.   Mature  thallus  functioning  as  a  single  sporangium  or  resting  spore. 

A.  Resting  spore  lacking  a  companion  cell. 

1.  Pseudolpidlum,  p.  67 

B.  Resting  spore  bearing  one  or  more  companion  cell^i. 

2.  Olpidiopsis,  p.  67 


CHYTRIDIALES  67 

II.  Mature  thallus  dividing  to  form  a  sorus  of  sporangia  or  resting  spores, 
or  functioning  in  its  entirety  as  a  resting  spore. 

A.  Sporangia  short-cylindrical,  lying  in  a  single  row,  filling  the  lumen 

of  the  host  hypha;  resting  spores  lying  free  as  isolated,  spiny 
spheres;  each  resting  spore  resulting  from  the  transformation  of 
an  entire  thallus. 

3.  Rozella,  p.  68 

B.  Sporangia  globose,  lying  free  in  the  host  cell  and  constituting  a 

loose  aggregation  of  indefinite  form;  resting  spores  similarly 
arranged  or  fused  to  form  a  warty  cystosorus. 

4.  Woronina,  p.  69 

1.  Pseudolpidium  Fischer  (1892:  33). 

syn.  Olpidiopsis  (Cornu)  Schroter  (1892:  69). 

Sporangium  smooth-walled;  resting  spore  spiny;  companion 
cell  lacking;  swarmspores  biciliate. 

This  genus  and  Olpidiopsis  differ  from  Olpidium  and  Pseudolpi- 
diopsis  respectively  of  the  following  family  chiefly  in  the  biciliate 
character  of  their  swarmspores.  They  are  said  to  agree  with  the 
other  members  of  the  Woroninaceae  in  the  absence  of  a  membrane 
on  the  young  thallus,  but  this  point  has  not  been  thoroughly 
demonstrated.  As  the  number  of  ciha  on  the  swarmspore  may  be 
determined  with  certainty  only  in  favorable  material  the  separa- 
tion of  species  of  these  corresponding  genera  involves  accurate 
observation.  A  discussion  of  the  interrelationships  of  the  four 
genera  is  given  below  under  Olpidium.  The  following  are  the 
best  known  species  of  Pseudolpidium. 

P.  saprolegniae  (Braun)  Fischer — in  Saprolegnia. 
P.  fusiforme  (Cornu)  Fischer — in  Achlya. 
P.  aphanomycis  (Cornu)  Fischer — in  Aphanomyces. 
P.  pythii  Butler — in  Pythium. 

2.  Olpidiopsis  (Cornu)  Fischer  (1892:  37). 

syn.   Diplophysa  Schroter,   subgenus  Euolpidiopsis  Fischer 
(in  Schroter  1892:  85). 
Sporangium  smooth-walled;  resting  spore  tuberculate  or  spiny; 
companion  cell  present;  swarmspores  biciliate;  all  known  species 
parasitic  in  Saprolegniaceae. 

The  following  species  have  been  critically  studied. 

0.  saprolegniae  Cornu— in  Saprolegnia  (Fig.  7,  e). 

0.  vexans  Barrett — in  Saprolegnia  (Fig.  7,  a-d). 

O.  minor  Fischer— in  Achyla. 

O.  aphanomycis  Cornu — in  Aphanomyces. 

O.  luxurians  Barrett — in  Aphanomyces. 


68 


THE  LOWER  FUNGI— PHYCOMYCETES 


3.  Rozella  Cornii  (1872:  114). 

A  small  genus  containing  two  species,  one  R.  septigena  Cornu 
(Fig.  8)  parasitic  in  threads  of  Saprolegnia,  the  other,  R.  simulans 
Fischer,  in  Achlija.  After  the  entrance  of  the  infecting  swarm- 
spore  the  parasite  exists  for  a  time  as  a  naked  protoplast  indis- 
tinguishable from  the  protoplasm  of  the  host.  It  grows  at  the 
expense  of  the  host,  and  finally  fills  entirely  the  lumen  of 
the  host  hypha.  The  formation  of  transverse  septa  divides  the 
thallus  into  a  single   row  of  short  cylindrical  sporangia  whose 


Fig.  7.- — (a-d)  Olpidiop.sis  vcxans  Barrett,  {c)  O.  saprolegniae  Cornii.  (a) 
Swollen  tip  of  hypha  of  Saprolegnia  containing  both  emptied  and  unemptied 
swarmsporangia  of  the  parasite,  (h)  Single  sporangium  with  abnormal,  long, 
coiled  exit  tubes,  (c)  Biciliate  swarmspores.  (d)  Emptied  swarmsporangia 
and  verrucosa  resting  spores  with  companion  cells,  (c)  Spiny  resting  spore  with 
companion  cell.      (After  Barrett  1912.) 

lateral  walls  are  fused  with  the  wall  of  the  host.  Each  spor- 
angium breaks  up  into  a  large  number  of  biciliate  swarmspores, 
and  these  escape  through  a  short,  usually  lateral  exit  papilla. 
Other  thalli  assume  the  spherical  form  and  develop  into  thick- 
walled  spiny  resting  spores  lying  free  in  the  host  cell.  They  occur 
more  often  in  short  lateral  branches  which  tend  to  become  globose, 
and  have  in  young  stages  the  aspect  of  immature  oogonia.  The 
method  of  germination  of  the  resting  spore  is  unknown.  No 
evidence  of  the  existence  of  sexuality  in  the  genus  has  been 
encountered. 


CHYTRIDIALES 


69 


4.  Woronina  Cornu  (1872:  114). 

The  thallus  in  early  stages  is  obscured  by  the  protoplasm  of 
the  host,  but  later  appears  as  a  naked  protoplast  of  variable  form. 
The  host  lays  down  transverse  septa  confining  it  to  a  definite 


Fig.  8. — Rozella  scptigena  Cornu  in  hyphae  of  Saprolegnia.  (a)  Linear  series 
(sorus)  of  sporangia  of  Rozella  in  end  of  host  hypha,  lower  three  fully  formed, 
terminal  three  developing  at  expense  of  host  protoplasm,  (b)  Similar  sorus, 
the  terminal  sporangium  of  which  is  freeing  swarmspores.  (c)  Single  terminal 
sporangium;  the  wall  of  the  parasite  distinguishable  from  that  of  the  host  where 
the  lateral  exit  papillae  are  pushing  out.  ((/)  Swarmspores.  (c)  Spiny  resting 
spores  of  Rozella  lying  in  lateral  host  branches  which  are  perhaps  oogonia.  (After 
Cornu  1872.) 


short  cell  or  compartment.  Several  such  cells  enclosing  different 
thalli  may  form  a  linear  series.  At  maturity  the  thallus,  having 
absorbed  completely  the  protoplasm  of  the  host  cell,  fragments, 
forming  a  number  of  globose  sporangia  each  of  which  then 


70 


THE  LOWER  FUNGI— PHYCOMYCETES 


assumes  a  thin  smooth  membrane.  The  sporangia  lie  in  a  loose 
cluster  free  from  one  another  and  only  partially  fill  the  host  cell. 
Each  sporangium  at  maturity  frees  a  number  of  biciliate  swarm- 
spores  through  an  inconspicuous  axit  papilla.  Other  thalli 
develop  the  resting  stage.     In  W.  pohjcystis  Cornu  occurring  in 


c  b. 


^S^r^-J" 


Fig.  9. —  (a-g)  Woronina  polycystis  Cornu  in  Saprolegnia.  (h)  TV.  glomcrata 
(Cornu)  Fischer  in  Vaucheria.  (a)  Host  hypha  with  two  sori  of  swarmsporangia, 
and  at  the  tip  a  compartment  in  which  the  thallus  of  the  parasite  is  as  yet 
indistinguishable  from  the  cytoplasm  of  the  host.  {!>)  Linear  series  of  compart- 
ments, two  containing  sori  of  swarmsporangia  and  two  cystosori.  (c)  Sorus 
of  swarmsporangia.  (d)  Two  sori  of  swarmporangia  and  three  cystosori,  one 
imusually  small,  (e)  Swarmspores  delimited  in  sporangia.  (/)  Swarmspores. 
((7)  Median  section  of  cystosorus.  {h)  Sorus  of  resting  spores,  {d,  and  /, 
after  A.  Fischer  1882;  others  after  Cornu  1872). 


Saprolegnia  the  thallus  fragments  to  form  a  number  of  resting 
spores  but  these  fuse  forming  a  single  large  thick-walled  warty 
body  termed  the  cystosorus  (Fig.  9,  a~g).  In  W.  glomerata 
(Cornu)  Fischer,  in  Vaucheria,  each  restign  spore  assumes  a 
spiny  wall,  and  a  loose  cluster  of  small  spherical  resting  spores 
resembling  the  sporangial  sorus  results  (Fig.  9,  h). 


CHYTRIDIALES  71 

The  genus  Pyrrhosorus  Juel  (1901:  14)  founded  on  P.  marinus 
Juel,  a  saprophyte  in  dead  branches  of  Cystoclonium  purpura- 
scens,  is  imperfectly  known,  but  seems  to  fall  near  Woronina. 

Olpidiaceae 

Mycelium  wholly  lacking;  thallus  intramatrical,  provided  from 
an  early  period  with  a  thin  membrane,  at  maturity  functioning 
in  its  entirety  as  a  single  sporangium  or  resting  spore;  zoospores 
uniciliate;  cilium  at  the  posterior  end  of  the  spore. 

Key  to  Genera  of  Olpidiaceae 

I.   Sporangium  lying  free  in  the  host  cell. 

A.  Sporangium  not  provided  with  numerous  exit  tubes. 

1.  Mature  sporangium  ellipsoidal  to  fusiform,  lacking  elongate 

exit  tubes,  dehiscing  at  one  or  both  ends  by  a  simple  pore 
or  short  papilla. 

1.  Sphaerita,  p.  72 

2.  Mature  sporangium  more  or  less  globose. 

a.  Resting  spore  globose  to  ellipsoidal,  becoming  stellate 
by  shrinkage;  sporangium  sometimes  dehiscing  by  a 
simple  pore,  sometimes  by  an  exit  tube. 

2.  Olpidiaster,  p.  72 

h.  Resting  spore  not  becoming  stellate  by  shrinkage; 
sporangium  dehiscing  by  one  to  few  elongate  exit 
tubes. 

(1)  Resting  spore  not  bearing  a  companion  cell. 

3.  Olpidium,  p.  73 

(2)  Resting  spore  bearing  one  or  more  companion  cells. 

4.  Pseudolpidiopsis,  p.  76 

B.  Sporangium  with  numerous  exit  tubes. 

1.  Sporangium  tubular;  exit  tubes  short  and  arranged  in  a  row. 

5.  Ectrogella,  p.  77 

2.  Sporangium  globose;  exit  tubes  long  and  protruding  in  many 

directions. 

6.  Pleotrachelus,  p.  78 

II.  Sporangial  wall  tightly  appressed  to  the  wall  of  the  host  cell. 

A.  Wall  of  host  and  that  of  parasite  completely  fused;  no  line  of 

demarcation  discernible  between  them;  parasites  on  other  fungi. 

7.  Pleolpidium,  p.  78 

B.  Walls  of  host  and  parasite  merely  in  contact,  not  fused;  parasites 

in  algae. 

8.  Plasmophagus,  p.  70 


72 


THE  LOWER  FUNGI— PHYCOMYCETES 


1.  Sphaerita  Dangeard  (Ann.  Sci.  Nat.  7  sqr.  6o«.,  4:277,  1886). 

(See  also  Le  Botaniste,  1 :  46,  pi  2-S;  4 :  234,  fig.  7-8,  and 

Bui.  Soc.  Bot.  France,  74 :  472,  1927.) 

The  genus  was  founded  on  S.  endogena  Dang,   parasitic  in 

Euglena  and  other  Protozoa.     As  described  by  Dangeard  the 

sporangium  is  clhpsoidal  (Fig.  10,  a,  6)  and  opens  by  a  pore. 


Fig.  10. — Sphaerita  endogena  Dangeard  in  Euglena.  (a)  Young  swarmsporan- 
gium.  (h)  Germinating  swarmsporangium.  (c,  c)  Spiny  resting  sporangium. 
(d)  Fusiform  swarmsporangium.  (a,  b,  c,  e,  after  Dangeard  1880;  d,  after  Ser- 
binow  1907.) 

In  a  later  account  by  Serbinow  (Scripta  Hort.  Bot.  Petrop.,  24  :  154, 
pi.  5,  1907)  it  is  pictured  as  fusiform,  and  is  stated  to  have  a 
short  exit  papilla  at  one  or  both  ends  (Fig.  10,  d).  Another 
species  S.  trachelomonadis  Skvortzow  (1927:  205)  has  been 
described  from  China  in  Trachelomonas. 


2.  Olpidiaster  Pascher  {Beih.  Bot.  Centralhl,  35^ :  578,  1917). 
syn.    Asterocystis    DeWildeman   (Ann.   Soc.   Beige  Micros., 
17:  21,  1893);  antedated  by  Asterocystis  Gobi  (1879),  an 
algal  genus. 


CHYTRIDIALES  73 

A  single  species,  0.  radicia  (De  Wild.)  Paschcr,  is  included 
in  the  genus.  It  is  parasitic  on  the  roots  of  various  plants, 
especially  the  Cruciferac,  and  causes  chlorosis.  The  genus 
differs  from  Olpidium  chiefly  in  the  stellate  aspect  of  the  shrunken 
resting  spore.  As  originally  described  the  sporangia  dehisce 
by  a  simple  pore.  Recently,  however,  Guyot  (1927:  79)  has 
figured  sporangia  of  0.  radicis  provided  with  elongate  exit  tubes 
and  the  question  of  the  advisabihty  of  merging  this  genus  in 
Olpidium  may  well  be  raised.  The  wall  of  the  resting  spore  in 
Olpidiaster  is  colorless. 

The  genus  Chnjsophlyctis  Schilbersky  was  included  in  the 
Olpidiaceae  by  von  Minden,  and  resembles  Olpidiaster  in  having 
a  resting  sporangium  which  is  somewhat  stellate  in  form,  though 
the  wall  differs  in  being  dark  colored.  The  genus  is  based  on  a 
single  species,  Ch\  endobiotica  Schilb.,  cause  of  the  black  wart 
of  potato.  Further  investigation  has  shown  that  this  species 
is  in  fact  a  Synchyfrium,  and  it  is  discussed  under  that  genus  in 
the  following  family. 

3.  Olpidium  Schroter  (1886:  180). 

The  largest  and  best  known  genus  of  the  family,  containing 
about  twenty-five  species  on  a  variety  of  substrata,  including 
the  tissue  of  higher  plants,  pollen  grains,  uredospores,  mycelium 
of  Saprolegnia,  various  algae,  and  lower  animals.  Both  swarm- 
sporangia  and  resting  spores  are  commonly  developed.  The 
former  are  relatively  thin-walled,  globose  to  elhpsoidal,  and 
smooth.  They  germinate  usually  by  a  single  prominent  exit 
tube,  which  penetrates  the  host  tissue,  ruptures  at  its  apex,  and 
frees  swarmspores.  The  resting  spores  are  thicker-walled, 
smooth  or  verrucose,  and  also  germinate  by  swarmspores.  The 
following  species  are  common. 

O.  brnssicae  (Wor.)  Dang. — in  cabbage  (Fig.  11). 

O.  pendulum  Zopf — in  pollen  in  water. 

O.  endogemim  (Braun)  Schroter — in  desmids. 

O.  uredinis  (Lag.)  Fischer — in  uredospores  of  rusts. 

O.  zygnemicolum  P.  Magnus — in  Zygnema. 

O.  entophytum  Braun — in  Spirogyrn,  Vaucheria,  and  Cladophora. 

O.  oedogoniarum  (Sorokin)  De  Wildeman — ^in  Oedogonium. 

The  genera  Olpidium  and  Pseudolpidiopsis  of  this  family  and 
Pseudolpidium  and  Olpidiopsis  of  the  preceding  family  should 
be  discussed  together  since  the  similarity  in  form  and  aspect  of 


74 


THE  LOWER  FUNGI— PHYCOMYCETES 


these  fungi  raises  at  once  the  question  of  their  relationship. 
The  generic  Hmits  used  here  are  those  adopted  by  von  Minden 
(1911:  228,  260)  and  differ  considerably  from  those  of  older 
authors.  Schroter  (1886:  195;  1892:  67,  84),  in  his  treatment  of 
these  forms,  includes  in  the  genus  Diplophysa  all  species  in  which 
the  resting  spore  bears  companion  cells.  He  placed  the  remaining 
species  in  Olptdium  and  Olpidiopsis,  including  in  Olpidium  those 
with  uniciliate  zoospores  and  smooth-walled  resting  spores,  and 
in  Olpidiopsis  those  with  biciliate  zoospores  and  spiny  resting 
spores.  Fischer  (1892:  16)  recognized  three  genera  correspond- 
ing in  their  limits  with  those  of  Schroter,  but  in  his  treatment 
the  name  Pseudolpidium  replaces  Olpidiopsis  while  Olpidiopsis 


Fig.  II.' — Olpidium  hrassicae  (Woronin)  Dangoard.  (a)  Three  swarmsporan- 
gia  with  long  exit  tubes.  (6)  Swarmspores.  (c)  Roughened  thick-walled 
resting  spores.      {After  Woronin  1878.) 

replaces  Diplophysa.  This  confusing  difference  in  application 
of  generic  names  makes  necessary  a  critical  consideration  of  all 
the  points  involved. 

The  classification  of  von  Minden  (1911:  227)  differs  strikingly 
from  older  arrangements  in  the  recognition  of  the  new  family 
Woroninaceae.  In  this  family  are  placed  those  forms  in  which 
the  zoospores  are  biciliate,  and  in  which  the  thallus  is  naked  in 
at  least  its  early  stages.  The  genera  Pseudolpidium  and  Olpidiop- 
sis included  in  the  Woroninaceae,  correspond  respectively  with 
Olpidium  and  Pseudolpidiopsis  of  the  Olpidiaceae  and  differ 
from  them  only  in  the  family  characters. 

The  companion  cell  present  on  the  resting  spore  in  Olpidiopsis 
and  Pseudolpidiopsis  affords  a  morphological  character  useful 
in  generic  separation  irrespective  of  the  question  of  sexuality 


CHYTRIDIALES  75 

involved.     In  these  genera  two  thalli  come  in  contact  in  early- 
stages,  one  functioning  as  the  male  gametangium,  the  other  as 
the  female.     The  male  individual,  after  discharging  its  contents 
through  a  pore  connection  into  the  female,  remains  attached  to 
it,  and  is  present  later  on  the  enlarged  mature  female  cell  (resting 
spore)  as  a  small  empty  companion  cell.     In  some  cases  more 
than  one  companion  cell  may  be  present.     Those  thalli  which 
do  not  conjugate  develop  into  thin-walled  swarmsporangia.     A 
critical  cytological  study  of  three  species  of  Olpidiopsis  was  made 
by  Barrett  (1912),  and  his  results  indicate  strongly  that  the  two 
thalli  which  fuse  show  true  sexual  differentiation.     He  regards 
these  fungi  as  primitive  Oomycetes.     The  absence  of  a  companion 
cell  on  the  resting  spore  of  Olpidium  and  Pseudolpidium  does 
not  on  the  other  hand  of  necessity  indicate  a  lack  of  sexuality 
in  these  forms.     A  fusion  of  ciliate  gametes   (resembling  zoo- 
spores) has  been  observed  in  several  cases  and  perhaps  occurs 
in  many  species  of  these  genera.     In  such  cases  complete  fusion 
results  in  a  zygote,  there  being  no  emptied  male  cell.     Kusano 
(1912)  has  described  the  fusion  of  such  swarmspore-like  gametes 
in  0.  viciae,  and  finds  that  the  zygote  develops  into  a  resting 
sporangium,    while    zoospores    (without    fusing)    develop    into 
swarmsporangia.     It  seems  probable  from  the  observations  of 
Nemec  (1912)  that  the  same  type  of  life  history  exists  in  0.  bras- 
sicae,  and  careful  study  will  doubtless  demonstrate  it  in  other 
species.     It  was  long  ago  observed  by  Fisch  (1884:  17)  in  the 
two  species  on  which  he  based  the  genus  Reesia.     In  this  genus 
ciliate  zoospore-like  gametes  fuse  in  pairs  outside  the  host.     The 
zygote  infects  the  host,  and  in  it  is  amoeboid  for  a  considerable 
period,  finally  maturing  into  a  resting  sporangium.     Whether 
the  nuclei  fuse  is  not  known.     Von  Minden  (1911 :  238,  243)  does 
not  recognize  the  genus,   and  incorporates  the   species  under 
Olpidium.     An  imperfectly  understood  species  occurring  in  the 
leaves  of  ragweed,  and  made  by  Griggs  (1910:  50)  the  type  of  a 
new  genus,  Monochytrium  Griggs,  also  probably  belongs  here. 
In  this  case  the  stages  outside  the  host  are  unknown,  but  in  the 
host  cells,  uninucleate  amoeboid  individuals  fuse  in  pairs,  the 
zygote  finally  being  invested  in  a  thick  wall.     Neither  nuclear 
fusion  nor  germination  of  the  resting  spore  was  observed.     The 
occurrence  of  planogamic  copulation  in  these  forms  is  of  par- 
ticular interest  to  the  student  of  phylogeny  since  it  demonstrates 
parallelism  of  the  evolution  of  the  sexual  process  between  fungi 


76 


THE  LOWER  FUNGI—FIIYCOMYCETES 


and  algae  down  to  the  level  of  the  most  primitive  forms.  An 
interesting  elaboration  of  this  point  is  given  by  Ramsbottom 
(1914). 


-4-^--^ 


Fig.  12.- — Pscudolpidiopsis  schcnkinna  (Zopf)  v.  Mindon  in  Spirofjyra.  (a) 
Encysted  swarmsporcs  germinating  and  acconiijlisliing  infection,  {h)  Young 
thallus  developing  from  protoplast  of  s\varmsi)ore  and  still  attached  to  the 
empty  cyst  wall,  (c-e)  Mature  swarmsporania.  (/)  After  conjugation  of 
two  young  thalli  in  a  host  cell,  (y)  Mature  resting  spore  with  companion  cell. 
{h)  Germinating  resting  spore.      {After  Zopf  18S4)- 

4.  Pseudoipidiopsis  v.  Minden  (1911:  255). 

syn.  Diplophysa  Schroter,  subgenus  Pleocystidium  Fischer 
(in  Schroter  1892:85). 
A  single  character,  the  presence  of  the  companion  cell  on  the 
resting  spore,  serves  to  separate  this  genus  from  Olpidium.     The 


CHYTRIDIALES 


77 


two  genera  are  evidently  very  closely  related  and  should  perhaps 
be  merged.  The  first  species  enumerated  below  (Fig.  12)  is  the 
type  of  the  genus.  In  it  the  resting  spore  is  smooth- walled. 
The  other  species  possess  spiny-walled  resting  spores  and  have 
not  been  studied  sufficiently  to  warrant  their  certain  inclusion 
here.     All  of  the  species  occur  in  green  algae. 

F.  schenkiana  (Zopf)  v.  Mindcn— in  the  filaments  and  zygospores  of 
Spirogyra,  Mougentia,  and  Me.socarpus.  Anotlicr  form,  1\  parasitica  (Fisch) 
V.  Minden,  said  to  differ  in  having  several  companion  cells  on  the  resting 
spore  is  perhaps  the  same. 

P.  zopfii  (De  Wild.)  v.  Minden  and  P.  fibrillosa  (De  Wild.)  v.  Minden 
occur  in  Spirogyra  and  differ  chiefly  in  the  character  and  arrangement  of  the 
spines  which  ornament  the  resting  spore. 

P.  appendicvlata  (De  Wild.)  v.  Minden  and  P.  ellipticd  (Schroter)  v. 
Minden  occur  in  Mesocarpus.  The  companion  cell  of  the  first  is  vermiform, 
that  of  the  latter  globose. 


v/- 


S^^miim^^j//i9M«mie^^M 


Fig.  1.3.^ — Ectrogella  haciUariacearum  Zopf  in  the  diatom  Pinnularia.  (a) 
Young  ellipsoidal  thallus.  (6)  Germinating  swarmsporangium  provided  with 
four  exit  tubes.      (.After  Zopf  1884.) 

In  this  genus,  as  in  Olpidiopsis  and  other  genera  of  the  Chytri- 
diales  in  which  sexuality  occurs,  the  resting  spore  has  received 
various  names  (e.g.,  resting  sporangium,  oospore,  oosporangium), 
but  it  should  be  noted  that  the  wall  of  the  mature  spore  is  merely 
the  thickened  or  modified  membrane  of  the  female  gametangium. 
An  oospore  lying  free  in  the  oogonium,  as  in  the  Ancyhstalcs 
and  Oomycetes,  is  never  formed. 

5.  Ectrogella  Zopf  (1884:  175). 

Erected  on  E.  haciUariacearum  Zopf,  parasitic  in  diatoms  and 
first  observed  by  Zopf  near  Berlin.     It  also  occurs  in  America 


78  THE  LOWER  FUNGI— PHYCOMYCETES 

(Atkinson  1909  a :  338) .  The  swarmsporangia  are  usually  slender 
and  vermiform,  and  put  out  as  many  as  ten  short  exit  tubes 
arranged  in  one  or  two  definite  rows  (Fig.  13,  6.).  Resting 
spores  are  unknown.  Another  species,  E.  perforans  Petersen 
(1905:  466),  is  described  from  Denmark  in  Licniophora  and 
Synedra,  and  several  other  species  on  the  same  or  related  hosts 
have  been  described  by  Scherffel  (1925:  10). 

6.  Pleotrachelus  Zopf  (1884:  173). 

This  genus  was  founded  on  a  single  species,  P.  fulgens  Zopf, 
occurring  in  Pilobolus.  In  parasitized  host  plants  sporangia, 
normally    present,    are    suppressed    and    only    zygospores    are 


Fig.  \A.— Pleotrachelus  fulgens  Zopf  in  Piloholus.      {After  Zopf  I884.) 

developed.  The  sporangia  of  the  parasite  are  globose  and 
resemble  those  of  Olpidium  but  differ  in  emitting  a  number  of 
long  slender  exit  tubes  which  protruiie  in  many  directions 
(Fig.  14).  About  ten  other  species  have  been  described  from 
algae  and  roots  of  higher  plants  {Saccardo,  Sylloge  Fungorum, 
21:  24). 

7.  Pleolpidium  Fischer  (1892:  43). 

The  members  of  this  genus  occur  as  parasites  in  the  hyphac 
or  sporangia  of  various  relatively  rare  water  moulds.  The  out- 
standing character  of  the  genus  is  indicated  in  the  derivation 
of  the  name  Pleolpidium  (pleos:  filled,  and  Olpidium),  which 
refers  to  the  tendency  of  the  parasite  to  fill  the  host  cell.  In 
those  species  which  occur  in  the  sporangium  of  the  host  the 
thallus  enlarges  until  it  completely  fills  the  sporangium,  the  wall 


CHYTRIDIALES 


79 


Fig.  15. — Pleolpidium 
monohlepharidis  (Cornu) 
Fischer  in  fusiform  en- 
largements of  hyphae  of 


of  the  parasite  being  so  tightly  appressed  to  that  of  the  host 
that  no  line  of  separation  between  the  two  is  visible.  Conse- 
quently, a  parasitized  host  sporangium  may  be  easily  mistaken 
for  a  normal  one.  The  species  occurring  in 
the  hyphae  of  the  host  stimulate  the  for- 
mation of  pronounced  fusiform  or  ellipsoi- 
dal enlargements,  and  the  thallus  at  matur- 
ity completely  fills  the  lumen  of  the  hypha 
at  the  point  of  its  enlargement.  The  thal- 
lus then  functions  as  a  swarmsporangium. 
It  is  thin-walled,  smooth  and  hyaline,  and 
forms  one  or  more  inconspicuous,  short  exit 
tubes  indefinite  in  position.  Other  thalU 
develop  into  resting  spores.  These  lie  free 
in  the  host  cell  as  brownish  spheres,  and 
have  a  thick,  finely  echinulate  wall.  In  its 
relation  to  the  host  cell  the  thallus  resem-  ,,    ,     .     ,  ^  t,,   , 

Monoblephans.    (a)  inal- 

bles  that  of  Rozella  of  the  Woronmaceae  lus  of  parasite.    (6)  Rest- 
but   in  that  genus  fragmentation  of   the  ing    spore  of    parasite. 

,       .        1       p  .  •  (After  Cornu  1872.) 

thallus  at  maturity  results  m  the  formation 

of  a  sorus  of  sporangia,  while  the  swarmspores  are  biciliate.     The 

following  species  are  the  best  known. 

P.  araiosporae  (Cornu)  v.  Minden — 'in  sporangia  of  Araiospora. 

P.  apodyae  (Cornu)  Fischer — -in  sporangia  of  Apodachlya. 

P.  blastocladiae  v.  Minden— in  sporangia  of  Blastocladia. 

P.  monoblepharidis  (Cornu)  Fischer  (Fig.  15)— in  hyphae  of  Monoblepharis. 

P.  cuculus  Butler — -in  sporangia  of  Pijthium. 

8.  Plasmophagus  De  Wildeman,  {Ann.  Soc.  Beige  Micros., 
19:219,  1895). 
A  single  species,  P.  oedogoniorum  DeWild.,  in  the  vegetative 
cells  of  Oedogonium,  comprises  this  genus.  Resting  spores  have 
not  been  observed.  The  thallus  tends  to  fill  the  host  cell  as  in 
the  preceding  genus,  but  the  two  walls  remain  distinct.  The 
thallus  enlarges  as  the  host  thread  develops,  and  failure  of  the 
latter  to  form  the  usual  cross  walls  may  result  in  a  long  cell  fiUed 
by  the  parasite.  Sometimes  several  thalH  occur  in  the  same  host 
cell.  The  thallus  at  maturity  functions  as  a  sporangium,  and 
uniciliate  swarmspores  escape  through  a  short  inconspicuous 
papilla.  The  sporangial  wall  is  assumed  relatively  late,  the 
naked  protoplast,  in  early  stages,  being  indistinguishable  from 
that  of  the  host. 


80  THE  LOWER  FUNGI— PHYCOMYCETES 

Synchytriaceae 

Mycelium  wholly  lacking;  thallus  intramatrical,  provided  from 
an  early  period  with  a  membrane,  at  maturity  either  functioning 
in  its  entirety  as  a  resting  sporangium,  or  divided  by  cleavage 
planes  to  form  a  sorus  of  sporangia  enclosed  in  a  common  soral 
membrane;  zoospores  uniciliate;  cilium  at  the  posterior  end  of 
the  spore. 

Key  to  Genera  of  Synchytriaceae 

I.   Resting  spore  relatively  large;  parasites  in  higher  plants. 

1.  Synchytrium,  p.  80 
II.  Resting  spore  very  small;  parasites  in  algae. 

2.  Micromyces,  p.  87 

I.  Synchytrium  de  Bary  &  Woronin  (1863:  22). 

Probably  no  other  genus  of  the  Chytridiales  is  as  widely  known 
as  Synchytrium.  It  is  cosmopolitan  in  range,  and  several  of  its 
members  are  of  considerable  economic  importance.  The  species 
are  all  parasitic  in  higher  plants  and  cause  noticeable  galls. 

The  most  extensive  and  satisfactory  taxonomic  treatment  is 
that  of  Tobler  (1913),  but  the  monographs  of  Fischer  (1892:  45) 
and  von  Minden  (1911:  287)  will  also  be  found  useful.  Much 
work  remains  to  be  done  before  we  will  have  a  satisfactory 
knowledge  of  specific  limits. 

The  genus  may  be  split  into  four  apparently  natural  groups  of 
species,  and  these  are  treated  here  as  subgenera. 

I.  Resting  spores  unknown;  mature  thallus  functioning  as  a  summer  sorus 
of  thin-walled  sporangia;  sporangia  delimited  within  the  thallus  wall 
and  freed  by  its  rupture. 

subgenus  Woroninella 

II.  Resting  spores  known. 

A.  Life  cycle  embracing  summer  sori  and  the  resting  spore;  the  latter 

in  germination  functioning  as  a  single  sporangium  and  freeing 
swarmspores  directly  without  the  extrusion  of  a  vesicle. 

1.  The  sporangia  of  the  summer  sorus  delimited  within  the 

thallus  wall  and  freed  by  its  rupture. 

subgenus  Eusynchytrium 

2.  The  thallus  functioning  as  a  prosorus  and  extniding  a  thin- 

walled  vesicle  into  which  the  protoplast  flows  antl  in  which 
the  sporangia  are  then  delimited. 

subgenus  Mesochytrium 

B.  Summer  sori  not  formed;  resting  spore  in  germination  functioning 

as  a  prosorus,  and  extruding  the  endospore  as  a  thin-walled 
vesicle  in  which  the  sporangia  are  then  delimited. 

subgenus  Pycnochytrium 


CHYTRI  1)1  ALES 


81 


We  are  ignorant  of  the  life  cycles  of  a  considerable  number 
of  species  but  apparently  the  majority  belong  to  Pijcnochyirium. 
De  Bary  gave  this  group  generic  rank  and  Schroter  (1892:  73) 
follows  the  same  procedure.  In  the  present  incomplete  state  of 
knowledge  it  would  seem  that  nothing  is  to  be  gained  by  removing 
any  of  the  forms  from  Synchytrium.  Considerable  doubt  exists 
as  to  just  how  much  importance  is  to  be  attached  to  the  differ- 
ences in  sporangial  formation  which  constitute  the  basis  for  the 
above  key  to  subgenera.  If  the  extrusion  of  the  thin-walled 
vesicle  should  prove  to  be  inconstant  in  some  species,  as  has  been 
shown  to  be  the  case  in  Phytophthora,  the  above  separation  could 
not  be  maintained.  In  any  case,  the  genus  as  it  stands  consti- 
tutes a  coherent  whole. 


Fig.  16.- — Synchytrium  taraxaci  de  Bary  &  Woronin  on  Taraxacum,  (a) 
Sorus  of  swarnisporangia.  (6)  Single  swarmsporangium,  more  enlarged, 
germinating.      {After  de  Bary  and  Woronin  1865.) 

As  representative  of  the  subgenus  Eusynchytrium  the  species, 
S.  taraxaci  de  Bary  &  Woronin  (1863:  22),  occurring  in  Europe, 
Australia,  and  North  America  on  Taraxacum,  may  be  discussed 
(Fig.  16).  In  it  several  generations  of  swarmspores  are  formed 
during  the  summer,  and  only  the  last  develop  into  resting  spores. 
The  earlier  generations  form  summer  sori  of  sporangia.  The 
sorus  is  enclosed  in  a  definite  membrane,  and  at  maturity  con- 
tains fifteen  to  twenty  sporangia.  Though  there  is  usually 
only  one  sorus  in  a  single  host  cell  there  may  be  several.  The 
sporangia  are  very  unequal  in  size,  are  irregularly  polyhedral 
from  mutual  pressure,  and  when  fully  formed  have  a  thick 
hyaline  wall  and  reddish  orange  contents.  The  swarmspores 
are  freed  on  the  living  host  and  reinfect  it.  Each  swarmspore 
is  globose,  uniciliate,  and  contains  one  or  more  reddish  oil 
globules.  The  resting  spore  formed  at  the  close  of  the  season 
lies  free  in  the  host  cell,  is  globose,  and  at  maturity  is  provided 


82  THE  LOWER  FUNGI— PHYCOMYCETES 

with  a  thick  brown  exospore  and  a  thin  hyahne  endospore. 
Germination  occurs  in  the  spring,  both  walls  rupturing  without 
the  extrusion  of  the  endospore,  and  numerous  swarmspores 
being  freed  directly.  If  sexuality  is  concerned  in  resting  spore 
formation  it  has  never  been  demonstrated.  Another  well  known 
species  belonging  to  the  subgenus  Eusynchytrium  is  >S.  fulgens 
Schroter  occurring  on  Oenothera. 

The  best  known  member  of  the  subgenus  Mesochytrium  is  *S. 
endobioticum  (Schilbersky)  Percival,  cause  of  the  much  feared 
and  destructive  disease  of  potatoes  known  as  black  wart  (Fig.  17) 
introduced  into  the  United  States  from  Europe  (Orton   1919; 


Fig.   17. — Synchytrium  endobioticum  (Schilb.)   Percival,   cause  of  "black  wart" 
disease  of  potatoes.      {Photograph  by  McCuhbin.) 

Hartman  and  McCubbin  1924).  This  species  was  made  the  basis 
of  a  new  genus  by  its  discoverer  Schilbersky,  being  named  by  him 
Chrysophlyctis  endobiotica  Schilb.  The  genus  was  included  by 
von  Minden  (1911 :  228)  in  the  Olpidiaceae  where  it  was  separated 
from  the  other  genera  of  the  family  by  the  strikingly  angular 
form  of  the  resting  spore.  The  position  of  the  species  in  classi- 
fication was  for  a  time  in  controversy,  but  its  inclusion  by  Percival 
in  Synchytrium  has  been  justified  by  the  results  of  more  recent 
research.  The  genus  Chrysophlyctis  therefore  disappears.  The 
following  discussion  of  the  morphology  and  life  history  of  the 
species  is  based  largely  on  the  account  of  Curtis  (1921:  409). 
Her  paper  is  of  unusual  interest  in  that  she  shows  that  the  resting 
spore  in  this  species  results  from  a  sexual  fusion  of  motile  isoga- 


CHYTRIDIALES 


83 


Fig.  18.^ — Synchytrium  endohioticum  (Schilb.)  Percival.  (a)  Uninucleate 
thallus.  (6)  Thallus  functioning  as  a  prosorus;  its  contents  streaming  out  into  a 
thin-walled  vesicle,  the  sorus.  (c)  Uninucleate  sorus.  {d)  Sorus  plurinucleate 
by  division  of  primary  nucleus,  (e)  Cleavage  planes  have  divided  the  sorus 
into  sporangia  and  repeated  nuclear  division  has  occurred.  (/)  Mature  sporan- 
gium; papilla  of  dehiscence  forming,  {g)  Three  mature  sporangia  in  a  common 
soral  membrane;  swarmspores  escaping;  the  old  prosoral  envelope  flattened 
against  the  host  wall,  (k)  Two  gametes  in  contact,  (m)  Binucleate  zygote 
following  fusion,  (n)  Zoospores  encysted  on  host  wall;  the  cilia  have  dis- 
appeared and  nuclear  fusion  has  occurred,  ip)  Infection  by  zygote,  (s) 
Young  resting  sporangium,  {t)  Epidermal  region  of  gall  containing  resting 
spores  (resting  sporangia)  near  maturity.      {After  Curtis  1921.) 


84  THE  LOWER  FUNGI—PHYCOMYCETES 

metes  (Fig.  18,  k,  m).  In  the  accounts  of  early  workers  on  the 
Synchytriaceae  so  many  references  to  the  observation  of  giant 
bicihate  swarmspores  occur  that  a  sexual  fusion  of  ciliate  cells 
has  long  been  suspected.  The  demonstration  of  its  occurrence 
in  this  species  makes  logical  the  assumption  that  the  resting 
spores  of  other  species  are  also  truly  sexual  in  nature.  In 
this  connection  the  discussion  of  planogamic  copulation  given 
above  (p.  81)  should  be  read.  In  this  species,  as  in  S.  taraxaci 
discussed  above,  both  summer  sori  and  resting  spores  are  formed. 
The  resting  spore  in  germination  produces  swarmspores  directly. 
These  infect  the  host  and  produce  thalli  which  at  maturity  func- 
tion as  prosori.  The  prosorus  is  provided  with  a  thick  orange 
exospore  and  a  thin  hyaline  endospore.  At  first  it  is  uninucleate 
(Fig.  18,  a-c).  The  cytoplasm  and  nucleus  pass  out  into  a  vesicle 
consisting  of  the  extruded  endospore,  and  in  this  vesicle  nuclear 
division  occurs,  approximately  a  dozen  nuclei  being  formed 
before  the  sporangia  are  delimited.  The  sporangial  walls  are 
formed  simultaneously  and  independent  of  the  nuclei,  about 
four  to  nine  sporangia  composing  the  sorus.  The  extrusion  of  the 
endospore  occurs  while  the  fungus  still  lies  in  the  host  cell,  and 
the  exospore  may  be  flattened  out  at  one  side  by  the  pressure 
exerted  by  the  protoplast,  and  at  maturity  be  relatively  incon- 
spicuous. Nuclear  divisions  continue  in  the  sporangia  until  two 
hundred  to  three  hundred  nuclei  are  formed  in  each.  The 
enlarging  sporangia  exert  sufficient  pressure  to  finally  rupture  the 
soral  membrane  and  the  wall  of  the  host  cell,  and  are  thus  set  free. 
Then  one  or  two  hyaline  papillae  are  formed  on  each  sporangium, 
and,  at  the  rupture  of  one  of  these,  numerous  uninucleate  motile 
cells  escape.  Some  of  these  motile  cells  function  as  swarmspores 
and  after  infecting  the  host  develop  into  other  prosori.  Some 
of  them  function  as  gametes  and  fuse  in  pairs,  the  resulting 
zygote  penetrating  into  the  host  and  developing  there  into  a 
resting  sporangium.  It  is  probable  that  the  two  gametes  which 
fuse  originate  in  different  sporangia,  though  the  point  is  difficult 
to  demonstrate.  Their  nuclei  fuse  in  the  zygote  before  infection 
occurs.  The  mature  resting  spore  swells  by  the  imbibition  of 
water  and  bursts,  freeing  swarmspores  directly.  Other  species 
belonging  in  the  subgenus  Mesochytrium  are  S.  succisiae  de  Bary 
&  Woronin  on  Succisa,  S.  cellulare  Davis  (1924:  287)  on 
Lycopus,  and  S.  stellariae  Fuckel  on  Stellaria.  In  the  subgenera 
Eusynchytrium  and  Mesochytrium  few  data  are  available  concern- 


CHYTRIDIALES  85 

ing  the  germination  of  the  resting  spore.  Though  it  is  assumed 
that  it  frees  swarmspores  directly  in  all  the  species,  it  may  yet 
be  shown  to  function  in  some  as  a  prosorus  as  in  Pycnochytrium. 
The  species  of  Pycnochytrium  may  be  separated  into  two 
groups,  those  in  which  the  contents  of  the  resting  spore  are 
colored  (Chrysochytrium)  and  those  in  which  they  are  hyaline 
{Leucochijtrium) .  Eight  or  nine  species  may  be  placed  in  each 
group  with  certainty,  and  there  are  many  other  doubtful  forms. 
Throughout  the  subgenus  the  resting  spore  functions  in  all  known 
cases  as  a  prosorus,  the  sporangia  being  formed  in  an  extruded 
vesicle.  Summer  sori  are  not  formed  in  any  case.  Perhaps 
the  best  known  species  of  the  subgenus  is  S.  aureum  Schroter. 
While  most  species  are  limited  to  a  few  hosts  this  one  occurs  on  no 
fewer  than  one  hundred  and  thirty  plants  representing  such  widely 
separated  genera  as  Viola,  Ulmus,  Trifolium,  Solidago,  and 
Mentha.  None  of  the  species  of  Pycnochytrium  is  of  any  great 
economic  importance.     The  following  occur  in  North  America: 

S.  aureum  Schroter — on  many  hosts. 

S.  myosotidis  Kiihn — on  Lithospermurn. 

S.  anemnnes  (DC.)  Woronin — on  Anemone. 

S.  anomalum  Schroter — on  Adoxa. 

S.  holwayi  Farlow — on  Monarda. 

S.  mercurialis  (Libert)  Fuckel — on  Oenothera 

S.  cinnamomeum  Davis — on  Ranunculus. 

The  three  subgenera  Eusynchytrium,  Mesochytrium,  and 
Pycnochytrium  constitute  the  genus  in  the  older  treatments.  To 
these  Gaumann  (1927:  169)  has  recently  added  the  fourth, 
Woroninella. 

Raciborski  (1898)  erected  the  genus  Woroninella  Rac.  on  a 
single  species,  W.  psophocarpi  Rac,  occurring  in  Java  on  Pso- 
phocarpus  tetragonolohus  DC.  He  states  that  it  differs  from 
Syyichytrium  in  the  possession  of  biciliate  swarmspores.  He 
regarded  it  as  intermediate  between  Woronina  and  Synchytrium. 
Later  he  (Raciborski  1900:  7)  added  another  species,  W.  vulcanica 
Rac,  found  on  Lespedeza.  Both  of  these  fungi  cause  galls  on 
their  hosts,  and  in  general  resemble  species  of  Synchytrium. 
Sydow  (1914)  then  transferred  to  Woroninella  five  species 
previously  incorporated  m.  Synchytrium  by  other  authors  including 
S.  aecidioides  (Peck)  Lag.  and  S.  puerariae  (Hennings)  Miyabe. 
The  group  of  forms  thus  brought  together  resemble  one  another 
in  the  absence  of  a  thick-walled  resting  spore  and  in  the  powdery 


86  THE  LOWER  FUNGI— PHYCOMYCETES 

aspect  of  the  open  sorus  of  swarmsporangia.  This  latter  charac- 
teristic led  earlier  investigators  to  mistake  these  fungi  for  rusts. 
In  fact  several  species  were  first  described  in  Aecidium  and 
Uredo. 

The  common  North  American  representative  of  the  genus, 
W.  aecidioidcs  (Peck)  Sydow,  was  first  described  by  Peck  in  the 
genus  Uredo.  It  was  later  placed  in  Synchytrium  by  Farlow,  and 
will  be  most  frequently  encountered  in  the  literature  under  the 
name  S.  decipiens  Farlow.  The  species  occurs  in  America  on  the 
hog  peanut,  Amphicarpa  monoica  and  A.  pitcheri,  and  in  Oriental 
India  and  Japan  on  A.  edgeworthii.  It  is  probably  the  best  known 
representative  of  the  Chytridiales  in  the  United  States.  It  has 
been  studied  cytologically  by  Harper  (1899),  Stevens  (1903; 
1907),  and  Griggs  (1908;  1909  a,  b,  c).  The  infecting  swarm- 
spore  is  uninucleate,  and  the  uninucleate  condition  is  main- 
tained in  the  developing  thallus  until  it  approaches  maturity. 
This  nucleus,  termed  the  primary  nucleus,  enlarges  rapidly  as  the 
thallus  grows,  and  finally  attains  an  extraordinary  size.  It  then 
divides  to  form  nuclei  for  the  sporangia,  and  these  in  turn,  after 
the  sporangial  walls  are  initiated,  divide  to  provide  nuclei  for  the 
swarmspores.  The  species  forms  galls  on  the  leaves,  stems, 
and  other  aerial  portions  of  the  host,  and  may  sometimes  be 
found  even  on  the  fleshy  subterranean  pods  of  the  lower  flowers. 
The  species  is  clearly  very  closely  related  to  W.  puerariae  (Henn- 
ings)  Sydow  occurring  in  the  Far  East  on  Pueraria. 

Kusano  (1909:  86, 112)  studied  the  latter  species  very  critically, 
and  found  the  swarmspores  to  be  uniciliate.  He,  consequently, 
followed  the  nomenclature  of  Miyabe  (1905:  199)  who  had  first 
placed  the  species  in  Synchytrium.  Later  Ito  and  Homma 
(1926)  confirmed  this  finding,  and  demonstrated  that  the  swarm- 
spores are  uniciliate  in  W.  aecidioides  also.  Since  these  two 
species  fail  to  show  the  swarmspore  character  described  for 
Woroninella,  and  since  the  open  powdery  nature  of  the  sorus  is 
not  typical  of  Synchytrium  they  erected  a  new  genus  Miyabella 
Ito  and  Homma  for  them. 

The  following  year  Gaumann  (1927)  examined  the  type  species 
of  Woroninella,  W.  psophocarpi,  and  proved  that  in  it  also  the 
swarmspores  are  uniciliate.  There  is  no  longer,  therefore,  any 
reason  for  retaining  the  genus  Woroninella.  Nevertheless,  since 
the  group  of  species  here  treated  differ  from  the  other  known 
species  of  Synchytrium  in  the  strikingly  powdery  aspect  of  their 


CHYTRIDIALES 


87 


open  aecidium-like  sori  and  in  the  absence  of  the  resting  spore 
stage  it  would  seem  that  Gaumann's  erection  of  the  subgenus 
Woroninella  was  warranted.  It  is  possible  that  further  study- 
will  make  desirable  merging  the  group  with  Eusynchytrium. 

North  American  species  of  Synchytrium  not  listed  above 
because  of  their  uncertain  position  in  the  genus  include  the 
following. 

S.  asari  Arthur  &  Holway — on  Asarum. 

S.  caricis  Tracy  &  Earle — on  Carex. 

S.  innoviinntum  Farlow — on  Malacothrix. 

S.  nigrescens  Davis — on  Aster. 

S.  scirpi  Davis — on  Scirpus. 

S.  vaccinii  Thomas — on  Vaccinium,  Kalmia,  Cassandra,  etc. 


Fig.    19. 


Micromyces    zygoyoni    Daiigourd    in    Zygogonium.      {After    Dangeard 
1889.) 


2.  Micromyces  Dangeard  {Le  Botaniste,  1:55,  1889). 

A  small  and  imperfectly  understood  genus  included  here  as 
a  doubtful  member  of  the  family.  The  genus  was  based  by 
Dangeard  on  a  single  species,  M.  zygogoni  Dang.  (Fig.  19),  found 
in  France  in  the  cells  of  the  alga  Zygogonium.  Subsequently 
several  other  species  have  been  described  from  other  algae. 
These  include  M.  mesocarpi  DeWildeman  in  Mesocarpus  in 
Belgium,  M.  spirogyrae  Skvortzow  in  Spirogyra  in  China,  and 
M.  petersenii  in  Mougeotia  in  Czechoslovakia. 

The  mature  thallus  is  a  small  sphere.  It  becomes  invested 
in  a  coarsely  spiny  membrane,  and  functions  as  a  resting  spore. 
In  germination  it  either  frees  zoospores  directly,  or,  as  in  the 
subgenus  Pycnochytrium  of  Synchytrium,  its  contents  pass  into 
a  thin-walled  vesicle  and  there  form  a  small  sorus  of  sporangia 
which  in  turn  form  zoospores. 


88  THE  LOWER  FUNGI— PHYCOMYCETES 

The  genus  Micromycopsis  Scherffel  (1926:  167)  based  on  M. 
cristata  Scherffel  in  Hyalotheca  and  M.  fischerii  Scherffel  in 
Zygogonium  should  be  considered  in  this  connection. 

Rhizidiaceae 

Although  this  family  contains  a  larger  number  of  genera  than 
any  other  in  the  order  it  is  probably  the  least  well  known.  The 
forms  are  chiefly  transient  in  character,  and  are  with  difficulty 
kept  under  observation  long  enough  for  the  completion  of 
satisfactory  studies.  The  members  of  the  group  vary  greatly 
in  morphology,  and  present  many  interesting  features  whose 
further  elucidation  will  tend  to  shed  light  on  the  general  problem 
of  phylogeny  in  the  order  (see  key,  p.  48). 

In  the  following  key  the  essential  characters  of  the  genera 
are  indicated,  and  to  avoid  unnecessary  repetition  these  are 
omitted  in  the  text.  For  a  more  detailed  taxonomic  treatment 
the  student  should  consult  von  Minden  (1911)  or  Fischer  (1892). 
It  is  highly  probable  that  many  as  yet  undescribed  species  exist 
in  nature. 

Key  to  Genera  of  Rhizidiaceae 

I.   Mycelium  wliolly  intramatrical. 
A.  Sporangia  epibiotic. 

1.   Mycelium   consisting   of   delicate,    more   or   less   branching 
threads. 
a.  Resting  spores  when  present  epibiotic. 

(1)  Mycelium    usually    monophagus;    resting    spore 
germinating  by  svvarmspores. 
(o)  Sporangium  lacking  a  subsporangial  vesicle. 

1.  Rhizophidium,  p.  91 

(6)  Sporangium  provided  with  a  subsporangial 
vesicle. 

1'.  Sporangium    with    an    extramatrical 
stalk. 

a'.  Sporangium  with  a  solid  apical 
spine;  the  stalk  in  open  con- 
nection with  the  sporangium; 
saprophytes. 

2.  Obelidium,  p.  92 

h'.  Sporangium  lacking  the  apical 
spine,  separated  by  a  septum 
from  the  stalk;  parasites. 

3.  Podochytrium,  p.  92 


CHYTRIDIALES  89 

2'.  Sporangium  lacking  an  oxtramatrical 
stalk. 

a'.  Swarmsporcs  freed  through  an 
apical  opening. 
1".  Sporangium  opening  by  a 
large  lid;   resting  spore 
formed    bj'    a    definite 
sexual  process  in  which 
a  male  individual  sends 
a  fertilization  tube  into 
a  female  individual. 
4.  Zygorhizidium,  p.  93 
2".  Sporangium  not  opening 
by  a  lid. 

a".  Contents  of  spor- 
angium escaping 
into  a  thin-walled 
vesicle  in  which 
the  swarmspores 
are  then  formed. 
6.  Rhizidiomyces,  p.  93 

b".  Swarmspores     for- 
med      in       the 
sporangium. 
1'".  Swarm- 
spores 
encysting 
at        the 
mouth  of 
the   spor- 
a  n  g  i  u  m 
as  in 

Achlya. 

6.  Achlyella,  p.  94 

2'".  Swarm- 
spores  es- 
c  aping 
without 
encyst- 
ment. 

7.  Phlyctochytrium,  p.  94 
b'.  Swarmspores    freed    through    a 

basal  or  subbasal  opening. 
1".  Sporangial  wall  spiny. 

8.  Asterophlyctis,  p.  94 
2".  Sporangial  wall  smooth. 

a".  Mycelial  threads 
drawn  out  to 
extremely  slen- 
der tips. 

9.  Rhizoclosmatium,  p.  94 


90  THE  LOWER  FUNGI— PHYCOMYCETES 

h".  Mycelial  threads 
more  definitely 
tubular. 

10.  Siphonaria,  p.  95 

(2)  Mycelium  often  wide-spreading,  saprophytic; 
resting  spore  in  germination  functioning  as  a 
prosporangium,  the  swarmspores  being  delim- 
ited in  the  extruded  endospore. 

11.  Rhizidium,  p.  96 

b.  Resting  spores  intramatrical. 

12.  Dangeardia,  p.  96 

2.   Mj'celium  not  consisting  of  delicate  threads. 

a.  Mycelium  consisting  of  a  delicate  stalk  flattened  at  its 

tip  to  form  a  small  disc  which  is  either  applied  to  or 
developed  in  the  host  wall;  sporangia  long,  fusiform, 
proliferating. 

13.  Harpochytrium,  p.  96 

b.  Mycelium  not  forming  such  a  disc. 

(1)  Re.sting  spore  endobiotic,  germinating  to  form  an 

epibiotic  sporangium;  mycelium  consisting  of  a 
short  broad  tube. 

14.  Chytridium,  p.  96 

(2)  Resting      spore      epibiotic,       germinating      by 

swarmspores. 

(a)  Contents  of  sporangium  escaping  into  a 
thin-walled  vesicle  in  which  the  swarm- 
spores are  then  formed;  mycelium  con- 
sisting of  a  lobed  or  slightly  divided 
haustorivnn. 

15.  Saccomyces,  p.  98 

(6)  Sporangium  not  extruding  a  vesicle;  myce- 
lium consisting  of  an  unbranched  fihform 
or  bladder-like  haustorium. 

16.  Phlyctidium,  p.  98 

B.   Sporangia  and  resting  spores  intramatrical,  developing  from  a 
swelling  formed  at  the  tip  of  the  germ  tube  of  the  swarmspore. 

1.  Sporangia  and  resting  spores  lacking  a  subsporangial  vesicle. 

Resting  spore  wall  smooth. 

17.  Entophlyctis,  p.  98 

2.  Subsporangial  vesicle  present;  resting  spore  wall  spiny. 

18.  Diplophlyctis,  p.  98 

II.  Only  the  tips  of  the  branches  of  the  mycelium  intramatrical,  entering 
several  host  cells  (polyphagus),  parasitic. 
A.  Individual  functioning  as  a  sporangium  or  resting  spore. 

1.  Swarmspores  freed  from  the  sporangium  through  a  definite 
opening. 

19.  Rhizophlyctis,  p.  99 


CHYTRIDIALES  91 

2.  Swarmspores  freed  l>y  disintegration  of  the  sporangial  wall 
and  remaining  together  for  a  time  as  a  rotating  sphere. 

20.  Nowakowskia,  p.  99 

B.  Individual  functioning  as  a  prosporangium,  its  contents  extruded 
into  a  thin-walled  vesicle  in  which  the  spores  are  formed.  Rest- 
ing spore  formed  as  a  result  of  the  copulation  of  two  individuals. 

1.  Sporangiospores  non-motile,  germinating  in  the  sporangium 

as  in  Aplanes. 

21.  Sporophlyctis,  p.  100 

2.  Sporangiospores  ciliated  and  escaping  before  germination 

22.  Polyphagus,  p.  100 

1.  Rhizophidium     Schenck     (tJber    Vorkommen     Kontraktiler 

Zellen  1858). 

A  large  genus  of  about  thirty  species  occurring  in  the  water 

on  algae,  lower  fungi,  lower  animals,  pollen  grains  (Fig.  20),  and 

similar  substrata.     A  key  to  most  of  the  known  species  is  given 


Fig.  20. — Rhizophidium  pollonis  (A.  Braun)  Zopf,  on  pollen  grains,  (a) 
Swarmsporangium  and  swarmspores.  (6)  Two  resting  spores  and  four  swarm- 
sporangia,  two  of  which  have  freed  their  spores.      {After  Zopf  1888.) 

by  von  Minden  (1911:  316).  Notes  of  particular  interest  to 
American  students  are  given  by  Atkinson  (1894;  1909  a),  Coker 
(1923:  186),  Martin  (1922),  Melhus  (1914  a),  and  Zeller  (1918). 
In  the  search  for  chytrids  in  algae,  members  of  this  genus  are 
more  often  encountered  than  other  forms,  R.  globosum  (Fig.  21) 
being  particularly  common. 

The  genus  Latrostium  Zopf  (1894),  erected  on  L.  comprimens 
Zopf  occurring  on  Vaucheria,  resembles  Rhizophidium  in  the 
form  of  the  swarmsporangium.  The  statement  that  the  cilium 
precedes  the  swarmspore  in  swimming  raises  a  question  as  to 
the  actual  relationships  of  the  form,  and  it  is  here  treated  as 
doubtful  (see  key,  p.  48). 


92 


THE  LOWER  FUNGI— PHYCOMYCETES 


2.  Obelidium  Nowakowski  (1876:  86). 

Erected  on  the  single  species,  0.  mucronatum  Nowak.,  occurring 
in  Europe  on  larvae  and  nymphs  lying  in  the  water  (Fig.  22). 


FiG.  21. — Rhizophidium  globosum  (A.  Braun)  Schrotcr.  A.  Young  plant 
developed  from  encysted  swarmspore,  the  penetration  tube  forming  rhizoids. 
B.  Mature  plant.  C.  Plant  funetifjning  as  a  swarmsporangium  and  freeing 
ewarmspores.     {After  Atkiiison  1909.) 


Via.  22. — Obdidiitm  mucronatum  Nowakowski.  SporMiitriiiiu  with  a  solid 
apical  spine;  swarinspcjres  escajjing  through  a  suhapical  lateral  pore.  {After 
Nowakowski  1876.) 

3.  Podochytrium  Pfitzer  (Sitzungsber.  Nicder-rhein.  Ges.  Natur. 

und  Heilkunde.  pp.  62,  Bonn.  1870). 

Erected  on  the  single  species,  P.  davatum  Pfitzer,  occurring 

in  Pinnularia.     The  same  thing  was  described  and  well  figured  by 

Zopf  (1888)  under  the  name,  Septocarpus  corynephoriis  (Fig.  23). 


CHYTRIDIALES 


93 


4.  Zygorhizidium  Lowenthal  (Archiv  fur  Protistenkunde,  5 :  228, 
pi.  8,  1904). 
Erected  on  the  single  species,  Z.  willei  Lowenthal,  in  Cylin- 
drocystis  in  Norway. 


Fig.  23.- — Podochytrium  clavatum  Pfitzer  in  Pinnularia.  (a)  Young  plant. 
{b,  c)  Mature  plants  showing  subsporangial  extramatrical  stalk.  (After  Zopf 
1888.) 


Fig.  24. — Rhizidiomycrs  apophysatus  Zopf  in  oogonium  of  Achlya.     A.  sporangia. 
B.  stages  in  swarmspore  formation.      {After  Zopf  1884-) 

5.  Rhizidiomyces  Zopf  (1884:  188). 

Two  species,  K.  apophysatus  Zopf  (Fig.  24),  in  the  oogonia  of 
Achlya  and  Saprolegnia,  originally  described  from  Europe  and 


94 


THE  LOWER  FUNGI— PHYCOMYCETES 


reported  by  Coker  (1923:  186)  from  North  America,  and  R. 
ichneumon  Gobi  in  Chloromonas. 

6.  Achlyella  Lagerheim  {Hedw.  29:  143,  1890). 

Erected  on  the  single  species,  A.  flahaultii  Lag.,  found  in 
pollen  grains  of  Typha  in  water. 

7.  Phlyctochytrium  Schroter  (1892:  78). 

A   relatively   large   genus   containing   over   a   dozen   species 
occurring  chiefly  as  parasites  in  algae.     Except  in  the  possession 


A\  d 


Fig.  25. — Rhizidium  mycophUum  A.  Braun  in  slime  of  Chaetophora.  (a) 
Branching  thallus  bearing  a  sporangium,  {h)  Sporangia  freeing  swarmspores. 
(c)  Smooth-walled  resting  sporangium  functioning  as  a  prosporangium.  {d) 
Hairy  resting  sporangium,  (e)  Same  functioning  as  a  prosporangium.  {After 
Nowakowski  1877.) 

of  a  subsporangial  vesicle  the  genus  corresponds  to  Rhizophidium. 
Resting  spores  are  unknown.  Two  species,  P.  planicorne  Atk. 
and  P.  equale  Atk.,  have  been  found  in  North  America  (Atkinson 
1909  a)  on  Spirogyra. 

8.  Asterophlyctis  Petersen  (Jour,  de  Botanique,  17:  218,  1903). 
Erected  on  a  single  species,  A.  sarcoptoides  Petersen,  sapro- 
phytic in  empty  nymph  cases  lying  in  water. 

9.  Rhizochlosmatium  Petersen  {Jour,  de  Botanique,  17  :  216, 1903). 
Erected  on  a  single  species,  R.  globosum  Petersen,  saprophytic 

in  empty  nymph  cases  lying  in  water. 


CHYTRIDIALES 


95 


Fig.  26. — Harpochytrium  hedenii  Wille  on  Spirogyra  and  Zygnema  {a-c) 
Young  thalli  developed  from  swarmspores.  (d)  Mature  plant,  (e)  Zoospores 
escaping  in  amoeboid  state;  secondary  sporangium  forming  below  primary. 
(J,  g)  Uniciliate  swarmspores  escaping;  proliferation  of  sporangia,  {h)  One 
individual    of    Harpochytrium    attacked    by    another.      (After    Atkinson    1903.) 


10.  Siphonaria  Petersen  (Jour,  de  Botanique,  17:  220,  1903). 

Erected  on  a  single  species,  *S.  variabilis  Petersen  saprophytic 
in  empty  nymph  cases  lying  in  water. 


96 


THE  LOWER  FUNGI— PHYCOMYCETES 


11.  Rhizidium  A.  Braun  (Monatsbcr.  Berl.  Akad.,  p.  591,  1856). 
Several  species  described  from  pAirope  include,  R.  mycophilum 

A.  Braun  (Fig.  25),  in  slime  of  Chaetophora,  R.  lignicola  Lindau, 
saprophytic  on  wood  in  water,  and  R.  operculatum  (De  Wildeman) 
von  Minden,  probably  saprophytic,  on  submerged  surfaces  of 
aquatic  higher  plants. 

12.  Dangeardia  Schroder  (Bcr.  Deut.  Bot.  Gesell,  16:  314,  pi.  20, 

1898). 
Erected  on  a  single  species,  D.  mamillata  Schroder,  found  on 
Pandorma. 


Fig.  27. — Chytridium  olla  Braun.  («)  Mature  swarmsporangia  attached  to 
oospore  of  Oedogonium.  {h)  Swarmsporangium  enlarged,  (c)  Resting  spore, 
(d,  e)  Germinating  resting  spores,  (a,  b,  after  A.  Braun  1855;  c-e,  after  de  Bary 
1887.) 

13.  Harpochytrium  Lagerheim  (Hediv.,  29:  142,  1890). 

syn.  Fulminaria  Goh\,{Scripta  Hort.  Bot.  Petrop.,  15:  283, 
1899; 

Rhahdium  Dangeard  (Ann.  Mycol.,  1:  61,  1903). 
A  small  but  interesting  genus  embracing  two  or  three  species 
parasitic  on  algae  (Fig.  26).     These  are  thoroughly  discussed 
and  well  illustrated  by  Atkinson  (1903). 


14.  Chytridium  A.    Braun    (Erscheinungen   der  Verjungung.  p. 
198,  1850;  Berl.  Akad.  Abhandl.,  p.  23,    pi.  1,  1855). 
The  oldest  genus  of  the  order.     As  here  constituted  it  contains 
the  type  species,  C.  olla  Braun  (Fig.  27)  and  about  six  others  of 
similar  character,  all  occurring  in  algae. 


CHYTRIDIALES 


97 


Fig.  28. — Phlydidium  brevipes  (Atk.)  v.  Minden.  A.  Mature  swarnisporan- 
gium  crowded  with  swarmspores;  inner  layer  of  sporangial  wall  protruding  as  a 
papilla;  rhizoids  lacking.  B.  Swarmspores  escaping.  C,  D.  A  few  swarms- 
pores germinating  in  the  sporangium  after  failing  to  locate  the  exit  pore.  {After 
Atkinson  1900.) 


Fig.  29. —  (a,  h)  Entophlyctis  bulligcra  (Zopf)  Fischer,  (c,  d)  Ent.  confervae- 
Olomcratae  (Cienkowski)  Fischer,  (a)  Mature  plant  with  papilla  of  dehiscence 
consisting  of  the  membrane  of  the  infecting  swarmspore.  {b)  Young  plants 
developing  from  infecting  swarmspores.  (c)  Young  plant  with  rhizoids 
developed  from  swarmspore;  also  an  encysted  swarmspore  before  germination. 
id)   Resting  spore.      {After  Zopf  1884.) 


98 


THE  LOWER  FUNGI^PHYCOMYCETES 


15.  Saccomyces  Serbinow   (Scripta  Hort.  Bot.  Petrop.,  24:  162, 
1907). 

Erected  on  a  single  species,   S.   dangeardii  Serb.,   found  in 
Euglena  in  Russia.     See  also  Rhizosiphon  Scherffel  (1926:  167). 

16.  Phlyctidium  A.  Braun  (Monatsber.  d.  Akad.  d.  Wiss.  1855). 
The  genus  contains  several  species,  all  of  which  occur  in  algae. 

One  of  these  P.  brevipes  (Atk.)  v.  Minden  (Fig.  28)  was  first 


J'iG.  30.- — Diplophlyctis  intestina  (Schenk)  Schroter.  (a)  Infecting  swarm- 
Bporc.  (/))  Young  plant,  (c)  Older  plant  with  subsporangial  vesicle,  {d) 
Mature  plant  with  papilla  of  dehiscence,  (e)  Sporangium  freeing  swarmspores. 
(/)   Swarmspores.      (fif)   Resting  sporangium.      {After  Zopf  1884-) 


described  by  Atkinson  (1909  a)  from  North  America  on  Spirogyra 
as  Rhizophidium  brevipes  Atk.  Perhaps  Physorhizophidium 
Scherffel  (1926:  181)  belongs  here. 

17.  Entophlyctis  Fischer  (1892:  114). 

The  genus  contains  several  species  (Fig.  29),  all  of  which  occur 
in  algae.  A  critical  study  of  E.  heliomorpha  has  been  made  by 
Karling  (1928). 

18.  Diplophlyctis  Schroter  (1892:  78). 

Erected  on  D.  intestina  Schroter  (Fig.  30),  found  occurring  in 
dead  or  dying  cells  of  Cham  and  Nitella  (consult  Karling  1928: 
204). 


CHYTRIDIALES 


99 


19.  Rhizophlyctis  Fischer  (1892:  119). 

The  genus  contains  several  species,  all  of  which  occur  in  algae 
(Fig.  31). 


Fig.  31. — Rhizophlyctis  mastigotrichis  (Now.)  Fischer,  (a)  Mature  swarm- 
sporangium  with  rhizoids  attached  to  host  threads.  (6)  Same  with  swarm- 
spores,      (c)   Swarmspores.      (After  Nowakowski  1876.) 


®0® 


Fig.  32. — Nowakowskia  hormotheceae  Borzi  in  Hormotheca  sicula.  (a)  Plant 
sending  rhizoids  into  several  host  cells.  (6)  Mature  swarmsporangium.  (c) 
Swarmspores  in  naked  mass  after  disintegration  of  sporangial  wall,  (d)  Swarm- 
spore  mass  broken  into  smaller  colonies,  (c)  Germinating  swarmspores.  (After 
Borzi  1885.) 


20.  Nowakowskia  Borzi  {Bot.  Centralbl,  22:  23,  pi.  1,  1885). 

This  genus,  based  on  N.  hormothecae  Borzi  (Fig.  32)  on  Hormo- 
theca sicula  in  Sicily,  is  regarded  as  doubtful  by  Fischer  (1892: 
122).     It  is  essentially  the  same  as  Rhizophlyctis  except  in  the 


100  THE  LOWER  FUNGI— PHYCOMYCETES 

method  of  svvarinspore  discharge.  In  Nowakowskia  according 
to  Borzi  the  sporangial  wall  disintegrates  leaving  the  swarm- 
spores  in  a  spherical  Volvox-Vike  mass  which  retains  its  form  and 
rotates  for  a  time,  the  spores  finally  separating  from  one  another 
and  swimming  away. 

21.  Sporophlyctis  Serbinow   (Srripta  Bot.   Hort.   Univ.  Petrop., 
24:  116,  164,  1907). 

Erected  on  the  single  species,  *S.  rostrata  Serbinow,  found  on 
Draparnaldia  in  Russia.  It  has  been  collected  also  in  America 
(Graff,  1928:158). 

22.  Polyphagus  Nowakowski  (1876:  203). 

Erected  on  the  single  species,  P.  euglenae  Nowak.,  parasitic 
in  Euglena  and  Chlamydomonas.  The  fungus  is  thoroughly  dis- 
cussed by  Wager  (1913),  who  outlines  the  sexual  process  as 
follows.  Two  cells,  not  differing  morphologically  from  the 
vegetative  cells,  function  as  sex  cells.  The  male  cell,  which  is 
usually  somewhat  smaller  than  the  female,  puts  out  a  slender 
pseudopodium-like  process  which  comes  in  contact  with  the 
female  cell  and  fuses  with  it.  The  zygote  is  formed  in  the  tip 
of  this  tube,  the  contents  of  both  male  and  female  cells  passing 
into  it.  A  smooth  or  spiny  wall  is  then  formed  on  the  zygote, 
and  it  assumes  the  spherical  form  of  the  mature  resting  spore. 

Cladochytriaceae 

The  members  of  this  family  correspond  with  the  Rhizidiaceae 
in  the  possession  of  a  definite  mycelium,  but  here  it  is  wide- 
spreading  and  usually  bears  more  than  a  single  sporangium. 
Terminal  and  intercalary  enlargements,  formed  throughout  the 
mycelium,  are  transformed  wholly  or  in  part  into  sporangia  or 
resting  spores. 

Key  to  Genera  of  Cladochytriaceae 

I.  Sporangiospores  non-ciliate,  amoeboid. 

1.  Amoebochytrium,  p.  101 

II.  Sporangiospores  ciliate. 

A.  Sporangia  formed  from  enlargements  of  the  mycelium,  terminal  or 
intercalary;  resting  spores  rare  or  absent. 
1.  Sporangium  opening  by  a  lid,  proliferating. 

2.  Nowakowskiella,  p.  101 


CHYTKIDIALES  101 

2.  Sporangium  lacking  a  lid  and  not  proliforating 

fl.  Mycelium  of  rather  broad,  cylindrical  threads;  sporan- 
gia developed  from  fusiform  enlargements  of  the 
hyphae  and  separated  by  short  cylindri(;al  cells. 

3.  Catenaria,  p.  101 

h.  Mycelium  of  extremely  delicate  branching  strands, 
developing  globose  or  irregidar  enlargements  which 
sometimes  become  septate  into  several  cells;  sporan- 
gium developed  from  an  entire  eidargement  or  from 
one  of  its  cells;  resting  spores  unknown. 

4.  Cladochytrium,  p.  102 
B.  Sporangia  rarely  formed,  when  present  epibiotic  and  developing 

directly  from  the  swarmspore;  resting  spores  always  present  and 
abundant. 

1.  Resting  spore  globose  to  ellipsoidal,  usually  not  flattened  on 

one    side;    parasite    resulting   in    discoloration    or   slight 
thickening  of  the  affected  plant  parts. 

5.  Phy  so  derma,  p.  103 

2.  Resting  spore  globose,  but  usually  flattened  to  concave  on 

one  side;  considerable  deformation  of  affected  portions  of 
the  host  occurring. 

6.  Urophlyctis,  p.  107 

1.  Amoebochytrium  Zopf  (1884:  181). 

Erected  on  the  single  species,  A.  rliizidioides  Zopf,  found  in 
slime  of  Chaetophora  spp.,  but  not  in  the  cells,  apparently  known 
only  from  the  original  collection.  Sporangium  developed  either 
from  the  spore  or  from  an  enlargement  of  the  mycelium,  flask- 
shaped  with  a  long  neck,  described  as  freeing  amoeboid  non- 
ciliate  spores.  Resting  spores  unknown.  It  is  possible  that 
ciliate  spores  occur  under  certain  conditions  of  environment. 

2.  NowakowskieUa  Schroter  (1892:  82). 

Two  species  are  included,  N.  elegans  (Nowakowski)  Schroter 
(Fig.  33)  described  from  the  slime  of  Chaetophora  in  Germany, 
and  N.  ramosa  Butler  (1907:  137)  seen  in  decaying  wheat  culms 
in  India.  The  former  species  has  been  found  in  America  (Mat- 
thews, 1928). 

3.  Catenaria  Sorokin  {Ann.  Sci.  Nat.  6  ser.  hot.,  4:  67,  1876). 
The  genus  includes  the  type  species,  C.  anguillulae  (Fig.  34) 

found  in  nematode  and  trematode  worms,  rotifer  eggs,  cysts  of 
infusoria  and  Nitella,  and  C.  pygmaea  Serbinow  a  doubtful 
species  in  Moiigeotia.  The  most  recent  and  complete  discussion 
of  the  genus  is  that  of  Butler  {Ann.  Botany,  42:  813,  1928). 


102 


THE  LOWER  FUNGI—PHYCOMYCETES 


4.  Cladochytrium  Nowakowski  (in  Cohn,  Beitr.  Biol.  Pflanzen, 
2:  92,  1877). 
A  thorough  comparative  study  of  this  genus  and  the  two  follow- 
ing is  greatly  needed.     The  separation  used  here,  adapted  from  von 


Fig.  33. — NowahowskieUa  elegans  (Nowak.)  Schroter.  (a)  Terminal  sporan- 
gium on  branching  mycelium;  secondary  sporangium  formed  by  proliferation 
within  the  primary ;  lids  of  both  fallen  away.  (6)  Swarmsporangium  containing 
spores,  (c)  Swarmspores.  (d)  Amoeboid  zoospores.  {After  Nowakowski 
1876.) 

Minden  (1911 :  389),  is  clearly  inadequate,  but  can  not  be  replaced 
by  a  more  natural  grouping  until  much  additional  work  has  been 
done.  As  here  constituted  the  genus  Cladochytrium  contains 
relatively  few  species,  and  only  one  of  these,  the  type  species, 


CHYTRIDIALES 


103 


C.  tenue  Nowak.  (Fig,  35),  can  be  included  with  certainty.  This 
species  differs  from  those  of  Physoderma  and  Urophlyctis  in  its 
failure  to  form  resting  spores  and  in  forming  its  sporangia  from 
enlargements  of  the  mycelium.  It  has  been  found  in  Europe 
in  the  tissues  of  various  marsh  plants  (Acorns,  Iris,  etc.),  and  in 


Fig.  34. — Caienaria  anguillidac  Sorokin  (a)  Young  thallus  developed  from 
swarmspore.  (6)  Mature  thallus  with  swarmsporangia  and  delicate  terminal 
branches,      (c)    Swarmsporangium     freeing     swarmspores.      {After     Dangeard.) 

the  slime  which  often  covers  their  submerged  surfaces.  Other 
species  doubtfully  included  in  the  genus  are  C.  polystomum  Zopf, 
C  cornutum  De  Wildeman,  and  C.  irregulare  De  Wildeman. 

5.  Physoderma  Wallroth,  (Flora  Crypt.  Germ.,  2 :  192,  1833). 

In  this  genus  and  in  Urophlyctis  all  the  species  are  parasitic 
in  the  tissues  of  higher  plants.     Resting  spores  are  always  present 


Fig.  35. — Cladochytrium  tenue  Nowakowski,  showing  mycelium,  swarmsporan- 
gia, and  swarmspores.      {After  Nowakowski  1876.) 


and  abundant.  Sporangia  have  been  found  in  only  a  few  species, 
and  when  formed  are  epiphytic  and  develop  directly  from  the 
swarmspore  instead  of  from  the  mycelial  enlargements.  In  these 
cases  [P.  maculare  Wallr.,  P.  butomi  Schrot.,  U.  pidposa  (Wallr.) 
Schrot.],  the  mycelium  attached  to  the  sporangium  is  limited  in 
extent,  monophagus,  and  similar  in  appearance  to  that  of  Rhizo- 
phidium  of  the  preceding  family.     Other  swarmspores  infecting 


104  THE  LOWER  FUNGI— PHYCOMYCETES 

the  host  send  their  germ  tubes  into  the  interior  and  develop  a 
wide-spreading  mycehum  having  no  connection  with  the  sporangia. 
On  this  mycehum  definite  turbinate  enhirgements  are  formed 
(Fig.  37,  t),  which  at  maturity  become  septate,  and  from  one  of 
the  cells  of  each  enlargement  a  thick-walled  resting  spore  devel- 
ops. The  other  cells  remain  attached  for  a  time,  and  in  the  litera- 
ture bear  the  name  ^^  Sammelzellen.^'  The  mycelium  is  very 
delicate,  and  soon  disappears,  the  resting  spores  then  lying  free 


Fiu.  30.- — Urophlyclis  alfalfae  (Lagerheim)   Magnus,  causing  galls  at  the  crown 
of  an  alfalfa  plant.     {After  Jones  and  Drechsler  1920.) 

in  the  host  cells  and  giving  no  indication  of  their  origin.  They 
have  been  mistaken  for  the  resting  spores  of  Synchytrium,  e.g.,  U. 
-pluriannulatus  (B.  &  C.)  Farlow  (1908:  12).  The  details  of 
resting  spore  formation  are  discussed  by  Clinton  (1902:  56)  for  P. 
maculare,  by  Tisdale  (1919:  147)  for  P.  zeae-maydis,  and  by 
Jones  and  Drechsler  (1920:  305)  for  U.  alfalfae  and  V.  pluri- 
annulatus. From  the  latter  account,  especially  it  is  evident  that 
the  development  of  the  mycelium  and  resting  spores  is  a  very 
definite    process.     A    comparison   of  the   figures   published   by 


CHYTRIDIALES 


105 


Clinton  and  Drechsler  shows,  moreover,  a  striking  similarity  in 
morphology  between  species  of  the  two  genera.  The  presence 
of  the  Sammclzellcn  on  the  resting  spores  of  these  forms  was 
interpreted  by  Schroter  as  indicating  a  sexual  conjugation  of 
young  thalli,  and  he  erected  the  genus  Urophlydis  to  include 
the  sexual  forms.  This  genus  was  incorporated  by  him  in  his 
family  Oochytriaceae,  while  the  forms  in  which  indications  of 
sexuality  are  absent  were  retained  in  Physoderma  of  the  Cladochy- 


FlG.  37. —  Urophlydis  pluriannulatus  (B.  &  C.)  Farlow  in  Sanicula,  except 
(s)  which  is  U.  alfalfae  (Lagerheim)  Magnus,  (h)  Zone  of  haustoria.  (m) 
Secondary  series  of  turbinate  cells,  (n)  Young  turbinate  cells  of  tertiary  series, 
(r)  Mature  resting  spore  which  arose  as  a  terminal  expansion  of  the  apical 
haustorium  of  turbinate  cell  (s)  Mature  resting  spore  bearing  zone  of  pits  mark- 
ing points  of  disappearance  of  haustoria.  (i)  Septate  turbinate  cell  whose  cells 
have  put  out  hyphae  bearing  apically  a  secondary  series  of  turbinate  cells. 
(After  Jones  and  Drcchder  1920.) 


triaceae.  His  view  was  supported  by  investigations  of  Magnus 
(1897;  1901 ;  1902)  but  has  not  been  confirmed  by  others.  There 
seems  to  be  at  present  no  reason  for  believing  that  a  sexual 
process  occurs  in  resting  spore  formation  in  any  of  the  species. 
Consequently,  a  new  basis  for  separation  of  the  genera  Physo- 
derma and  Urophlydis  has  been  sought,  the  one  used  here  being 
that  suggested  by  von  Minden.  As  here  constituted,  the  genus 
Physoderma  includes  those  species  which  cause  merely  discolora- 
tion or  slight  tliickening  of  the  affected  host  parts,  while  Uro- 


106 


THE  LOWER  FUNGI— PHYCOMYCETES 


phlyctis  embraces  those  which  cause  pronounced  deformation  or 
gall  formation.  Correlated  with  this  distinction  there  is  a  sUght 
difference  in  the  shape  of  the  resting  spore,  that  of  Urophlyctis 
being  more  often  and  more  strikingly  flattened  on  one  side.  This 
separation  is  clearly  inadequate  and  further  investigation  of 
these  forms  will  probably  result  either  in  the  fusion  of  the  two 
genera  or  in  a  rearrangement  of  the  species  on  a  wholly  new  and 
as  yet  unsuspected  basis. 


Fig.  38. — (a)  Urophlyctis  leproides  (Trabut)  P.  Magnus  forming  galls  on  beet 
root;  (b)  U.  kriegeriana  Magnus,  showing  section  through  gall  on  Carum  con- 
taining sorus  of  resting  spores;  (c)  U.  pulposa  (Wallroth)  Schroter,  showing 
resting  spores  in  cells  of  Chenopodium.  (a,  b,  after  Magnus;  c,  after  Schroter 
1897.) 


The  genus  Physoderma  as  here  constituted  contains  about 
twenty  species,  of  which  the  following  are  known  to  occur  in 
North  America. 

P.  macular e  Wallr. — in  Alisma  plnntago. 

P.  menyanthis  de  Bary — in  Menyanthis  trifoliata. 

P.  zeae-maydis  Shaw — in  Zea  mays  (see  Mycologia,  14:  81,  1922). 

P.  vagans  Schroter — in  Sium,  etc. 

P.  heleocharidis  Schroter— in  Eleocharis. 


CHYTRIDIALES  107 

6.  Urophlyctis  Schroter  (Jahresber.  Schles.  Gesell.  f.  Vaterl. 
Ciiltur,  60:  198,  1882). 
The  present  status  of  the  genus  Urophlyctis  is  indicated  in  the 
above  discussion  of  Physoderma.  Some  of  the  species  of  the 
genus  are  limited  to  the  underground  portions  of  their  host, 
while  others  occur  only  in  the  parts  above  ground.  Some  exert 
a  dissolving  action  on  the  cells  of  the  host  and  develop  a  wide- 
spreading  mycelium;  others  are  limited  to  the  cells  originally 
infected  by  the  swarmspores.  Eight  species  are  included  in  the 
genus  by  von  Minden.  The  following  are  known  to  occur  in 
North  America. 

U.  pulposa  (Wallroth)  Schroter  (Fig.  38,  c) — in  Atriplex  and  Chenopodium. 
U.  alfalfae  (Lagerheim)   Magnus  (Fig.  36,  37,  s) — in  Medicago  (Wilson 
1920). 

U.  pluriannulatus  (B.  &  C.)  Farlow  (Fig.  37,  t) — in  Sanicida. 
U.  major  Schroter — in  Rumex. 

Doubtful    Chytridiales 

1.  Hyphochytrium  Zopf  (1884:  187). 

syn.  Hyphophagus  v.  Minden  (1911:  420). 
Those  chytrids  in  which  the  mycelium  is  described  as  of  con- 
siderable diameter  were  brought  together  in  the  family  Hypho- 
chytriaceae  by  Schroter  (1892:  83).  He  included  the  genera 
Catenaria,  Hyphochytrium,  Polyrhina,  and  Tetrachytrium.  Later 
von  Minden  (1911:  383)  used  the  family  name  but  excluded 
Hyphochytrium,  the  family  as  formed  by  him  embracing  Macro- 
chytrium,  Zygochytriwm,  and  Tetrachytrium.  There  seems  to  be 
no  sound  basis  for  the  recognition  of  the  family  and  it  is  here 
discarded.  The  genus  Hyphochytrium  contains  a  single  species, 
H.  infestans  Zopf  (Fig.  39),  parasitic  in  the  apothecia  of  Helotium. 
The  mycelium  is  rather  broad,  richly  branched,  of  uniform 
diameter,  and  occasionally  septate.  Sporangia  are  formed 
from  terminal  or  intercalary  swellings.  The  swarmspores  are 
uniciliate.     Resting  spores  are  unknown. 

2.  Tetrachytrium  Sorokin  {Botaii.  Zeitung,  32 :  307,  1874). 

This  genus,  based  on  the  single  species,  T.  'triceps  Sorokin 
(Fig.  40),  is  known  only  from  the  original  description  and  figures. 
It  is  included  in  the  Hyphochytriaceae  by  Schroter  (1892:  83) 
and  von  Minden  (1911:  387). 


108 


THE  LOWER  FUNGI— PHYCOMYCETES 


3.  Zygochytrium  Sorokin  (Botan.  Zeitung,  32:  305,  1874). 

This    genus,    based   on    the    single    species,    Z.    aurantiacum 
Sorokin  (Fig.  41),  is  known  only  from  the  original  description 


Fig.  39. — Hypochytrium  infestans  Zopf  in  apothecia  of  Helotium.  (a)  Apothe- 
cia.  {h)  Portion  of  apothecium  in  section  showing  swarmsporangia  of  the 
parasite,      (c,  d)   Intercalary  and  terminal  swarmsporangia.      {After  Zopf  1884-) 


M)<fih 


Fig.  40.' — Tetrachylrium  triceps  Sorokin.  (a)  Swarmsporcs.  {b)  Con- 
jugating gametes,  (c)  Zygote,  {d)  Germinating  zygcjtes.  {c)  Immature 
plant.  (/)  Mature  plant  with  haustorial  disc,  {g)  Sporangium  escaping 
from  prosporangium;  lid  fallen  away,  {h)  Free  sporangium,  {k)  Sporangium 
with   four   swarmsporcs.      {v)   Escape    of   swarmspores.      {After   Sorokin    1874-) 

and  figures.  If  not  founded  on  faulty  observation  it  is  an 
extremely  interesting  form,  bearing  uniciliate  swarmspores  in 
sporangia  at  the  tips  of  a  homothallic  zygophore  recalling  that 
of  Sporodinia. 


CHYTRIDIALES 


109 


4.  Macrochytrium  v.  Minden  {Centralbl.  f.  Bakt.,  8:824,  1902). 

(See  also  v.  Minden,  1911:  385). 

An  interesting  genus  of  doubtful  relationships  based  on  the 

single   species,  M.  botryoides  von  Minden,  found   in   Germany 

growing  saprophytically  on  a  submerged  decaying  apple.     The 


Fig.  41. — Zygochytrium  aurantiacum  Sorokin.  (a)  Mature  plant  bearing 
two  prosporangia  with  papillate  lids,  (b,  c)  Sporangium  emerging  from  pore 
after  turning  aside  of  lid.  (d)  Free  sporangium,  (e)  Sporangiurn  containing 
swarmspores.  (/,  g,  h)  Swarmsporcs  escaping,  becoming  amoeboid,  and  ger- 
minating, {k,  m)  Conjugation  of  gametic  branches,  (n)  Mature  zygospore. 
{p)   Zygospore  germination.      {After  Sorokin  1874.) 

mycelium  is  cylindrical  and  broader  than  in  other  members  of 
the  order.  Superficially  the  fungus  resembles  Rhizophidiwn 
except  in  its  much  greater  size.  The  sporangium  dehisces  by  a 
large  hd.     Resting  spores  are  unknown. 


Fig.    42.^PoIyrhina    muHiformis    Sorokin.      (a)    Thallus    and    sporangia,      (h) 
Mature  swarmsporangia  with  escaping  swarmsporcs.      (After  Sorokin.) 

5.  Rhodochytrium  Lagerheim  {Botan.  Zeitmig,  51:  43,  1893). 

The  genus  Rhodochytrium,  based  on  R.  spilanthidis  Lag.  para- 
sitic on  the  common  ragweed,  Ambrosia,  is  of  extreme  interest 
to  the  student  of  phylogeny.     The  organism  is  evidently  an 


110  THE  LOWER  FUNGI— PHYCOMYCETES 

alga,  stores  starch,  and  is  most  closely  related  to  another  algal 
genus,  Phyllobium  Klebs  {Bot.  ZeiL,  39:  249,  1881).  Its  para- 
sitic habit  and  its  lack  of  chlorophyll  nevertheless  indicate 
fungous  tendencies.  The  life  history  and  cytology  of  the 
species  are  discussed  by  Griggs  (1912),  Atkinson  (1908  a,  b),  and 
Ramsbottom  (1913).  In  gross  aspect  the  organism  resembles 
Synchytrium  (see  p.  13). 

6.  Mitochytridium  Dangeard. 

See  discussion  under  Ancylistales. 

7.  Polyrhina  Sorokin. 

The  single  species,  P.  multiformis  Sorokin  (Fig.  42),  is  appar- 
ently the  same  as  Harposporium  anguillulae  Lohde  (see  Zopf, 
1888,  for  good  figures).     Its  position  is  doubtful. 

8.  Rhizidiocystis  Sideris  (Phytopathology,  19:  376,  1929). 
Based  on  R.  ananasi  Sideris,  parasitic  in  root  hairs  of  pineapple. 

Placed  by  the  author  in  the  Cladochytriaceae. 

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Wilson,  O.  T.,  Crown-gall  of  alfalfa.     Botan.  Gaz.,  70 :  51-68,  pi.  7-10, 1920. 
WiNGE,  O.,  Cytological  studies  in  the  Plasmodiophoraceae.     Arkiv  Butanik, 

129:  1-39,  pi.  1-3,  1912. 
WoRONiN,    M.,    Plasmodiophora    Brassicae,    Urheber    der    Kohlpfianzen- 

hernie.     Jahrb.  Wiss.  Botanik,  11 :  548-574,  pi.  29^34,  1878. 
Zeller,  S.  M.,  Fungi  found  on  Codium  mucronatum.     Publ.  Puget  Sound 

Biol.  Station,  2:  121-125,  pi.  20,  1918. 
ZoPF,  W.,  Zur  Kenntniss  der  Phycomyceten.     Nova  Acta  Ksl.  Leop.-Carol. 

Deufschen  Akademie  der  Naturforscher.,  47:  143-236,  pi.  12-21,  1884. 
,   Zur   Kenntniss  der  Infections-Krankheiten  niederer  Thiere  und 

Pflanzen.     Nova     Acta     Ksl.    Leop.-Carol.    Deutschen    Akademie    der 

Naturforscher.,  52:  313-376,  pi.  17-23,  1888. 
-,  Uber  einige  niedere  thiorische  und  pflanzliche  Organismen  u.s.w. 


Beitr.  z.  Physiol,  u.  Morph.  niederer  Organismen,  4 :  43-68,  1894. 


CHAPTER  IV 
ANCYLISTALES 

The  members  of  this  order  are  all  endobiotic  parasites,  the 
thallus  in  most  eases  being  confined  to  a  single  host  cell.  The 
parasite  gains  entrance  to  the  host  by  means  of  a  delicate  infection 
tube,  which  on  reaching  the  interior  rounds  up  at  the  tip  to  form  a 
small  spherical  bladder.  This  bladder  by  further  growth 
develops  into  the  thallus.  The  young  thallus  is  a  rather  short, 
unicellular,  more  or  less  cylindrical  tube.  In  some  species  it  is 
somewhat  branched  or  lobed.  At  maturity,  it  is  usually  divided 
by  transverse  septa  into  a  number  of  cells.  The  component  cells 
of  the  thallus  may  function  variously,  some  as  sporangia,  some 
as  gametangia,  and  some  vegetatively.  In  the  last  case  the 
cell  germinates  directly  by  a  slender  germ  tube,  which  may 
become  much  elongated  and  serve  as  an  infection  thread  by 
means  of  which  the  fungus  enters  another  host  cell.  The  cell 
of  the  thallus  in  this  case  is  perhaps  to  be  regarded  properly  as 
a  sporangium  which  has  assumed  the  method  of  germination 
characteristic  of  this  structure  in  the  higher  Oomycetes.  This 
type  of  germination  is  relatively  rare  in  the  order,  the  sporangia 
in  most  species  forming  swarmspores.  In  some  cases  all  the 
cells  of  a  single  thallus  function  alike.  Sporangia  and  sexual 
cells  are  developed  in  the  same  or  different  thalli,  a  given  species 
being  usually  either  homothalHc  or  heterothallic. 

The  sexual  process  in  the  group  has  not  yet  been  adequately 
studied.  The  cells  of  the  thallus  which  function  as  male  and 
female  gametangia  respectively  show  a  relatively  slight  degree 
of  morphological  differentiation  as  compared  with  those  of  the 
Oomycetes.  The  female  is  typically  larger  and  more  character- 
istically barrel-snaped  than  the  male  which  is  commonly  cyUn- 
drical.  Usually  copulation  of  the  two  cells  is  accomplished  by 
means  of  a  more  or  less  elongate  conjugation  tube.  The  terms 
oogonium  and  antheridium  may  be  used  only  tentatively  since 
oosphere  formation  has  not  been  convincingly  demonstrated. 
In  Ancijlistes  the  oosphere  seems  to  be  clearly  absent.  If  present 
in  other  members  of  the  group  it  is  at  best  imperfectly  differ- 

117 


118  THE  LOWER  FUNGI— PHYCOMYCETES 

entiated.  Nevertheless,  the  resting  spore  at  maturity  Ues  free 
in  the  female  cell  and  resembles  the  oospore  of  the  Saprolegniales. 
The  sexual  process  has  been  studied  cytologically  in  only  two 
species,  Myzocytium  vermicolum  Zopf  and  Ancylistes  closterii 
Pfitzer.  The  nuclear  history  in  these  forms  is  described  by 
Dangeard,  and  his  results  are  discussed  under  these  genera  below. 
Other  cytological  investigations  are  urgently  needed,  since  at 
present,  the  fundamental  nature  of  the  sexual  process  in  the 
various  members  of  the  group  is  in  doubt.  Not  infrequently 
resting  spores  are  formed  apparently  parthenogenetically  from 
the  contents  of  a  single  cell.  The  resting  spore  in  all  cases  is 
spherical  and  thick-walled.  In  some  species  it  germinates  by 
swarmspores,  in  others  by  a  germ  tube. 

In  several  respects  the  members  of  the  order  seem  to  be  more 
highly  developed  than  the  Chytridiales.  The  resting  spore  lies 
free  in  the  female  gametangium,  a  conjugation  tube,  rare  in  the 
chytrids,  is  commonly  formed,  and  in  Ancylistes  both  the  spor- 
angium and  resting  spore  germinate  by  germ  tube.  The  cells 
composing  the  thallus  show,  moreover,  a  greater  abiUty  to 
function  in  diverse  capacities,  division  of  labor  comparable  to 
that  in  higher  groups  being  evident.  In  these  various  respects 
the  group  appears  to  approach  the  Saprolegniales  and  is  perhaps 
to  be  regarded  as  intermediate  in  type  between  that  order  and 
the  Chytridiales.  The  group  is  regarded  as  more  primitive  than 
the  Saprolegniales  in  that  mycehum  is  absent  or  poorly  developed, 
a  well  defined  oosphere  absent,  and  the  gametangia  not  clearly 
differentiated  as  oogonium  and  antheridium.  In  Ancylistes, 
particularly,  zygomycetous  features  are  evident. 

The  order,  as  here  treated,  contains  the  single  family  Ancy- 
listaceae. 

Key  to  Genera  of  Ancylistales 

I.  Asexual     reproduction     accomplished     by     swarmspores     freed     from 
sporangia. 
A.  Mature  thallus  an  unbranched  tube,  divided  by  transverse  septa 

into  a  row  of  cells  of  similar  size  and  form,  usually  constricted  at 

the  septa. 

1.  Swarmspores  escaping  from  the  sporangium  fully  formed, 

and  encysting  individually  at  its  mouth  as  in  Achlya. 

1.  Achlyogeton,  p.  119 

2.  Swarmspores  not  encysting  at  the  mouth  of  the  sporangium ; 

contents  of  sporangium  usually  extruded  into  a  vesicle. 

2.  Myzocytium,  p.  120 


ANCYLISTALES  119 

B.  Mature  thallus  more  or  less  branched,  transversely  septate,  but 
not  markedly  constricted  at  the  septa;  component  cells  often 
differing  considerably  in  size  and  form. 

3.  Lagenidium,  p.  122 

ir.  Swarmspores  not  formed;  asexual  cells  of  thallus  germinating  by  germ 
tubes;  thallus  sometimes  considerably  branched. 

4.  Ancylistes,  p.  124 

1.  Achlyogeton  Schenk  (1859). 

In  this  genus  the  mature  thallus  is  an  unbranched  elongate 
tube,  septate  at  regular  intervals,  and  constricted  so  deeply  at 
the  septa  that  a  row  of  broadly  ellipsoidal,  slightly  connected 
cells  results.  Each  cell  functions  as  a  sporangium,  the  swarm- 
spores passing  through  an  exit  tube  to  the  exterior  of  the  host 
cell.  At  the  rupture  of  the  tip  of  the  tube  the  swarmspores  pass 
out  and  encyst  individually  at  the  mouth,  forming  a  globose 
aggregation  of  tiny  spheres  as  in  Achlya.  After  encystment  they 
swim  away.     They  were  figured  as  uniciliate  by  Schenk,  but 


Fig.  43. — Achlyogeton  entophytum  Schenk,  in  thread  of  Cladophora.     Chain  of 
segments  functioning  as  sporangia.      (After  Schenk  1859.) 

inasmuch  as  the  swarmspores  in  all  the  other  accepted  members 
of  the  order  (see  Resticularia)  are  bicihate  the  point  requires 
verification.  No  indication  of  sexuahty  has  been  obtained. 
Martin  (1927)  figures  thick-walled  resting  spores  which  he  found 
associated  with  the  sporangia  but  fails  to  demonstrate  their  true 
nature.  Oospore-like  resting  spores,  such  as  occur  in  other 
genera  of  the  family,  are  unknown. 

The  genus  was  based  on  a  single  species,  A.  entophytum  Schenk 
(Fig.  43),  found  in  cells  of  Cladophora.  It  was  recently  redis- 
covered by  iMartin  (1927)  in  Iowa.  Another  species  found  in 
the  bodies  of  Anguillulidae,  and  referred  to  this  genus  by  Sorokin 
as  A.  rosiratum  is  imperfectly  known,  and  may  be  more  properly 
included  in  or  near  Myzocytium  vermicolum  (Zopf)  Fischer, 
found  in  the  same  host. 


120 


THE  LOWER  FUNGI— PHYCOMYCETES 


2.  Myzocytium    Schenk    (tJber    das    Vorkommen    Kontraktiler 
Zellen  in  Pflanzenreich,  p.  70,  1858), 

The  mature  thallus  in  this  genus  corresponds  rather  closely  in 
form  with  that  of  Achlyogeton,  consisting,  as  there,  of  a  simple 
unbranched  tube.  Transverse  septation  results  in  the  formation 
of  a  row  of  more  or  less  bead-like  cells,  as  many  as  ten  being 
formed  in  a  single  thallus.     Rarely  reduced  non-septate  thalli 


Fig.  44.- — (a-c)  Myzocytium  proliferum  Schenk  in  Spirogyra.  (o)  Different 
cells  of  a  single  thallus  functioning  as  sporangia  and  sex  cells.  (6)  Chain  of 
sporangia,  (c)  Swarmsporo.  (d)  My.  vcrmicolum  (Zopf)  Fischer  in  Anguillula. 
{After  Zopf  I884.) 


occur  which  may  be  easily  confused  with  those  of  Olpidium.  A 
reduced  two-celled  thallus  was  misunderstood  by  Sorokin,  and 
made  the  basis  of  his  genus  Bicricium.  The  cells  of  the  thallus 
in  Myzocytium  function  either  as  sporangia  or  sexual  cells.  In 
the  latter  case  contiguous  cells  of  the  thallus  usually  function 
as  oogonium  and  antheridium,  since  the  species  are  almost  exclu- 
sively homothalhc.  Following  fertilization  a  spherical  thick- 
walled  resting  spore  ("oospore")  is  formed,  and  at  maturity 
lies  free  in  the  oogonium.     After  hibernation  it  germinates  by 


ANCYLISTALES  121 

swarmspores.  Sporangia  and  sexual  cells  are  formed  in  the  same 
or  different  thalli.  The  germinating  sporangium  puts  out  a 
slender  exit  tube  as  in  Achlyogeton,  but  here  a  thin-walled  vesicle 
rounds  up  at  the  tip  of  the  tube  and  the  contents  of  the  spor- 
angium pass  into  it.  In  M.  prolifemni  Schenk  (Fig.  44,  h)  the 
process  of  swarmspore  delimitation  is  completed  in  the  vesicle, 
the  swarmspores  being  no  more  than  imperfectly  fashioned 
when  the  protoplasm  flows  through  the  tube.  In  M.  vermicolum 
(Zopf)  Fischer  (Fig.  44,  d),  the  swarmspores  are  fully  formed  in 
the  sporangium,  and  the  vesicle  may  rupture  before  all  of  the 
swarmspores  have  passed  into  it  (Dangeard,  1906:  'pl.  3).  In 
any  case  there  is  no  Achlya-MkQ  encystment  comparable  to  that 
occurring  in  Achlyogeton. 

The  cells  of  the  thallus  which  function  as  sporangia  are  globose, 
ellipsoidal,  or  irregularly  contoured.  Rarely  two  exit  tubes 
occur.  The  swarmspores  are  laterally  biciliate,  the  cilium  which 
trails  in  swimming  being  longer  than  that  which  precedes  the 
spore.  The  gametangia  resemble  the  sporangia  in  shape,  the 
male  cell  being  commonly  the  more  slender. 

Knowledge  of  nuclear  phenomena  in  the  genus  rests  on  the 
work  of  Dangeard  (1906)  on  M.  vermicolum  Zopf.  Numerous 
nuclei  lie  scattered  through  the  young  thallus.  Each  sporangium 
receives  several  nuclei  when  segmentation  of  the  thallus  occurs, 
and  subsequently  these  divide  repeatedly  to  provide  the  nuclei 
for  the  uninucleate  swarmspores.  In  those  cells  of  the  thallus 
which  are  to  function  as  gametangia  a  relatively  small  number 
of  nuclei  exist.  The  male  gametangium  ("  antheridum  ")  usually 
contains  two  nuclei,  while  the  female  gametangium  ("oogonium  ") 
contains  approximately  eight.  Later  all  but  one  of  the  female 
nuclei  disintegrate  and  disappear.  One  male  nucleus  enters 
the  female  gametangium,  while  the  other  usually  fails  to  function. 
In  cases  in  which  the  male  cell  is  intercalary  between  two  female 
cells  it  is  possible  that  the  two  male  nuclei  fertihze  different 
female  cells.  A  coenocentrum  was  not  demonstrated.  The 
sexual  nuclei  fuse  in  the  young  resting  spore.  After  hibernation 
the  fusion  nucleus  divides,  about  ten  nuclei  being  provided  for 
the  swarmspores. 

The  genus  was  founded  on  M.  proliferum  Schenk,  occurring  in 
the  c  ells  of  varous  green  algae  {Oedogonium,  Cladophora,  Zygnema, 
Spirogyra,  Mesocarpiis,  Mougeotia).  This  species  is  widely 
distributed  in  Europe  and  has  been  collected  in  America  (Martin 


122 


THE  LOWER  FUNGI— PHYCOMYCETES 


1927;  Graff  1928).     The  following  additional  species  have  been 
referred  to  the  genus. 

M.  megastomurn  De  Wildeman— in  Closierium  and  Spirotaenia. 
M.  vermicolum  (Zopi)  Fischer — in  Anguillulidae. 

M.  (?)  irregulare  Petersen  (perhaps  a  species  of  Lagenidiurn)^\\\  Costna- 
riurn  and  Micrasterias. 


Fig.  45.- — Lagcnidium  rahenhorstii  Zopf  in  vegetative  cells  of  Spirogyra.  (a) 
Infecting  swarmspores.  (b)  Young  non-septate  thallus  developed  from  swarm- 
spore,  (c)  Septate  thallus.  (d,  e)  Cells  of  thallus  functioning  as  sporangia 
(sp.),  antheridia  (A),  and  oogonia  (0).  (J-h)  Swarmsporo  formation.  {After 
Zopf  1884.) 


3.  Lagenidium  Schenk  (Verhandl  PJnjs.  Med.  Gesell.  Wiirzhurg, 

9:  27,  1857). 

The  mature  thallus  in  Lagenidium  is  an  irregular  tube,  more 

or  less  branched  or  provided  with  protuberances.     Septa  divide 

the  thallus  at  indefinite  intervals  into  cells,  but  prominent  con- 


ANCYLISTALES 


123 


strictions  at  the  septa  are  usually  not  present.  The  resulting 
cells  differ  in  size  and  form,  and  some  of  them  may  be  slightly 
branched.  As  in  Myzocytium  the  component  cells  of  the  thallus 
may  function  either  as  sporangia  or  sexual  cells,  but  here  the 
male  and  female  gametangia  may  occur  on  the  same  or  on  differ- 
ent thalU.  In  some  species  {e.g.,  L.  entophijtum)  male  cells  are 
not  differentiated,  the  "oospores"  being  developed  without 
fertiUzation  (parthenogenetically).  The  germination  of  these 
spores  has  not  yet  been  observed.  The  classical  figures  of  Zopf 
(1884:  pi.  1-3)  picture  the  various  steps  in  the  life  cycle  in  two 
species  of  the  genus.  According  to  his  account  and  those  of  other 
early  students  the  sporangium  germinates  by  the  emission  of 


Fig.  46.- — Lagenidium  amcricanum  Atkinson  in  zygospores  of  Spirogyra. 
(a,  b)  Sporangia,  some  emptied,  {c-h}  Stages  in  swarmspore  formation. 
{After  Atkinson  1909.) 

the  contents  into  a  bladder  at  the  mouth  of  the  exit  tube,  the 
swarmspores  being  delimited  in  the  bladder.  Atkinson 
(1909:  330)  after  studying  two  species,  including  one  of  those 
figured  by  Zopf,  states  that,  in  fact,  a  bladder  is  not  formed. 
According  to  his  account  the  protoplasm  escapes  from  the  tip 
of  the  tube  as  a  naked  mass  and  though  usually  remaining  at  the 
mouth  in  the  form  of  a  ball  sometimes  breaks  away  as  a  detached 
sphere.  In  a  few  moments  a  rotary  motion  begins,  and  the 
swarmspores  are  gradually  delimited  and  escape  one  by  one  from 
the  moving  mass.  The  details  of  the  process  are  described  at 
some  length  and  in  an  interesting  manner.  To  the  writer  it 
seems  likely  that  the  bladder  is  sometimes  present  and  that  at 
other  times  the  tip  of  the  exit  tube  ruptures  before  it  forms.  It 
would  seem  that  too  much  emphasis  has  been  placed  on  the 


124  THE  LOWER  FUNGI— PHYCOMYCETES 

taxonomic  importance  of  the  presence  or  absence  of  the  vesicle 
here  and  elsewhere  in  the  Phycomycetes. 

The  genus  is  the  largest  in  the  order,  the  following  species 
being  included  by  von  Minden  (1911).  More  recently  still  other 
species  have  been  described  (Scherffel  1925). 

L.  rabenhorstii  Zopf  (Fig.  45)- — ^in  vegetative  cells  of  Spirngijra,  Mougeotia, 
and  Alesocarpuii. 

L.  entophytum  (Pringsheim)  Zopf — in  the  zygospore  of  Spirogijra,  often 
filling  it,  but  not  found  in  the  vegetative  cells.  The  species  L.  americanum 
Atkinson  (Fig.  46)  occurring  in  the  same  location  is  perhaps  the  same  species. 

L.  gracile  Zopf — ^also  in  the  zygospore  of  Spirogyra.  This  species  has  a 
more  slender,  less  branched  thallus  than  the  preceding.  "Antheridia"  are 
absent  in  both. 

L.  enecans  Zopf — in  diatoms. 

L.  pygmaeum  Zopf — in  pollen  grains. 

L.  ellipticum  De  Wildeman — An  imperfectly  known  and  doubtful  form 
occurring  in  rhizoids  of  mosses. 

L.  interniediuin  De  Wildeman — in  Cloi^terium. 

L.  closterii  De  Wildeman — in  Closterium. 

L.  syncytiorum  Klebahn — -in  Oedogonium. 

L.  marchelianurn  De  Wildeman — in  Oedogonium. 

4.  Ancylistes  Pfitzer  (1872). 

The  young  thallus  in  this  genus  is  a  cylindrical  tube,  and  may 
be  somewhat  branched.  At  maturity  it  becomes  septate  at 
rather  regular  intervals.  The  resultant  cells  may  swell  shghtly, 
but  deep  constriction  at  the  septa  is  not  usual.  Several  thalli 
may  lie  parallel  in  the  host  cell.  Swarmspores  are  not  formed 
in  the  genus,  and  typical  sporangia  are  lacking.  The  cells  of  the 
thallus  function  either  as  sexual  cells  or  vegetative  cells.  In 
the  latter  case  a  slender  germ  tube  arises  from  the  cell,  passes 
through  the  wall  of  the  host  cell,  and  elongates  into  a  mycelial 
thread.  This  comes  in  contact  with  another  host  cell,  bends 
around  it,  penetrates  it  by  means  of  a  delicate  infection  tube, 
and  discharges  its  contents  through  this  into  a  thin-walled 
bladder  which  forms  at  the  inner  end  of  the  tube.  This  bladder 
then  develops  into  a  new  thallus.  The  cells  which  develop 
vegetatively  in  this  manner  are  clearly  homologous  with  the 
sporangia  of  related  genera,  but  they  never  form  endogenous 
spores.  They  have  merely  assumed  the  method  of  germination 
usual  in  higher  Oomycetes. 

The  genus  was  founded  on  a  single  species,  A.  closterii  Pfitzer 
(Fig.  47),  occurring  in  the  desmid  Closterium.     In  this  species 


ANCYLISTALES 


125 


all  the  cells  of  a  single  thallus  function  alike,  as  vegetative  cells, 
as  male  cells,  or  as  female  cells.  This  species  is  consequently 
heterothallic,  two  thalli  lying  side  by  side  functioning  as  male 
and  female  thalh  respectively,  and  all  the  resting  spores  being 
formed  in  one  thallus.  The  male  gametangium  puts  out  a  short 
fertilization  tube  which  fuses  with  the  wall  of  the  nearest  female 
cell  and  the  content  of  the  male  cell  then  passes  over.  A  definite 
oosphere  has  not  been  demonstrated,  but  the  contents  of  the 


Fig.  47. — Ancylistcs  dostcrii  Pfitzer  in  cells  of  Clostcrium.  (a)  Cells  of  thallus 
germinating  to  form  infection  threads,  {h)  Oospores,  (c,  d)  Cells  of  neigh- 
boring thalli  united  by  conjugation  tubes  preceding  oospore  formation.  {After 
Pfitzer  1872.) 

fertilized  cell  contract  to  form  an  oospore-like  resting  spore. 
Germination  of  the  spore  is  by  germ  tube.  Another  species,  A. 
pfeifferi  de  Beck,  also  occurring  in  Closterium,  has  been  incor- 
porated in  the  genus  but  is  imperfectly  understood.  In  it  the 
male  and  female  gametangia  appear  to  alternate  in  the  same 
thallus,  but  this  has  not  been  clearly  demonstrated.  Some 
thalli  function  vegetatively  as  in  the  above  species.  The  method 
of  resting  spore  germination  is  unknown.  The  absence  of  swarm- 
spores  gives  the  genus  particular  interest,  and  the  formation  of 


126  THE  LOWER  FUNGI— PHYCOMYCETES 

germ  tubes  marks  it  as  the  most  highly  developed  member 
of  the  order. 

Knowledge  of  the  nuclear  history  in  the  genus  rests  wholly  on 
the  work  of  Dangeard  (1906)  on  A.  closterii  Pfitzer.  He  pictures 
the  young  thallus  as  plurinucleate,  the  nuclei  being  regularly 
spaced  in  a  single  row  in  the  thread.  In  the  segmentation  of 
the  thallus  each  cell  receives  several  nuclei.  In  the  beginning, 
each  vegetative  cell  contains  four  or  five  nuclei,  but  the  number 
is  doubled  by  a  single  simultaneous  mitosis.  The  eight  or  ten 
resultant  nuclei  pass  over  with  the  cytoplasm  through  the  germ 
tube  and  infection  thread  into  the  new  host  cell.  The  male 
gametangium  at  first  usually  contains  two  nuclei  while  the 
female  possesses  six  or  eight,  A  single  simultaneous  division 
later  doubles  the  number  in  each.  The  nuclei  and  cytoplasm  of 
the  male  cell  enter  the  female,  but  nuclear  fusion  apparently 
fails  to  occur.  The  resting  spore  matures  in  the  plurinucleate 
condition,  containing  both  male  and  female  nuclei.  It  is  possible 
that  a  fusion  occurs  at  the  time  of  germination,  though  it  has 
not  been  seen.     Germination  is  by  tube  (Dangeard,  1886). 

Doubtful  or  Excluded  Genera 

1.  Resticularia  Dangeard  (Le  Botaniste,  2:  96,  pi.  4,  1891). 
This  genus  was  based  on  a  single  species,  R.  nodosa  Dang. 

(Fig.  48),  found  parasitic  in  Lynghya.  It  was  accepted  by 
Fischer  (1892:  84)  and  Schroter  (1893:  92),  both  authors  placing 
it  next  to  Ancylistes.  Later  this  species  was  discovered  by 
Fritsch  (1903 :  649)  in  England  growing  in  Tolypothrix,  and  was 
redescribed  by  him.  He  states  that  it  occasionally  forms 
sporangia  containing  uniciliate  swarmspores.  He  also  described 
as  new  another  species,  R.  boodlei  Fritsch,  found  in  the  same 
host.  The  genus  is  listed  by  von  Minden  (1911 :  444)  as  a  doubt- 
ful member  of  the  Ancylistales.  In  the  present  state  of  our  knowl- 
edge a  satisfactory  disposition  of  it  cannot  be  made. 

2.  Rhizomyxa  Borzi. 

Discussed  above  under  Sorosphaera  of  the  Plasmodiophoraceae. 

3.  Lagenidiopsis  De  Wildeman  (Ann.  Soc.  Beige  Micros.,  20:  109, 

1896). 
A  single  imperfectly  understood  species,  L.  reducta  De  Wild., 
found  in  oogonia  of  Characeae. 


ANCYLISTALES 


127 


4.  Mitochytrium  Dangcard  (1911:  200). 

This  genus  was  erected  on  the  single  species,  M.  ramosum 
Dang.,  found  in  the  cells  of  Docidium,  a  desmid.  The  thallus, 
as  figured,  resembles  that  of  Lagenidium  except  that  it  is  provided 
at  several  points  with  finely  branched  rhizoids  and  is  non-septate. 
The  form  was  inadequately  discussed,  but  was  regarded  by  Dan- 
geard  as  intermediate  between  the  Ancylistales  and  Chytridiales. , 

5.  Protascus  Dangeard  (1906),  not  Protascus  Wolk  (1913). 
This  is  a  monotypic  genus  based  on  the  single  species,  P.  sub- 

idiformis  Dang.,  parasitic  in  the  body  of  Anguillulidae.     The 


Fig.  48.- — Resticularia  nodosa  Dangeard  in  Lyngbia.  (a)  Thallus  sending 
branches  outside  of  host.  (6)  Sporangium  germinating.  {c,d)  Zygospore 
formation.      {After  Dangeard  1890.) 

fungus  resembles  in  general  structure  Myzocytium  and  Lageni- 
dium but  differs  in  several  striking  respects.  The  endozoic 
thallus  is  septate  at  maturity  into  eight  cells  of  similar  aspect. 
These  fall  apart  at  the  septa,  and  may  be  termed  segments. 
They  function  as  sporangia  or  gametangia.  The  number  of 
spores  in  the  sporangium  is  extremely  variable  (approx.  8-200). 
They  pass  through  an  exit  tube  to  the  surface  of  the  host,  and 
are  there  apparently  discharged  with  considerable  violence.  The 
spore  is  non-motile  and  in  form  is  clavate  with  the  narrow  end 
tapering  to  a  sharp  point.  Infection  is  accomplished  when  the 
narrowed  end  of  the  spore  attaches  itself  to  the  new  host.  Seg- 
ments functioning  as  sporangia  and  gametangia  may  result  from 


128  THE  LOWER  FUNGI— PHYCOMYCETES 

a  single  thallus,  but  conjugating  segments  arise  from  different 
thalli.  As  a  result  of  conjugation  a  spherical  "oospore"  is  formed 
in  one  segment  of  each  pair. 

The  species  has  been  studied  by  Dangeard  (1906)  and  Maupas 
(1915).  The  former  author  saw  it  only  in  the  sporangial  stage, 
and  regarded  it  as  one  of  the  Hemiascales.  The  reasons  for 
incorporating  the  genus  in  the  Ancylistales  are  discussed  by  Maire 
(1915).  He  suggests  that  the  fungus  be  made  the  basis  of  a  new 
family,  Protascaceae,  which  he  regards  as  intermediate  between 
the  Lagenidiaceae  and  Ancylistaceae,  The  erection  of  the  new 
family  seems  premature  in  the  light  of  our  incomplete  knowledge 
of  the  order,  while  the  small  size  of  the  group  makes  it  unneces- 
sary. The  name,  Protascaceae,  is  unfortunate,  in  that  the  group 
may  easily  be  confused  with  the  Protascales  of  the  Ascomycetes. 

The  writer  is  not  convinced  that  Protascus  is  closely  related 
to  the  other  genera  incorporated  in  the  Ancylistales,  and  its 
inclusion  here  is  at  best  tentative.  At  present,  no  more  satis- 
factory disposition  of  it  seems  possible. 

6.  Lagena  Vanterpool  &  Ledingham  (1930:  192). 

A  monotypic  genus,  recently  erected  on  L.  radicicola  Vanter- 
pool &  Ledingham,  an  obligate  parasite  in  rootlets  of  cereals  in 
Sashatchewan.  Mycelium  is  absent.  The  thallus  is  unicellular, 
unbranched,  ovoid  to  cylindrical,  sometimes  curved,  and  is 
attached  to  the  host  wall  by  a  neck.  It  may  function  as  a 
sporangium  or  "coenogametangium."  The  contents  of  the 
sporangium  escape  into  a  thin-walled  vesicle,  in  which  bean- 
shaped,  laterally  biciliate  swarmspores  are  formed.  Thalli 
functioning  as  "coenogametangia"  conjugate  in  pairs  by  means 
of  a  tube,  and  a  thick-walled  "oospore"  recalling  that  of  Pythium 
is  formed.     Apparently  the  genus  lies  near  Lagenidium. 

BIBLIOGRAPHY:  ANCYLISTALES 

Atkinson,  G.  F.,  Some  fungous  parasites  of  algae.     Botan.  Gaz.,  48:  321- 

338,  fig.  1-8,  1909. 
,  Some  problems  in  the  evolution  of  the  lower  fungi.     Ann.  Myc,  7 : 

441-472,  1909. 
BoRzi,  A.,  Rhizomyxa,  nuovo  ficomicete.     53  pp.,  2  pi.,  Messina,  1884. 
Dangeard,    P.A.,    Note  sur  la  germination  de  I'oospore  de  TAncylistes 

closterii.     Bui.  Soc.  Linn.  Normandie,  10:  1886. 
,  Recherches  sur  le  d6veloppement  du  perith^ee  chez  les  ascomycetes — 

I.  Les  ancetres  des  champignons  sup6rieurs.     Le  Botanists,  9 :  207-226, 

pi.  2-8,  1906. 


ANCYLISTALES  129 

Dangeard,  p. a.,  Un  nouvcaii  genre  de  Chytridiaeccs.    Bui.  Snc.  Myc.  France, 

27:  200-203,  fig.  1,  1911. 
Fischer,  A.,  Archimycetes.     Die  Pilze  Deutschlanxh,  Oesterreichs  und  der 

Schweiz  {Rabenhorsf  s  Kryptogamen-Flora)  V:  11-160,  1892. 
Fritsch,  F.  E.,  Two  fungi,  parasitic  on  species  of  Tolypothrix  (Resticularia 

nodosa  Dang.,  and  R.  Boodlei  n.  sp.).     Ann.  Botany,  17:  649-664,  pi. 

29,  1903. 
Graff,  P.  W.,  Contributions  to  our  knowledge  of  western  Montana  fungi — ■ 

II.  Phycomycetes.     Mycologia,  20:  158-179,  1928. 
Maire,  R.,  Remarques  sur  le  Protascus  subuliformis  a  propos  de  la  com- 
munication de  M.  E.  Maupas.     Bui.  Soc.  Hist.  Nat.  Afrique  Nord.,  7': 

50-51,  1915. 
Martin,  G.  W.,  Two  unusual  water  molds  belonging  to  the  family  Lagen- 

idiaceae.     Mycologia,  19:  188-190,  1  fig.,  1927. 
Maupas,  E.,  Sur  un  champignon  parasite  des  Rhabditis.     Bui.  Soc.  Hist. 

Nat.  Afrique  Nord.,  7^:  34-49,  1915. 
MiNDEN,  M.  v.,  Ancylistineae.     Kryptogamenflora  der  Mark  Brandenburg, 

5:  423-461,  1911. 
Pfitzer,  E.,  Ancylistes  Closterii,  ein  neuer  Algen-Parasit  aus  der  Ordnung 

der    Phycomyceten.     Monatsber.    d.    Konigl.    Akad.    d.    Wiss.,    Berhn, 

pp.  379-398,  fig.  1-16,  1872. 
Ramsbottom,  J.,  The  generic  name  Protascus.     Trans.  Brit.  Mycol.  Soc, 

5:  143,  144,  1915. 
ScHENK,  A.,  Achlyogeton,  eine  neue  Gattung  der  Mycophyceae.     Botan. 

Zeitung,  17:  398-400,  1859. 
Scherffel,  a.,  Endophytische  Phycomyceten-Parasiten  der  Baoillariaceen 

und  einige  neue  Monadinen.     Ein  Beitrag  zur  Phylogenie  der  Oomy- 

ceten  (Schroter).     Archiv  Protistenk.,  52:  1-141,  5  pL,  1925. 
ScHROTER,  J.,  Ancylistineae.     Die  Natiirliche  Pflanzenfamilien  (Engler  und 

Prantl),  V:  88-92,  1893. 
Vanterpool,  T.  C,  and  G.  A.  Ledingham,  Studies  on  "browning"  root 

rot  of  cereals  I.     The  association  of  Lagena  radicicola  n.  gen.  n.  sp.  with 

root  injury  of  wheat.     Canadian  Jour,  of  Research,  2:  171-194,  pi.  1-2, 

fi^.  1-7,  1930. 
WoLK,  P.  C.  van  DER.,  Protascus  colorans,  a  new  genus  and  a  new  species 

of   the    Protoascineae-group:   the   source  of  "yellow-grains"  in  rice. 

Mycol.  Centralbl,  3:  153-157,  pi.  1,  1913. 
ZoPF,  W.,  Zur  Kenntniss  der  Phycomyceten.     Nova  Acta  Ksl.  Leop.-Carol. 

Deutschen  Akadeynie  der  Natiirforscher,  47 :  143-236,  pi.  12-21,  1884. 


CHAPTER  V 
BLASTOCLADIALES 

This  small  order  consists  of  the  single  family  Blastocladiaceae 
embracing  about  a  dozen  species  in  three  genera.  The  forms 
included  agree  in  the  possession  of  non-cellulose  walls  and 
uniciliate  swarmspores.  The  group  is  apparently  most  closely 
related  to  the  Monoblepharidales.  It  has  been  given  ordinal 
rank  previously  by  Petersen  (1910:  494)  and  von  Minden  (1916: 
189).  Other  authors  have  incorporated  its  genera  in  the  Sap- 
rolegniales.  The  recent  monograph  of  Kanouse  (1927:  295)  is 
the  best  general  treatment  of  the  group.  The  members  of  the 
order  are  typically  aquatic.  They  occur  as  saprophytes  on 
submerged  plant  and  animal  substrata.  In  recent  years  a  few 
species  have  been  isolated  from  the  soil  (Coker  and  Braxton, 
1926:  146;  Harvey,  1925:  162;  1928:  560).  Of  the  three  genera 
included,  Blastocladia  and  Alloniyces  are  clearly  very  closely 
related.  The  third,  Gonapodya,  is  somewhat  less  certainly  a 
member  of  the  group. 

In  Blastocladia  and  Alloniyces  the  thallus  is  differentiated 
into  a  main  thickened  axis  or  trunk  and  slender  branches,  and 
is  attached  to  the  substratum  by  branching  rhizoids.  In  these 
respects,  relationship  is  indicated  to  both  the  Monoblepharidales 
and  the  Leptomitaceae  of  the  Saprolegniales.  The  similarity 
to  genera  such  as  Araiospora  and  Rhipidium  of  the  latter  group 
is  pronounced.  In  Gonapodya  there  is  no  differentiation  of  the 
thallus  into  a  central  thickened  portion  and  slender  branches, 
and  rhizoids  are  lacking.  The  thallus  is  composed  of  cylindrical 
hyphae  which  are  definitely  and  often  frequently  constricted  as 
in  the  Leptomitaceae,  and  cellulin  plugs  lie  in  the  constrictions. 

Asexual  reproduction  takes  place  by  means  of  swarmspores 
borne  in  thin-walled  sporangia  or  in  peculiar  thick-walled  resting 
sporangia.  The  thin-walled  sporangium  varies  in  shape  from 
ovoid  to  linear,  and  at  maturity  is  provided  with  a  single  apical 
exit  papilla  or  with  several  scattered  over  its  surface.  The 
sporangium  is  developed  terminally,  but  further  growth  of  the 

130 


BLASTOCLADIALES  131 

hypha  may  cause  it  to  assume  a  lateral  position.  Less  often 
sporangia  are  cut  off  in  basipetal  succession,  and  form  a  chain 
(Coker  and  Braxton,  1926:  pi.  10).  The  swarmspores  are  mono- 
planetic.  In  some  cases  they  pass  into  a  vesicle  as  in  Pythium 
before  being  freed.  In  Gonapodya  repeated  proliferation  of  new 
sporangia  within  the  old  occurs. 

The  resting  sporangium  is  an  outstanding  feature  of  the 
morphology  of  Blastocladia  and  Allomyces,  but  is  absent  in  Gona- 
podya. It  corresponds  more  or  less  in  form,  size,  and  position 
with  the  thin-walled  sporangium,  but  is  clearly  very  different 
in  character.  It  is  thick- walled,  the  wall  being  composed  of 
three  layers,  a  middle  thick  layer  and  outer  and  inner  thin  ones. 
The  outer  layer  is  in  reality  the  original  wall  of  the  hyphal  cell, 
and  in  some  species  at  the  maturity  of  the  resting  sporangium 
this  outer  wall  splits  allowing  the  sporangium,  enclosed  in  the 
other  two  walls,  to  fall  away.  In  other  cases  the  outer  wall 
remains  in  close  contact  with  the  sporangium  and  is  carried  away 
with  it.  The  appearance  of  the  mature  resting  sporangium  is 
characteristic.  In  no  other  known  group  of  Phycomycetes 
is  there  a  similar  structure.  Its  surface  is  covered  with  minute 
dots,  which  are  shown  in  section  to  be  the  mouths  of  cyhndric 
tubes  lying  in  the  middle  wall  and  almost  traversing  it.  At 
germination  this  wall  cracks  open,  and  a  prominent  exit  papilla 
is  formed  on  the  inner,  the  escaping  swarmspores  resembling 
those  freed  by  the  thin-walled  sporangium. 

Various  names  have  been  applied  by  different  writers  to  this 
resting  sporangium.  It  has  been  termed  the  conidium,  the 
resting  spore,  and  the  resting  cell.  Butler  (1911:  1030)  suggests 
that  it  is  perhaps  a  parthenogenetic  oospore.  Kanouse  (1927: 
292)  uses  the  terms  oogonium  and  oospore  in  this  connection 
without  quaUfication.  Moreover,  she  describes  and  figures  for 
Blastocladia  glohosa  Kanouse,  slender  filaments  associated  with  the 
resting  sporangium  which,  she  says,  are  undoubtedly  antheridial 
branches.  In  a  single  case,  she  found  a  cell  cut  off  at  the  tip  of  a 
branch  by  a  definite  septum,  and  regards  this  as  an  antheridium. 
The  process  of  fertiUzation  was  not  observed,  nor,  in  fact,  any 
indication  given  as  to  how  it  may  be  effected.  She  suggests 
the  possibility  that  it  is  accompHshed  by  means  of  motile  male 
cells,  though  none  were  observed.  She  admits  that,  in  any  case, 
these  so-called  "antheridia"  are  rare,  and  that  the  "oospores" 
(parthenospores)  usually  mature  parthenogenetically. 


132  THE  LOWER  FUNGI— PHYCOMYCETES 

The  true  nature  of  the  sexual  process  in  the  group  has  been 
only  very  recently  elucidated  by  Kniep  (1929).  Working  with 
a  hitherto  undescribed  species,  Allomyces  javanicus  Kniep,  he 
has  discovered  a  sexual  process  of  so  unique  and  distinctive  a 
type  that  on  this  basis  alone  the  group  is  deserving  of  ordinal 
rank.  In  this  species  the  usual  thin-walled  sporangia  and  the 
thick-walled  resting  sporangia  occur,  but  in  addition  to  these, 
thin-walled  sexual  organs  (gametangia)  resembUng  the  sporangia 
in  shape  are  produced.  The  male  and  female  organs,  though 
similar  in  shape,  differ  regularly  in  size.  In  both  of  them 
uniciUate  swarm  cells  termed  gametes  are  formed.  The  larger 
gametangium  is  regarded  by  Kniep  as  the  female.  The  gametes 
delimited  in  it  are  markedly  larger  than  those  formed  in  the 
smaller  male  gametangium.  After  their  escape  from  the  game- 
tangia the  larger  and  smaller  gametes  fuse  in  pairs  forming 
bicihate  zygotes.  The  zygote  swims  for  a  time,  but  finally  comes 
to  rest,  assumes  a  membrane,  and  puts  out  a  germ  tube  which 
develops  directly  into  the  rhizoid  system  which  is  to  anchor  the 
new  plant.  Kniep  applies  the  terms  antheridium  and  oogonium 
to  the  larger  and  smaller  sexual  organs  respectively. 

Fusion  of  cihate  gametes  in  pairs  is  not  known  to  occur 
elsewhere  in  the  Phycomycetes  above  the  level  of  the  Chytri- 
diales.  There  it  has  been  observed  in  several  species  of  Olpidium 
and  Synchytrium.  In  the  Monoblepharidales  the  male  game- 
tangium frees  wholly  similar  ciliate  cells,  but  the  content  of  the 
female  gametangium  rounds  up  to  form  a  non-ciliate  practically 
non-motile  oosphere.  As  the  Monoblepharidales  and  Blasto- 
cladiales  are  admittedly  closely  related  the  discovery  in  other 
species  of  these  groups  of  intermediate  types  of  sexuality  would 
not  be  surprising.  Since,  at  present,  the  sexual  process  in  other 
species  of  the  Blastocladiales  is  wholly  unknown  the  acceptance 
of  heterogamic  copulation  of  planogametes  as  the  typical  method 
of  sexuality  in  the  group  must  be  regarded  as  tentative. 

As  Kniep  finds  the  thick- walled  resting  sporangia  also  in  Allo- 
myces javanicus  these  structures  are  apparently  of  the  nature  of 
chlamydospores  and  are  hardly  to  be  regarded  as  parthenogeneti- 
cally  developed  oospores. 

Though  the  swarmspore  is  typically  unicihate  throughout 
the  order,  occasional  individuals  with  two  or  more  cilia  are 
observed.     Kniep  has  shown  that  these  represent  merely  cases 


BLASTOCLA  D I  ALES 


133 


in  which  the  final  cleavage  of  the  cytoplasm  of  the  sporangium 
has  failed  to  occur.     Such  swarmspores  have  two  or  more  nuclei. 

Key  to  Genera  of  Blastocladiaceae 

I.  Thallus  not  differentiated  into  a  stout  main  axis  and  more  slender 
brunelies,  composed  of  cylindrical  hyphae  which  are  definitely  and 
usually  frequently  constricted;  sporangia  proliferating;  thick-walled 
resting  sporangia  unknown. 

1.  Gonapodya,  p.  134 


Fig.  49. — (a,  h)  Gonapodya  siliquaeformis  (Reinsch)  Thaxter.  (c-e)  G. 
polymorpha  Thaxter.  (a)  Typical  plant,  segments  short,  sporangia  proliferating. 
(b)  Sporangium  freeing  unicDiate  swarmspores.  (c)  Segmented  portions  of 
plant  borne  sub-umbellately  on  a  slender  hypha.  {d,  e)  Sporangia  showing 
extreme  variation  in  size  of  swarmspores.      {After  Thaxter  1895.) 


II.  Thallus  provided  with  a  stout  main  axis  bearing  more  slender  branches; 
thick-walled  resting  sporangia  present. 

A.  Thallus  separated  into  definite  segments  by  pseudosepta,  some- 
times slightly  constricted  at  the  septa. 

2.  Allomyces,  p.  135 


134  THE  LOWER  FUNGI— PHYCOMYCETES 

B.   Thallus  lacking  pseudosepta,  not  definitely  constricted. 

3.  Blastocladia,  p.  136 

1.  Gonapodya  Fischer  (1892:  378). 

A  small  genus  of  two  species,  G.  siliquaeformis  (Reinsch) 
Thaxter  and  G.  polymorpha  Thaxter.  The  genus  is  of  somewhat 
doubtful  affinities,  and  is  placed  here  chiefly  on  account  of  its 
uniciliate  zoospores  and  non-cellullose  walls.  In  its  prominently 
segmented  mycelium  it  corresponds  to  the  members  of  the 
Leptomitaceae  of  the  Saprolegniales.  Since  the  species  are 
known  only  in  the  sporangial  condition  and  lack  the  pecuHar 
resting  sporangia  of  Blastocladia  and  Allomyces,  the  incorporation 
of  the  genus  here  is  at  best  tentative. 


Fig.  oO.— Allomyces  arhuscula  Butler,      (a)  Pseudosepta  as  seen  in  longitudinal 
section,      (h)  Same  in  transverse  section.      {After  Barrett  1912.) 

The  thallus  is  filamentous,  resembling  somewhat  that  of  Lep- 
tomitus,  but  with  shorter  segments  (Fig.  49).  A  basal  portion 
attached  to  the  substratum  by  rhizoids  is  lacking.  The  hyphae 
are  usually  deeply  constricted,  so  much  so  that  at  times  the  short 
rounded  segments  give  the  aspect  of  a  chain  of  beads.  Branching 
occurs  chiefly  at  the  tips  of  the  primary  hyphae,  dense  tufts 
of  segmented  branchlets  terminating  slender  more  or  less  unseg- 
mented  threads.  The  sporangia  are  borne  terminally,  and 
undergo  repeated  proliferation.  They  are  elongated  and  taper 
toward  the  tip.  The  zoospores  are  typically  uniciliate,  though 
biciliate  spores  apparently  sometimes  exist. 

The  species  occur  on  submerged  fruits,  twigs,  and  other  plant 
parts  and  are  saprophytic. 


BLASTOCLA  D I  ALES 


135 


2.  AUomyces  Butler  (1911:  1027). 

syn.  Septocladia  Coker  &  Grant  (1922:  180). 
The  thallus  is  differentiated  into  a  stout  basal  portion  and 
slender   branches.     The   former  is  attached  to  the  substratum 


Fig.  51. — Blastocladia  pringsheimii  Reinsch.  (a)  Single  large  plant  showing 
portion  of  rhizoid  system ;  branches  bearing  sporangia  and  young  resting  spores. 
(6)  Smaller  plant  bearing  spherical  resting  spores,  (c)  Resting  spores,  (d) 
Swarmspore.      (e)  Optical  section  of  wall  of  resting  spore.      (.After  Thaxter  1896.) 

by  rhizoids.  The  branches  are  separated  into  definite  seg- 
ments by  pseudosepta,  and  are  sometimes  constricted  at  the 
septa  (Fig.  50).  The  pseudosepta,  at  least  in  early  stages,  are 
perforated,  so  that  the  protoplasm  of  adjacent  segments  is 
continuous.  The  branching  of  the  thallus  is  dichotomous  to 
sympodial.     The  sporangium  is  provided  with  a  varying  number 


136  THE  LOWER  FUNGI— PHYCOMYCETES 

of  exit  papillae.  The  members  of  the  genus  seem  to  prefer 
animal  substrata,  being  found  on  dead  flies,  bones,  etc.,  in 
the  water. 

Four  species  have  been  described  which  belong  beyond  question 
in  this  genus.  They  are  Allomyces  arhuscula  Butler  (1911 :  1023), 
Blastocladia  strangulata  Barrett  (1912: 353),  Septocladia  dichotoma 
Coker  &  Grant  (1922:  180),  and  Allomyces  javanicus  Kniep 
(1929).  The  first  three  are  perhaps  identical,  but  the  various 
workers  who  have  published  on  the  group  do  not  agree  in  their 
treatments.  The  student  should  consult  von  Minden  (1916:  214), 
Fitzpatrick  (1923:  166),  and  Kanouse  (1927:  303),  as  well  as 
the  original  papers. 

3.  Blastocladia  Reinsch  (1878:  298). 

The  thallus  resembles  that  of  Allomyces,  but  lacks  pseudosepta 
and  is  not  definitely  constricted  (Fig.  51).  The  sporangium 
is  provided  with  only  a  single  exit  papilla.  The  genus  includes 
at  present  seven  species.  All  were  found  growing  saprophyti- 
cally  on  submerged  plant  substrata.  The  most  complete  treat- 
ment of  the  genus  is  that  of  Kanouse  (1927:  297)  but  the  papers 
of  Thaxter  (1896:  45)  and  von  Minden  (1916:  189)  also  should  be 
consulted. 

BIBLIOGRAPHY:  BLASTOCLADIALES 

Barrett,  J.  T.,  The  development  of  Blastocladia  strangulata  n.  wp.     Botan. 

Gaz.,  54:  353-371,  pi.  18-20,  1912. 
Butler,  E.  J.,  On  Allomyces,  a  new  aquatic  fungus.     Ann.  Botany,  26: 

1023-1034,  fig.  1-18,  1911. 
Coker,  W.  C.  and  H.  H.  Braxton,  New  water  molds  from  the  soil.     Jour. 

Elisha  Mitchell  Sci.  Soc,  42:  139-147,  pi.  10-15,  1926. 
Coker,  W.  C.  and  F.  A.  Grant,  A  new  genus  of  water  mold  related  to 

Blastocladia.     Jour.  Elisha  Mitchell  Sci.  Soc,  37 :  180-182,  pi.  32,  1922. 
Fischer,  Ai.f.,  Saprolegnieae,  Die  Pilze  Deutschlands,  Oesterreich,  und  der 

Schweiz.  {RahenhorsVs  Kryptogamen-Flora),  V:S10-378,  fig.  50-61, 1892. 
Fitzpatrick,    H.    M.,    Generic    concepts   in  the   Pythiaceae  and   Blasto- 

cladiaceae.     Mycologia,  15:  166-173,  1923. 
Harvey,  J.  V.,  A  study  of  the  water  molds  and  Pythiums  occurring  in  the 

soils  of  Chapel  Hill.     Jour.  Elisha  Mitchell  Sci.  Soc,  41:  151-164,  pi. 

12-19,  1925. 
,  A  survey  of  water  molds  occurring  in  the  soils  of  Wisconsin  as  studied 

during  the  summer  of  1926.     Trans.   Wise  Acad.  Sci.,  23:  551-565, 

pi.  4-7,  1928. 
Kanouse,  Bessie  B.,  On  the  distribution  of  the  water  molds,  with  notes  on 

the  occurrence  in   Michigan  of  members  of  the  Leptomitaceae  and 

Blastocladiaceae.     Papers  Michigan  Acad.  Sci.,  5:  105-114,  1925. 


BLASTOCLADI  ALES  137 

,  A  monographic   study  of  special  groups  of  the  water  molds   I. 

Blastocladiaceae   II.     Leptomitaceae  and   Pythiomorphaceae.     Amer. 

Jour.  Botany,  14 :  287-306,  335-357,  pi.  32-34,  48,  1927. 
Kniep,  Hans,  Allomyces  javanicus  n.  sp.  ein  anisogamcr  Phycomycet  mit 

Planogameten.     Ber.  Deut.  Bot.  Gesell.,  47 :  199-212,  7  fig.,  1929. 
MiNDEN,    M.    v.,    Saprolegniineae.     Kryptogamenflora   der  Mark  Branden- 
burg, 5:  479-608,  fig.  1-15,  1912. 
,   Beit  rage  zur   Biologic  und  Systematik  einheimischer  submerser 

Phycomyceten,     in     R.     Falck,     Mykologische     Untersuchungen    und 

Berichte.,  1:  146-255,  pi.  1-8,  1916. 
Petersen,  H.  E.,  An  account  of  Danish  freshwater  Phycomycetes,  with 

biological  and  systematical  remarks.     Ann.   MycoL,  8:  494-560,  fig. 

1-27,  1910. 
Reinsch,  p.  F.,  Beobachtungen  iiber  einige  neue  Saprolegnieae.     Jahrb. 

Wiss.  Bot.,  11:  283-311,  pi.  14-^7,  1878. 
ScHROTER,  J.,  Saprolegniineae.     Die  Naturliche  Pflanzenfamilien  {Engler  und 

Prantl),  V:  101-104,  fig.  83-87,  1893. 
Thaxter,    R.,    New   or  peculiar   aquatic   fungi — 3.  Blastocladia.     Bolan. 

Gaz.,  21:  4.5-52,  pi.  3,  1896. 


CHAPTER  VI 
M  ON  OBLEPH  ARID  ALES 

The  members  of  this  order  differ  strikingly  from  the  Saproleg- 
niales  in  that  the  antheridium  frees  ciliate  male  cells  (antherozoids, 
spermatozoids,  sperms)  which  swim  to  the  oogonium  and 
fertilize  the  oosphere.  Since  this  type  of  fertilization  occurs 
nowhere  else  in  the  fungi  the  group  is  of  unusual  interest  to  the 
student  of  phylogeny.  That  school  of  mycologists  which 
regards  the  fungi  as  a  heterogeneous  group  of  degenerate  forms, 
derived  at  various  points  from  different  types  of  the  algal  series, 
finds  in  this  order  a  convenient  intermediate  type  connecting 
the  Saprolegniales  with  such  algae  as  Vaucheria  and  Oedogonium 
in  which  fertilization  by  spermatozoids  occurs.  Those  students 
who  prefer  to  derive  the  higher  Phycomycetes  from  the  lower 
see  in  the  isogamic  fusion  of  zoospore-like  cells  in  certain  chytrids 
the  primitive  type  of  sexuality  from  which  the  heterogamic 
copulation  existing  in  the  Monoblepharidales  has  arisen.  This 
second  point  of  view  receives  support  from  the  recent  work  of 
Kniep  on  Allotnyces  javanicus  (p.  132)  and  from  the  fact  that  the 
oosphere  of  Monoblepharis  is  characterized  to  a  limited  degree 
by  motility. 

The  existence  of  this  remarkable  and  interesting  group  of 
aquatic  fungi  was  first  noted  by  Cornu  (1871 :  58) .  He  (1872 :  82) 
founded  the  genus  Monoblepharis  describing  and  figuring  two 
species,  M.  sphaerica  and  M.  polymorpha,  and  enumerating  a 
third,  M.  prolifera.  The  last  named  species  was  independently 
described  and  figured  by  Reinsch  (1876:  293)  under  the  name, 
Saprolegnia  siliquaeformis,  only  the  sporangial  stage  being  seen. 
Cornu  (1877:  227)  regarded  the  species  as  identical  with  his 
M.  prolifera,  and  stated  that  since  the  publication  of  his  earlier 
paper  he  had  observed  its  oospores.  He  says  that  these  are 
borne  in  oogonia  resembling  the  zoosporangia,  and  result  from 
fertilization  of  an  oosphere  by  motile  spermatozoids.  On  the 
basis  of  this  statement  and  because  of  the  uniciliate  character 
of  the  zoospores  the  species  has  been  retained  in  the  group  by 

138 


MONOBLEPHARI  DALES  139 

various  authorities.  Fischer  (1892:  378)  made  it  the  basis  of 
a  new  genus,  Gonapodya,  and  this  genus  and  Monohlepharis  make 
up  the  Monoblepharidineae  of  his  classification  and  that  of 
Schroter  (1893:  106).  The  statement  by  Cornu  that  spermato- 
zoids  occur  in  M.  prolifera  has  never  been  verified  by  any  other 
worker,  and  Thaxter  (1895:  478)  suggests  that  Cornu  may  have 
been  misled  as  to  their  presence  by  the  great  variation  in  size 
exhibited  by  the  zoospores  in  some  instances.  He  feels,  more- 
over, that  Cornu's  "oospores"  may  have  been  merely  encysted 
sporangia.  The  mycelium  of  Gonapodya  differs  very  strikingly 
from  that  of  Monohlepharis,  in  being  constricted  as  in  the  Lepto- 
mitaceae,  and  in  most  of  the  recent  classifications  (Thaxter, 
1895:  478;  v.  Minden,  1912:  576)  the  genus  is  included  in  that 
family.  Here  it  is  incorporated  instead  in  the  Blastocladiaceae 
(p.  134)  on  account  of  its  uniciliate  zoospores  and  non-cellulose 
cell  walls.  Laibach  (1927),  has  recently  studied  both  Mono- 
hlepharis and  Gonapodya  in  stained  preparations  and,  impressed 
by  the  similarity  of  nuclei  and  cytoplasmic  vacuolation  in  the 
two  genera,  advocates  the  incorporation  of  Gonapodya  in  the 
Monoblepharidales  on  cytological  bases. 

Following  the  establishment  of  the  genus  Monohlepharis  by 
Cornu  a  period  of  twenty-five  years  elapsed  before  any  member 
of  the  genus  was  seen  again,  some  workers  coming  to  doubt  the 
very  existence  of  a  genus  having  the  unique  characters  which 
he  figured  and  described.  However,  in  1895,  Thaxter  described 
two  new  species  from  America,  his  account  corroborating  the 
essentials  of  Cornu's  description.  Subsequently,  other  species 
have  been  observed  by  Thaxter  (1903)  in  America,  and  by  Lager- 
heim  (1900),  Woronin  (1904),  von  Minden  (1911),  and  Laibach 
(1926;  1927)  in  Europe. 

The  order  is  the  smallest  in  the  fungi,  and  as  here  treated  con- 
sists of  the  family  Monoblepharidaceae  containing  the  single 
genus,  Monohlepharis. 

The  mycelium  of  Monohlepharis  is  saprophytic,  occurring 
usually  in  decaying  twigs  lying  in  the  water.  It  is  coenocytic 
and  characteristic  in  aspect.  The  cytoplasm  forms  a  network  of 
meshes  which  are  regular  in  size  and  form,  a  strikingly  uniform 
vacuolation  resulting.  The  strands  of  protoplasm  tend  to  cross 
the  hyphae  at  right  angles  rather  than  to  run  longitudinally  as 
in  the  Saprolegniales.  The  fertile  hyphae  arise  from  a  branching 
vegetative  mycelium  which  is  fixed  to  the  substratum  by  rhizoids. 


140  THE  LOWER  FUNGI— PHYCOMYCETES 

They  are  rigid  in  habit,  usually  unbranched,  and  lack  septa  other 
than  those  cutting  off  the  sexual  organs  and  sporangia. 

Except  in  the  species,  M.  macrandra  Lag.,  the  oogonia  and 
antheridia  are  borne  together  on  the  same  hypha.  In  fact  in 
certain  species  the  antheridium  is  borne  on  the  oogonium.  It 
differs  from  the  oogonium  in  size  and  shape.  The  oogonium  is 
a  rounded  to  more  or  less  elongate  cell  tapering  above  to  a  defi- 
nite beak.  Before  fertilization  it  ruptures  at  the  apex,  an  open 
mouth  resulting  through  which  a  portion  of  the  contents  is 
expelled  by  the  violence  of  the  discharge.  The  remainder  of 
its  protoplasm  then  contracts  to  form  a  definite  oosphere.  The 
spermatozoids  escape  from  the  antheridium  through  a  terminal 
opening  and  are  uniciliate.  They  swim  about,  come  to  rest  on 
the  unfertilized  oogonium,  crawl  over  its  wall  with  an  amoeboid 
movement,  and  find  their  way  into  its  mouth.  A  single  sperma- 
tozoid  effects  fertilization,  sinking  slowly  into  the  substance  of 
the  oosphere.  In  some  of  the  species  the  fertilized  oosphere 
pushes  through  the  mouth  of  the  oogonium  and  rounds  up 
outside  before  assuming  the  thick  wall  which  marks  its  transfor- 
mation into  the  oospore.  In  other  species  it  matures  within  the 
oogonium.  Germination  of  the  oospore  occurs  apparently  in  all 
cases  by  a  germ  tube. 

Accounts  presented  by  different  workers  on  the  group  are 
not  in  agreement  with  respect  to  the  character  of  the  swarm- 
sporangia  and  swarmspores.  In  some  of  the  species  large  clavate 
organs  resembling  the  sporangia  of  Saprolegyiia  occur.  In 
these  are  formed  uniciliate  cells,  which  Lagerheim  regards  as 
swarmspores.  Thaxter's  studies  indicated  that  these  clavate 
cells  are  merely  abnormally  large  antheridia,  and  he  states 
that  intermediate  sizes  exist  between  them  and  the  normal 
smaller  type.  He  says  that  the  sporangia  correspond  in  size 
and  form  with  the  oogonia,  and  form  biciliate  swarmspores. 
Following  the  appearance  of  Thaxter's  paper  Lagerheim  founded 
the  genus  Diblepharis  to  include  the  species  in  which  Thaxter 
had  reported  biciliate  swarmspores,  and  retained  in  Monoblc- 
-pharis  the  species  in  which  he  believed  the  swarmspores  to  be 
uniciliate.  Later  Thaxter  (1903)  reported  the  biciliate  condition 
in  one  of  Lagerheim's  own  species.  Apparently  other  workers 
have  never  observed  biciliate  swarmspores,  and  recently  Laibach 
1927)  suggests  that  the  biciliate  cells  observed  by  Thaxter  were 
the   swarmspores   of   some   parasite    which    had    attacked    the 


MONOBLEPHARI  DALES 


141 


Wt.' 


mi 


oosphere.  He  maintains  the  position  that  the  swarmspores 
in  all  the  species  are  uniciliate.  In  any  case,  there  seems  to  be 
no  basis  at  present  for  retaining  the  genus  Diblepharis. 

The  genus,  Myrioblepharis,  founded  by  Thaxter  (1895)  on  a 
single  very  remarkable  species,  Myr.  paradoxa  (Fig.  52),  was 
incorporated  in  the  Monoblepharidales  by  Lotsy.  However, 
as  it  is  known  only  in  the  sporangial 
stage  its  position  is  uncertain.  The 
sporangium  is  developed  terminally 
and  at  maturity  emits  its  entire  con- 
tents as  a  naked  protoplast  through  an 
apical  opening.  This  adheres  at  the 
mouth  as  a  spherical  mass  where  it 
rotates  rapidly.  Proliferation  of  the 
sporangium  occurs  and  a  second  mass 
is  soon  pushed  out  below  the  first. 
Proliferation  continues  rapidly,  and  as 
the  third  mass  appears  the  first  breaks 
up  into  four,  rarely  more,  multiciliatc 
spores  which  swim  away.  This  proc- 
ess is  repeated  many  times,  a  series  of 
twelve  or  more  empty  sporangia  being 
sometimes  found  below  the  rotating 
spheres  at  the  tip  of  the  sporangio- 
phore.  Since  multiciliate  zoospores 
occur  in  no  other  genus  of  fungi  the 
form  is  of  peculiar  interest,  but  there 
seems  to  be  no  reason  for  including  it 
even  as  a  doubtful  species  in  the  pres- 
ent order.  The  zoospores  recall  those 
of  the  alga,  Vaucheria.  The  fungus 
is  discussed  by  vonMinden  (1912:  476) 
on  the  basis  of  material  collected  by  him  in  Germany.  He  is 
incUned  to  regard  the  multiciliate  spores  as  those  of  a  protozoan 
parasitic  in  a  species  of  Pythium. 

As  here  recognized  the  genus  Monoblepharis  includes  six 
species.  They  have  been  separated  on  rather  outstanding 
characters  as  follows. 


Fig.  52.- — M yriobU  pharis  para- 
doxa Thaxtor  {After  Thaxter.) 


142  THE  LOWER  FUNGI— PHYCOMYCETES 

Key  to  Species  of  Monoblepharis 

I.  Oospore  normally  maturing  within  the  oogonium. 

A.  Oospore  smooth,  antheridium  borne  on  the  oogonium. 

1.  Oogonia  large,  normally  superposed  in  single  series. 

1.  M.  insignis  Thaxter  (Fig.  54,  a-d) 

2.  Oogonia  small,  fasciculate  at  the  tips  of  the  hyphae. 

2.  M.  fasciculata  Thaxter  (Fig.  54,  e-g) 

B.  Oospore  warted,  antheridium  borne  below  the  oogonium. 

3.  M.  sphaerica  Cornu  (Fig.  53,  a-c) 

II.  Oospore  normally  maturing  outside  of  the  oogonium. 

A.  Oospore  adherent  to  the  mouth  of  the  oogonium,  tlie  antheridium 

normally  borne  on  the  oogonium. 

1.  The  antheridium  borne  above  the  middle  third  of  the  oogo- 

nium, lacking  an  abruptly  distinguished  point  of  insertion, 
narrowly  cylindrical. 

4.  M.  polymorpha  Cornu  (Fig.  53,  d-f) 

2.  The   antheridium   borne   below   the   terminal   third   of   the 

oogonium,  arising  from  an  abruptly  distinguished  point  of 
insertion,  broadly  cylindrical. 

5.  M.  brachyandra  Lagerheim  (Fig.  53,  g-h) 

B.  Oospore  falling  away  from  the  mouth  of  the  oogonium;  oogonia 

and  antheridia  normally  borne  on  separate  hyphae. 

6.  M.  inacrandra  (Lag.)  Woronin. 

Two  additional  species,  known  only  in  the  sporangial  stage,  M. 
regignens  Lag.  and  M.  ovigera  Lag.,  are  omitted  because  of 
imperfect  knowledge.  Laibach  (1927)  has  erected  for  these  the 
genus  Monoblepharopsis,  and  regards  it  as  intermediate  between 
Monoblepharis  and  Gonapodya.  He  recognizes  M.  regignens 
(Lag.)  Laibach  without  reserve,  but  suggests  the  probability 
that  M.  ovigera  (Lag.)  Laibach  constitutes  merely  a  variation 
of  it.  Moreover,  Laibach  states  that  Monoblepharis  brachyandra 
Lag.  represents  merely  a  developmental  phase  of  M.  polymorpha, 
and  intimates  that  M.  insignis  Thaxter  and  M.  fasciculata  Thax- 
ter belong  in  the  same  category. 

Although  Lagerheim  presented  isolated  facts  concerning  the 
cytology  of  Monoblepharis  our  knowledge  of  the  nuclear  history 
in  the  genus  rests  almost  wholly  on  the  recent  researches  of 
Laibach.  Both  writers  state  that  the  oogonium  is  uninucleate 
in  the  beginning  and  remains  so  until  after  fertilization.  In 
this  respect  the  female  organ  differs  strikingly  from  that  of  any 
other  known  member  of  the  Oomycetes.  Here  the  term  gamete, 
rather  than  coenogamete,  may  be  correctly  applied  (p.  31). 


MONOBLEPHA RI DALES 


143 


According  to  Laibach's  account  the  sporangium  and  antherid- 
ium  are  both  multinucleate  in  the  beginning,  and  differ  only  in 
the  number  and  size  of  the  ciliate  cells  which  are  formed,  the 
spermatozoids  being  fewer  and  smaller. 

After  the  male  nucleus  enters  the  oosphere  the  sex  nuclei  may- 
rest  side  by  side  for  a  considerable  period  before  fusion  takes 


Fig.  53. — (.a-c)  Monoblepharis  sphaerica  Cornu.  (d-f)  M.  polymorpha  Cornu 
ig-h)  M.  brachyandra  Lag.  {a,b)  Antheridium  below  oogonium,  (c)  Mature 
oospore,  (d-f)  Oogonia  and  antheridia.  (g)  Swarmsporangium  and  biciliate 
swarmspores.  {h)  Mature  oospores,  (a,  b,  c,  e,  after  Cornu;  others  after  Thaxter 
1903.) 


place.  Reduction  of  chromosomes  apparently  occurs  in  the  first 
division  of  the  fusion  nucleus.  Several  subsequent  mitoses 
occur,  and  when  the  germ  tube  is  put  out  by  the  oospore  as  many 
as  sixteen  nuclei  may  be  present. 

The  mycelium  is  wholly  non-septate  up  to  the  time  of  the 
formation  of  reproductive  cells.     Laibach  finds  that  sporangia 


144 


THE  LOWER  FUNGI— PHYCOMYCETES 


a 


Fig.  54. — (a-d)  Monoblepharis  insignis  Thaxtcr.  (c-g)  .1/.  fasciculala 
Thaxter.  (a)  Oogonia  in  linear  series  each  bearing  an  antiicridium.  (h) 
IMfferentiation  of  ooplasm  and  antherozoids.  (c)  Oosphere  formed;  finely 
granular  periplasm  escaping  through  pore  in  oogonial  wall ;  uniciliate  antherozoids 
creeping  over  wall  toward  pore,  (d)  Fertilized  oosphere  and  swarmsporan- 
gium.  (c)  Fasciculate  oogonia.  (/,  g)  Oogonia,  oospore,  antheridia.  Magni- 
fication of  (a)  and  («)  the  same;  that  of  others  same  but  higher.  {After  Thaxter 
1896.) 


MONOBLEPHA  li  I  DA  LES  145 

develop  in  greatest  numbers  in  fresh  water  at  about  10"C.  while 
antheridia  and  oogonia  appear  at  higher  temperatures  especially 
in  polluted  water.  Oospores  may  develop  in  the  spring  and 
germinate  in  the  autumn,  or  develop  in  the  autumn  and  hiber- 
nate until  spring. 

BIBLIOGRAPHY:  MONOBLEPHARIDALES 

Atkinson,  G.  F.,  Some  problems  in  the  evolution  of  the  lower  fungi.     Ann. 

Myc,  7:  459-462,  1909. 
CoRNU,  Max,  Note  sur  deux  genres  nouveaux  de  la  famille  des  Sap rolegn ices: 

Rhipidium  et  Monoblepharis.     Bull.  Soc.  Bot.  France,  18:  58,  1871. 
,  Monographie  des  Saprolegniees.     Ann.  Sci.  Nat.  Bot.  (5  ser.),  15: 

82-93,  vl.  2,  1872. 
,  Remarques  sur  quelques  Saprolegniees  nouvelles.     Bull.  Soc.  Bot. 


France,  24:  227,  1877. 
Fischer,  Alf.,  Monoblepharidaceae.     Die  Pilze  Deutschlands,  Oesterreich, 

der  Schweiz  {Rabenhorsl' s  Kryptogamen-Flora),  1^:  378,  1892. 
Lagerheim,    G.,    Mycologische    Studien    II.     Untersuchungen    iiber     die 

Monoblepharidiineen.     Bihand  till  K.  Svenska.  Vet.  Akad.  Handl.  25: 

Afd.  3,  No.  8,  1-42,  pi.  1-2,  1900. 
Laibach,  F.,  Zur  Zytologie  von  Monoblepharis.     Ber.  Deutsch.  Botan.  Ges., 

44:  59-64,  S  fig.,  1926. 
,  Zytologische  Untersuchungen  iiber  die  Monoblepharideen.     Jahrb. 

Wiss.  Botanik,  66:  596-630,  pi.  12-13,  12  fi^.,  1927. 
LoTSY,    J.    P.,    Vortrage   iiber  botanische  Stammesgeschichte  1 :  122-130, 

fig.  65-70,  1907. 
MiNDEN,  M.  v.,  Monoblepharidineae.     Kryptogamenflora  der  Mark  Branden- 
burg, 5:  462-478,  1911. 

,  Gonapodya.     Kryptogamenflora  der  Mark  Brandenburg,  5  :  576,  1912. 

Reinsch,    p.,    Beobachtungen   iiber   einige   neue   Saprolcgniineen.     Jahrb. 

Wiss.  Botanik,  11 :  293,  1876. 
ScHROTER,      J.,     Monoblepharidineae.     Die     Natilrliche     Pflanzenfarnilien 

(Engler  und  Prantl),  V:  106-107,  1893. 
Thaxter,  R.,  New  or  peculiar  aquatic  fungi — I.   Monoblepharis.  Botan. 

Gaz.  20 :  433-440,  pi.  29,  1895. 
,  New  or  peculiar  aquatic  fungi — 2.  Gonopodya  Fischer  and  Myrio- 

blepharis  nov.  gen.     Botan.  Gaz.,  20:  477-485.     pi.  31,  1895. 
-,  Notes  on  Monoblepharis.     Rhodora,  5 :  103-108,  pi.  1^6,  1903. 


WoRONiN,    M.,    Beitrag   zur   Kenntnis   der   Monoblepharideen.     Mem.    de 
L'Acad.  Imp.  d.  Sc.  de  St.  Petersburg  (8  ser.),  16 :  1-24,  pi.  1-3,  1904. 


CHAPTER  VII 
SAPROLEGNIALES 

The  fungi  composing  this  order  are  commonly  termed  the 
water  moulds.  By  certain  early  students  (Pringsheim,  1858: 
284)  they  were  incorporated  in  the  algae.  They  occur  more  or 
less  abundantly  in  all  fresh  waters,  usually  preferring  those 
which  are  clear  and  relatively  pure.  In  stagnant  or  polluted 
waters  their  development  is  retarded  by  the  presence  of  bacteria 
and  infusoria.  A  striking  exception  exists  in  the  case  of  Lep- 
tomitus  lacteus  which  grows  in  waters  containing  large  amounts 
of  organic  substances,  such  as  occur  in  the  drains  from  certain 
types  of  manufacturing  establishments,  paper  mills,  sugar 
factories,  etc.  The  members  of  the  order  are  usually  saprophytic, 
being  often  found  on  plant  or  animal  remains  lying  in  the  water. 
In  recent  years  many  species  have  been  isolated  from  the  soil. 
A  few  are  known  to  be  parasitic.  The  saprophytic  forms  occur 
on  a  wide  variety  of  substrata  including  decaying  algae,  woody 
or  herbaceous  parts  of  vascular  plants,  the  bodies  of  insects, 
and  other  types  of  non-living  organic  matter.  Practically  all 
the  species  may  be  grown  in  pure  culture.  Sterihzed  flies 
immersed  in  sterilized  water  in  watch  glasses  afford  perhaps 
the  most  commonly  used  source  of  nutriment.  Bits  of  egg 
albumen,  ant  pupae,  aphids,  and  cooked  peas  also  have  been 
extensively  used.  More  satisfactory  and  constant  results  may 
be  obtained  if  sterilized  synthetic  media  are  used,  and  if  isolations 
are  made  from  single  spores  or  hyphal  tips.  Marked  variation 
in  the  development  of  the  mycelium  and  reproductive  bodies 
may  be  obtained  by  altering  the  chemical  constitution  of  the 
medium.  The  physiological  treatises  of  Klebs  (1899),  Kauffman 
(1908),  Obel  (1910),  and  Pieters  (1915  a)  are  extremely  important 
in  this  connection,  and  should  be  consulted  before  any  attempt 
to  do  critical  taxonomic  work  is  made. 

The  mycelium  of  the  Saprolegniales  is  profusely  developed. 
It  usually  consists  of  two  sorts  of  hyphae,  internal  threads 
(rhizoids)  which  ramify  throughout  the  substratum  and  taper 

14t) 


SAPROLEGNIALES  1 4  7 

abruptly  to  pointed  ends,  and  external  filaments  which  arise  from 
the  former,  float  in  the  water,  and  have  in  mass  a  whitish  cottony 
aspect.     The  hyphal  walls  give  the  test  for  true  cellulose. 

Asexual  spores  are  borne  in  specialized  sporangia,  and  sexual 
reproduction  when  present  takes  place  by  the  formation  of 
antheridia  and  oogonia  which  differ  from  each  other  strikingly  in 
size  and  shape.  The  oogonium  is  usually  more  or  less  globose,  and 
at  maturity  contains  one  or  more  naked  protoplasmic  oospheres. 
Later  these  assume  a  cellulose  wall  and  are  then  termed  oospores. 
The  antheridium  is  clavate  and  smaller  than  the  oogonium.  In 
fertilization  a  tube  put  out  by  the  antheridium  enters  the  oogo- 
nium and  discharges  its  contents  directly  into  the  oosphere. 
Some  species  mature  their  oospores  without  fertilization  and  are 
termed  parthenogenetic  or  apogamous.  Some  lack  antheridia 
entirely  and  are  termed  apandrous.  Ciliate  sexual  cells  are 
wholly  absent.  Swarmspores  are  commonly  formed  and  are 
always  biciliate. 

In  the  development  of  abundant  mycelium  and  in  the  forma- 
tion of  morphologically  distinct  oogonia  and  antheridia  the  group 
shows  a  marked  advance  from  the  condition  in  the  Chytridiales 
and  Ancylistales.  In  the  absence  of  cihate  sexual  cells  it  is 
sharply  separated  from  the  Monoblepharidales  and  Blasto- 
cladiales.  It  is  clearly  most  closely  related  to  the  Peronosporales, 
these  two  orders  indeed  being  so  closely  connected  by  inter- 
mediate forms  that  no  single  absolute  point  of  distinction  between 
them  exists  as  the  basis  of  a  taxonomic  separation.  The  Sap- 
rolegniales  are  distinguished  in  general  by  their  aquatic  habit 
and  persistent  sporangia,  while  the  Peronosporales  for  the  most 
part  are  characterized  by  a  terrestrial  habit  and  deciduous 
sporangia,  the  latter  often  being  termed  conidia.  The  members 
of  the  family  Pythiaceae  of  the  latter  order  possess  characters 
more  or  less  intermediate  between  those  of  the  Saprolegniales 
and  Peronosporales,  and  in  some  classifications  are  included  in 
the  Saprolegniales. 

The  order  Saprolegniales,  as  here  constituted,  contains  two 
families,  Saprolegniaceae  and  Leptomitaceae,  embracing  a  total 
of  nearly  one  hundred  species  in  about  twenty  genera. 

Key  to  Families  of  Saprolegniales 

I.  Thallus   composed   of   cylindrical   branching   hyphae   lacking   definite 
constrictions. 

1.  Saprolegniaceae,  p.  148 


148  THE  LOWER  FUNGI— PHYCOMYCETES 

II.  Thallus  in  some  forms  consisting  of  cylindrical  l)rancliing  hyphae 
definitely  constricted  at  intervals;  in  others  differentiated  into  a 
prominent  stout  main  axis  from  which  usually  arise  relatively  more 
slender  branches,  with  or  without  definite  constrictions. 

2.  Leptomitaceae,  p.  171 

Saprolegniaceae 

The  hyphae  composing  the  floating  external  mycehum  in  this 
family  are  of  greatest  diameter  near  the  point  of  attachment 
to  the  substratum,  and  decrease  slowly  toward  their  outer 
ends.  They  are,  however,  nearly  cylindrical.  Their  branching 
is  usually  of  the  monopodial  type,  though  rarely  dichotomous. 
Septa,  other  than  those  cutting  off  the  reproductive  cells,  are 
absent ;  the  lumen  of  the  filament  consisting  of  a  single  continuous 
branching  cavity  containing  many  nuclei.  The  mycelium  is, 
therefore,  coenocytic,  as  in  the  majority  of  the  lower  Phyco- 
mycetes.  The  hyphal  walls  are  unlike  those  of  higher  fungi  in 
that  they  give  the  chemical  reaction  for  pure  cellulose  {i.e.,  turn 
blue  with  chloriodide  of  zinc).  Different  species  differ  greatly 
in  the  diameter  of  their  hyphae,  the  entire  range  extending 
approximately  from  five  to  one  hundred  microns.  The  length 
of  the  filaments  is  determined  to  an  extent  by  the  amount  of 
available  nutriment.  In  soil  inhabiting  species  the  mycelium  is 
relatively  depauperate,  and  in  culture  forms  a  dense  mat  of 
limited  extent. 

The  asexual  spores  are  borne  in  cylindrical,  clavate  to  globose 
sporangia  which  are  usually  terminal,  being  cut  off  by  transverse 
septa  at  the  tips  of  the  hyphal  branches.  Intercalary  sporangia 
sometimes  occur.  In  Dictyuchus  they  may  be  cut  off  terminally 
in  basipetal  succession. 

The  protoplasm  of  the  sporangium  is  much  denser  than  that 
in  the  remainder  of  the  hypha,  and  is  filled  with  numerous  nuclei 
which  flow  in  from  the  thread  before  the  septum  is  formed. 
Cleavage  planes  appear  in  the  protoplasm,  and  by  their  branching 
and  intersecting  the  content  of  the  sporangium  is  split  up  into 
a  number  of  small  irregularly  polyhedral  masses  each  containing 
a  single  nucleus.  These  are  the  spore  origins,  each  of  which 
finally  functions  as  an  independent  spore.  The  phenomena 
associated  with  the  escape  of  these  spores  from  the  sporangium 
and  their  germination  differ  in  different  species  of  the  group,  and 
to  a  considerable  extent  afford  bases  for  separation  of  genera. 


S-APROLEGNIALES  149 

In  several  genera  the  sporangiospores  encyst  within  the 
sporangium,  each  spore  enveloping  itself  in  a  thin  cellulose 
membrane.  In  other  cases  the  spore  is  provided  with  a  pair  of 
cilia,  and  escapes  from  the  sporangium  as  a  zoospore  without 
having  first  encysted. 

In  the  genus  Aplanes  the  sporangiospores  may  encyst  within 
the  sporangium,  and  then  germinate  in  situ  by  germ  tubes  which 
penetrate  the  sporangial  wall  and  reach  the  outside.  In  Geo- 
legnia  the  encysted  sporangiospores  are  thick-walled  and  remain 
quiescent  in  the  sporangium  until  freed  by  the  disintegration 
of  its  wall.  They  then  germinate  by  germ  tubes,  zoospores 
being  unknown.  In  Thraustotheca,  Calyptralegnia,  Dictyuchus, 
and  Brevilegnia  the  spore  after  encysting  within  the  sporangium 
germinates,  usually  by  the  emission  of  a  biciliate  zoospore  which 
swims  about  and  finally  encysts  again  before  germinating  by  a 
tube.  In  Thraustotheca,  Calyptralegnia,  and  Brevilegnia  the 
encysted  spores  escape  from  the  sporangium  before  germinating. 
In  Dictyuchus  the  zoospores  on  escaping  from  the  cysts  pass  to 
the  outside  through  individual  pores  in  the  sporangial  wall. 
In  Thraustotheca,  Calytralegnia,  and  Brevilegnia  the  wall  either 
disintegrates  or  is  ruptured  by  the  expansion  of  the  swelling 
spores  within;  the  spores  escaping  in  a  more  or  less  indefinite 
manner  through  an  opening  of  indeterminate  size.  In  all  the 
remaining  genera  of  the  family  the  spores,  instead  of  encysting 
within  the  sporangium,  escape  as  biciliate  zoospores  through  a 
small  pore  at  its  tip.  In  Achlya  and  Aphmiomyces  the  escaping 
spores  reach  the  water  just  outside  the  mouth  of  the  sporangium, 
and  there  became  encysted,  each  spore  rounding  up  and  assuming 
a  delicate  membrane.  The  escaping  spores  thus  form  a  more 
or  less  spherical  aggregation  at  the  mouth  of  the  sporangium. 
Their  failure  to  separate  from  one  another  on  reaching  the  water 
has  been  explained  by  Hartog  as  due  to  a  mutual  attraction, 
perhaps  chemical  in  nature,  to  which  he  applies  the  term  adelpho- 
taxy  (Couch,  1924  a;  Lounsbury,  1927).  After  a  period  of  rest  at 
the  mouth  of  the  sporangium  each  spore  slips  from  its  membrane, 
these  being  left  behind  as  empty  spheres.  The  escaping  zoo- 
spores are  reniform  (bean-shaped)  and  biciliate,  the  cilia  arising 
together  at  the  lateral  depression  corresponding  to  the  hilium 
of  the  bean.  After  a  period  of  swarming  in  which  the  zoospores 
swim  about  actively  they  come  to  rest  and  encyst  again,  the 
encysted  spores  being  termed  cystospores.     They  finally  ger- 


150  THE  LOWER  FUNGI—PHYCOMYCETES 

minate  by  a  germ  tube  which  develops  directly  into  mycelium. 
In  Saprolegnia,  Isoachlya,  and  Leptolegnia  the  zoospores  escape 
separately  into  the  water  and  swim  away  instead  of  encysting 
at  the  mouth  of  the  sporangium.  They  are  ovoid  or  pit-shaped, 
and  swim  by  means  of  two  cilia  attached  at  the  forward  more 
pointed  end.  After  a  period  of  motility  they  encyst  separately 
and,  later,  escaping  from  the  membrane,  swarm  again.  In  the 
second  period  of  motility  they  are  reniform  with  two  lateral 
cilia.  At  the  close  of  the  second  swarming  period  they  encyst 
and  germinate  by  germ  tube.  In  Protoachlya  some  of  the  spores 
escape  immediately  as  in  Saprolegnia  while  the  remainder 
encyst  at  the  mouth  of  the  sporangium  as  in  Achlya.  In  these 
genera  the  zoospores  are  termed  diplanetic  on  account  of  the  two 
periods  of  swarming,  the  phenomenon  of  diplanetism  exhibited 
here  contrasting  with  monoplanetism  in  those  genera  in  which 
only  a  single  swarming  occurs,  and  with  aplanetism  in  Aplanes 
and  Geolegnia.  The  spores  of  Achlya  and  Aphanomyces  are 
regarded  as  diplanetic  but  the  first  swarming  period  is  very  brief, 
being  confined  to  the  sporangium,  and  serves  only  to  carry  the 
spores  through  the  terminal  pore.  In  Achlya  the  spores  during 
this  period  correspond  to  those  of  the  first  type  in  Saprolegnia, 
and  this  is  probably  also  the  case  in  Aphanomyces,  although  the 
narrow  diameter  of  the  sporangium  in  this  genus  makes  demon- 
stration of  the  fact  difficult.  In  Thraustotheca  the  spores  are 
of  the  second  type  and  definitely  monoplanetic.  In  Pythiopsis 
they  are  monoplanetic,  but  strangely  enough  are  of  the  first  type. 
The  spores  of  Dictyuchus  have  been  regarded  as  monoplanetic, 
but  in  recent  years  a  peculiar  condition  has  been  shown  (Weston 
1919)  to  exist  in  this  genus.  The  spores  which  escape  from  the 
sporangium  are  of  the  reniform  type.  After  swarming  they 
encyst  and  later  under  favorable  conditions  may  swarm  again, 
though  germination  by  a  tube  often  occurs.  The  spores  in  the 
second  swarming  period  are  reniform  and  laterally  biciliate  as 
in  the  first  period.  Following  the  second  swarming,  encystment 
and  germ  tube  formation  occur.  This  condition  of  "repeated 
zoospore  emergence"  in  Dictyuchus  is  perhaps  present  also  in 
other  genera,  having  been  merely  overlooked.  It  seems  to  be 
present  in  Pythiopsis  intermedia  where  the  zoospore  is  of  the  first 
type.  The  two  swarming  periods  in  such  cases  are  not  to  be 
confused  with  true  diplanetism  in  which  zoospores  of  two  dis- 
tinct types  follow  each  other  always  in  the  same  order.     The 


SAPROLEGN I  ALES  151 

condition  in  Didyuchus  is  properly  to  be  regarded  merely  as  a 
variation  in  the  process  of  germination. 

The  existence  in  the  Saprolegniaceae  of  zoospores  of  two 
difTerent  forms  has  not  been  satisfactorily  explained.  Some 
authors  have  suggested  that  the  reniform  spore  is  the  primitive 
type  and  the  ovoid  spore  a  more  recent  development.  In  this 
connection  it  is  of  interest  to  note  that  the  zoospores  of  the 
Peronosporales  are  always  of  the  reniform  type.  Atkinson 
(1909)  gives,  as  evidence  of  the  monophyletic  nature  of  the  fungi, 
data  indicating  that  the  phenomenon  of  diplanetism  as  present 
in  the  Saprolegniaceae  has  gradually  evolved  through  the  Chy- 
tridales  and  Ancylistales. 

The  first  sporangium  formed  from  a  hypha  may  be  called  the 
primary  sporangium.  After  the  escape  of  the  zoospores  a  second 
sporangium  may  be  developed,  then  a  third,  and  so  on  until 
several  are  present.  The  secondary  sporangium  and  those  which 
follow  it  arise  by  one  of  several  different  methods.  In  Sap- 
rolegnia  and  Leptolegnia  the  new  sporangium  is  initiated  by  the 
upward  growth  of  the  septum  at  the  base  of  the  old  one,  and 
soon  fills  the  old  cavity  more  or  less  completely.  The  hypha 
may  even  grow  through  the  mouth  of  the  old  sporangium,  and 
cut  off  the  new  sporangium  at  a  considerable  distance  beyond 
its  tip.  Several  new  sporangia  may  be  developed  in  turn  within 
the  wall  of  the  primary  sporangium.  This  phenomenon  has 
been  termed  proliferation.  In  Achlya,  Aphanomyces,  Pythiopsis, 
and  Thraustotheca  cymose  branching  of  the  hypha  occurs  in 
the  development  of  new  sporangia,  lateral  sporangia  growing 
out  below  the  primary,  and  proliferation  being  absent.  In  Iso- 
achlya  and  Protoachlya  cymose  branching  and  proliferation  may 
both  occur  together.  Sometimes  sporangia  are  cut  off  in  basi- 
petal  succession  {Didyuchus).  Rarely  intercalary  sporangia 
occur. 

Certain  sporangia,  after  being  cut  off  from  the  hyphae,  may 
remain  quiescent  for  a  considerable  period,  and  later  discharge 
their  spores  in  the  usual  manner.  In  such  cases  the  term  resting 
sporangium  has  been  appHed.  These  are  merely  ordinary 
sporangia  whose  development  has  been  temporarily  arrested, 
perhaps  by  conditions  of  the  environment.  They  are  sometimes 
shorter  and  broader  than  the  typical  sporangia. 

The  term  chlamydospore  has  been  given  to  another  type  of 
non-sexual  repnxhictive  body  formed  in  many  species  of  the 


152  THE  LOWER  FUNGI— PHYCOMYCETES 

family.  These  bodies  are  usually  developed  at  the  ends  of  the 
hyphae  in  chains.  They  are  unicellular,  globose  to  ovoid  or 
pyriform,  thick-walled  resting  spores,  and  fall  apart  easily  at 
the  dividing  septa.  After  a  resting  period  of  variable  length 
they  germinate  by  a  germ  tube  on  which  a  sporangium  is  usually 
soon  formed.  The  chlamydospore  never  germinates  directly 
by  swarmspores,  and  in  this  respect  differs  distinctly  from  the 
resting  sporangium.  Chlamydospores  are  often  developed 
abundantly,  and  species  occur  (Humphrey,  1893:  83;  Weston, 
1917)  in  which  the  sexual  spores  seem  to  have  been  completely 
replaced  by  them.  Some  authors  avoid  the  term  chlamydospore, 
preferring  gemma,  conidium,  or  resting  spore. 

The  sexual  organs  are  developed  on  the  external  mycelium, 
and  are  usually  terminal  in  position,  though  occasionally  inter- 
calary. The  oogonium,  arises  as  a  swelling  of  the  hypha  which 
bears  it  (oogonial  branch),  and  at  maturity  is  definite  in  form. 
If  terminal  it  is  usually  more  or  less  globose,  if  intercalary 
barrel-shaped.  Its  wall  becomes  thickened  by  the  deposit  of 
new  material  on  the  inner  surface,  this  new  layer  failing  to  give 
the  reaction  for  true  cellulose  characteristic  of  the  primary  wall. 
Scattered  over  the  wall  in  some  species  a  varying  number  of 
small  circular  thin  spots  or  pits  occur.  These  constitute  points 
at  which  the  secondary  thickening  has  failed  to  take  place.  It 
was  formerly  supposed  that  the  fertilization  tubes  from  the 
antheridia  enter  at  these  spots,  but  this  has  been  shown  not 
to  be  necessarily  true.  Though  the  function  of  the  pits  is 
unknown  they  are  striking  in  appearance  and  of  taxonomic 
importance  in  certain  forms. 

The  antheridial  branches  are  slender  and  lateral.  The 
antheridium  is  cut  off  at  the  tip  of  the  antheridial  branch.  It 
is  cylindrical  or  clavate  in  form,  and  somewhat  thicker  than  the 
branch.  It  is  usually  applied  to  the  oogonium  in  such  a  fashion 
that  its  side  rather  than  its  tip  is  in  contact  with  the  oogonial 
wall.  In  some  species  antheridia  are  absent  or  only  rarely 
formed.  Not  infrequently  several  are  found  attached  to  a  single 
oogonium. 

The  same  primary  hypha  may  bear  both  oogonial  and  antherid- 
ial branches  or  only  those  of  one  sex.  In  ordinary  cultures  it  is 
often  impossible  to  determine  whether  two  hyphae  belong  to 
the  same  or  different  thalli,  and  since  single  spores  have  been 
used  as  the  starting  point  for  cultures  in  only  a  few  cases,  it 


SAPROLEGNIALES  163 

has  not  been  possible  for  workers  to  apply  with  certainty  the 
terms  monoecious  or  dioecious,  or  more  correctly  the  terms 
homothallic  and  heterothallic.  De  Bary's  terms  dichnous  and 
androgynous  have  been  commonly  used.  When  a  single  hypha 
gives  rise  to  both  oogonial  and  antheridial  filaments  the  species 
is  termed  androgynous.  In  such  cases  antheridia  may  attach 
themselves  to  oogonia  from  the  same  or  other  filaments.  If  a 
single  main  hypha  bears  filaments  of  only  one  sex  and  those  of 
the  other  sex  come  from  a  distance  and  seem  to  arise  from  other 
hyphae  the  species  is  diclinous.  Androgynous  species  have  been 
assumed  to  be  homothallic  and  diclinous  species  heterothaUic. 
True  heterothallism  has  been  demonstrated  by  Couch  (1924  b) 
in  Dictyuchus  monosporus  and  Achlya  hisexualis  (Coker,  1927: 
208),  and  will  doubtless  be  found  in  other  forms. 

The  protoplasmic  content  of  the  oogonium  is  at  first  homo- 
geneous, but  it  soon  becomes  differentiated  into  denser  more  or 
less  isodiametric  portions  separated  by  intervening  avenues  of 
clear  cell  sap.  These  naked  protoplasmic  bodies  gradually 
contract  and  become  spherical  in  form.  They  are  then  termed 
oospheres.  The  reserve  food  supply  present  in  the  oosphere 
exists  in  the  form  of  globules  of  fatty  material.  The  aspect  of 
the  oosphere  when  fully  formed  is  one  of  two  types  depending 
upon  the  position  and  size  of  these  globules.  In  all  cases  the 
fatty  reserve  lies  near  the  periphery,  but  in  one  type  it  is  in  the 
form  of  small  droplets  entirely  surrounding  the  protoplasm, 
while  in  the  other  it  is  collected  into  one  or  a  few  large  drops 
on  one  side.  In  the  latter  type  the  oosphere  has  a  one-sided 
aspect  and  is  termed  eccentric.  In  the  former  it  is  called  centric, 
while  intermediate  types  may  be  termed  subcentric.  Coker 
regards  this  situation  as  of  considerable  systematic  significance, 
and  says  that  one  type  of  oosphere  is  constant  in  a  given  species 
and  often  throughout  a  genus.  Finally  each  oosphere  secretes 
a  cellulose  wall  about  itself,  and  is  then  called  an  oospore.  The 
oospore  at  maturity  is  smooth  in  most  species,  but  in  some  is 
covered  with  prominent  warts  or  spines. 

As  soon  as  the  oospheres  are  differentiated  the  antheridia 
form  delicate  fertilization  tubes  which  penetrate  the  wall  of  the 
oogonium  and  branch  in  its  interior,  the  tip  of  each  branch  finally 
reaching  an  oosphere  and  coming  into  actual  contact  with  it. 
Earlier  writers  assumed  from  the  fact  of  the  presence  of  the 
fertilization  tubes  and  from  analogy  with  other  fungi  that  actual 


154  THE  LOWER  FUNGI— PHYCOMYCETES 

fertilization  occurs.  De  Bary,  failing  to  note  the  discharge  of 
the  content  of  the  tube  into  the  oosphere,  was  the  first  to  question 
it.  He  studied  living  material  of  several  species  of  Saprolegnia, 
and  concluded  that  even  in  those  cases  in  which  the  fertiUzation 
tubes  reach  the  oospheres  they  fail  to  rupture  and  fertilize  them. 
Parthenogenesis  was  believed  by  him  to  be  usual  in  the  group, 
and  his  views  have  subsequently  been  maintained  by  various 
students  including  Marshall  Ward,  Hartog,  and  Davis.  The 
early  work  on  the  problem  was  done  on  living  material.  Conse- 
quently the  study  of  nuclear  phenomena  was  impossible,  and 
the  actual  fusion  of  sex  nuclei  could  not  be  demonstrated.  Later, 
with  the  advent  of  modern  cytological  technique,  various  workers 
have  sought  to  solve  the  problem  of  sexuality  in  the  group. 
Unfortunately  the  results  have  been  diverse,  and  a  bitter  contro- 
versy has  ensued. 

Trow  has  published  several  papers  in  which  he  claims  to  have 
demonstrated  a  true  fertilization  and  a  fusion  of  sexual  nuclei 
in  several  species  of  Achlya  and  Saprolegnia.  His  statements 
have  been  severely  attacked  by  Hartog  and  later  by  Davis,  both 
of  whom  are  firm  in  the  conviction  that  parthenogenesis  is 
present  throughout  the  group.  Consequently,  our  knowledge 
of  the  sexuality  of  these  forms  is  in  a  state  of  uncertainty.  The 
papers  of  Hartog  (1896;  1899),  Trow  (1895;  1899;  1904),  and 
Davis  (1903)  afford  interesting  reading  on  account  of  the  fre- 
quently caustic  criticisms  which  they  contain.  The  fact  that 
in  cytological  investigation  interpretation  plays  an  important 
role  is  well  illustrated  by  the  work  on  this  group. 

The  oogonium  of  the  Saprolegniaceae  in  the  young  condition 
is  multinucleate.  When  the  oospheres  round  up  they  also  are 
multinucleate,  the  number  of  nuclei  in  the  oogonium  greatly 
exceeding  the  number  of  oospheres  formed.  The  oospheres  at 
maturity  are,  however,  uninucleate.  To  explain  the  disappear- 
ance of  the  remainder  of  the  nuclei  two  theories  have  been 
advanced.  Hartog  maintains  that  nuclear  fusions  many  times 
repeated  reduce  the  number  until  only  one  nucleus  remains  in 
each  oosphere.  Trow  and  Davis  believe  that  the  supernumerary 
nuclei  degenerate.  Occasionally  fully  formed  oospheres  are 
found  to  be  binucleate.  Hartog  considers  such  cases  as  merely 
the  last  stage  in  the  general  nuclear  fusion.  Davis  feels  that 
they  represent  those  instances  in  which  two  nuclei  happen  to  lie 
near  a  coenocentrum,  and  are  thus  both  saved  from  degeneration. 


SAPROLEGNIALES  155 

Trow  believes  that  they  constitute  evidence  of  a  true  fertihza- 
tion.  He  states  that  one  of  the  nuclei  in  each  binucleate  oosphere 
is  a  male  nucleus  introduced  by  an  antheridial  tube.  He  says 
that  while  the  fully  formed  naked  oosphere  is  uninucleate,  young 
oospores  with  very  delicate  membranes  contain  two  nuclei  one 
of  which  is  often  found  in  the  periphery  near  the  fertihzation 
tube,  and  older  oospores  with  thicker  membranes  each  contain 
a  single  large  central  nucleus. 

It  is  generally  known  that  certain  species  of  the  group  are 
apandrous,  the  antheridia  never  being  formed,  and  even  Trow 
agrees  that  in  such  cases  fertilization  does  not  occur.  In  the 
light  of  the  fact  that  degeneration  of  the  typical  sexual  process 
appears  to  be  taking  place  in  various  groups  of  the  fungi,  it  seems 
not  illogical  to  conclude  from  the  data  at  hand  that  conditions 
differ  in  different  species,  and  to  agree  with  the  conclusion  of 
Trow  that  some  species  {S.  dioica)  are  typically  sexual,  others 
(*S.  thureti)  obviously  apogamous,  while  between  the  extremes 
intermediate  conditions  exist.  In  recent  years  a  true  fertiliza- 
tion has  been  described  by  Claussen  (1908)  for  Saprolegnia 
monoica,  by  Miicke  (1908)  for  AcJilya  -pohjandra,  by  Patterson 
(1927)  for  Achlya  colorata,  and  by  Kasanowsky  (1911)  for 
Aphanomyces  laevis,  while  in  the  related  groups,  Pythiaceae, 
Leptomitaceae,  and  Peronosporaceae,  the  antheridia  apparently 
function  in  all  cases. 

In  apogamous  species  the  spores  developed  in  the  oogonium 
might  well  be  termed  aboospores  since  they  correspond  to  the 
azygospores  of  the  Zygomycetes.  The  number  of  oospores  in 
an  oogonium  is  extremely  variable  in  some  species  while  rather 
constant  in  others.  In  certain  species  of  Saprolegnia  and  Achlya 
an  oogonium  not  infrequently  contains  fifty  or  more  oospores, 
though  the  number  is  usually  much  less.  In  the  genera  Pythiop- 
sis,  Dictyuchus,  Aphanomyces,  Brevilegnia,  Geolegnia,  and 
Leptolegnia  a  single  oospore  is  usually  developed,  these  genera  indi- 
cating in  this  respect  evolution  toward  the  condition  in  the 
higher  Oomycetes.  After  a  period  of  rest  germination  of  the 
oospore  occurs.  The  inner  membrane  of  the  spore  is  pushed 
out  through  a  crack  in  the  outer  wall  and  develops  into  a  germ 
tube.  This  tube  may  come  into  contact  with  available  nutri- 
ment, put  out  rhizoids,  and  develop  directly  into  a  new  plant. 
More  often  after  a  brief  period  of  elongation  it  cuts  off  at  its 
apex  a  sporangium  typical  of  the  genus,  and  forms  sporangiospores. 


156  THE  LOWER  FUNGI— PIIYCOMYCETES 

The  single  nucleus  of  the  mature  oospore  undergoes  repeated 
divisions  to  furnish  the  nuclei  for  the  sporangiospores,  these 
divisions  taking  place,  in  some  species  at  least,  before  germina- 
tion occurs. 

The  most  recent  monographs  on  the  family  are  those  of  Coker 
(1923)  and  von  Minden  (1912),  but  those  of  Schroter  (1893), 
Fischer  (1892),  and  Humphrey  (1893)  will  also  be  found  valuable. 
Since  a  number  of  papers  have  appeared  recently  containing 
descriptions  of  new  genera  and  species  no  one  of  the  larger 
monographs  is  wholly  complete.  As  a  result  of  an  investigation 
of  the  soil  for  "water  moulds"  Coker  and  his  co-workers  have 
described  a  number  of  forms  which  in  the  Hght  of  earlier  work 
are  extremely  atypical.  Several  new  genera  {Calyptralegnia, 
Geolegnia,  Brevilegnia,  Protoachlya,  and  Isoachlya)  have  been 
described.  In  some  cases  these  are  based  on  forms  intermediate 
in  type  between  members  of  older  established  genera.  While 
the  writer  is  unprepared  in  the  light  of  present  knowledge  to 
accept  all  of  these  genera  as  good,  it  seems  best  to  incorporate 
them  in  the  key,  and  give  them  adequate  discussion  in  order 
that  the  student  may  orient  himself  clearly  regarding  the  present 
status  of  the  group. 

Key  to  Genera  of  Saprolegniaceae 

I.  Sporangiospores  normally  encysting  within  the  sporangium. 
A.  Oogonium  containing  more  than  one  oosphere. 

1.  Sporangia  extremely  rare;  behavior  of  sporangiospores  very 

imperfectly  known;  their  germination  in  situ  by  germ  tube 
occurring  at  least  at  times;  oogonium  provided  with  an 
exceptionally  thick,  prominently  pitted  wall. 

1.  Aplanes,  p.  158 

2.  Sporangia  abundant;  encysted  sporangiospores  germinating 

after  their  escape  from  the  sporangium;  wall  of  oogonium 

not  of  unusual  thickness. 

a.  Dehiscence  of  sporangium  not  occurring  at  a  definite 
point;  the  wall  either  deliquescent  throughovit,  or 
ruptured  by  internal  pressure  so  that  a  wide  opening 
of  indeterminate  position  results;  sporangiospores 
germinating  by  swarmspores  or  by  germ  tubes; 
oosphere  eccentric. 

2.  Thraustotheca,  p.  100 

6.  Dehiscence  of  sporangium  accomplished  by  breaking 
off  of  an  apical  cap,  leaving  a  wide  opening  through 
which   the  swelling  spores  escape  intermittently  in 


SAPROLEGNIALES  157 

groups  prior  to  their  germination  bj^  swarm  spores; 
oosphere  typicallj'  centric  with  many  oil  drops. 

3.  Calyptralegnia,  p.  162 

B.   Oogonium  containing  a  single  eccentric  oosphere. 

1.  Mycelium  well  developed,  of  the  usual  water  mould  type,  not 
depauperate;  sporangiospores  after  encysting  within  the 
sporangium,  escaping  from  the  cysts  as  laterally 
biciliate  swarmspores  and  passing  to  the  outside  through 
individual  pores  in  the  sporangial  wall;  the  emptied  poly- 
hedral cyst  walls  giving  the  emptied  sporangium  the  aspect 
of  a  net. 

4.  Dictyuchus,  p.  162 

'2.  Mycelium  depauperate,  forming  a  dense  opaque  mat. 

a.  Sporangium  in  form  and  method  of  dehiscence  corre- 
sponding to  Thrausiotheca;  encysted  sporangiospores 
extremely  variable  in  size  and  shape;  germination  by 
swarmspores  or  by  germ  tubes  in  different  species. 

5.  Brevilegnia,  p.  164 

6.   Sporangium  containing  a  single  row  of  large  spherical 
to  elongate  encysted  spores  which  are  finally  freed  by 
disintegration  of  the  persistent  sporangial  wall  and 
/  germinate  by  germ  tube;  swarmspores  unknown. 

6.  Geolegnia,  p.  164 

II.  Sporangiospores  not  normally  encysting  within  the  sporangium,  escap- 
ing through  a  terminal  pore. 

A.  Sporangia  typically  ovoid,  not  proliferating;  swarmspores  mono- 

planetic,  with  terminal  cilia;  oogonia  usually  1-spored. 

7.  Pythiopsis,  p.  165 

B.  Sporangia  clavate  to  cylindrical;  swarmspores  diplanetic. 

1.  Sporangia  usually  clavate;  swarmspores  arranged  irregularly 
in  the  sporangium;  oogonium  usually  several-  to  many- 
spored. 

a.  Swarmspores  escaping  separately  from  the  sporangium, 
not  encysting  at  its  mouth. 

(1)  Sporangia  proliferating,  the  secondary  sporangia 

not  developed  on   lateral   branches   below    the 
primary. 

8.  Saprolegnia,  p.  167 

(2)  Secondary  sporangia  arising  cither  by  prolifera- 

tion or  by  lateral  branching. 

9.  Isoachyla,  p.  167 

6.  Some  or  all  of  the  swarmspores  encysting  at  the  mouth 
of  the  sporangium. 

(1)  All  of  the  spores  encysting;  sporangia  not  pro- 
liferating, the  secondary  developed  as  lateral 
branches  below  the  primary. 

10.  Achlya,  p.  167 


158  THE  LOWER  FUNGI— PHYCOMYCETES 

(2)  Some  of  the  spores  encysting  in  an  irregular  clump, 
the  others  swimming  away  at  once;  secondary 
sporangia  usually  developed  as  lateral  branches 
below  the  primary  but  sometimes  formed  by 
proliferation. 

11.  Protoachlya,  p.  167 

2.  Sporangia  not  clavate;  oogonia  usually  1-spored. 

a.  Sporangium    of    very    irregular    and    complex    form; 

consisting  of  a  much  inflated  branching  basal  portion 
in  which  swarmspores  are  formed  in  several  series, 
and  a  slender  elongate  filamentous  apical  portion  in 
which  they  are  cut  out  in  a  single  row;  the  filamentous 
portion  acting  as  an  exit  tube  through  which  all  the 
swarmspores  pass;  swarmspores  encysting  at  the 
mouth  of  the  tube  as  in  Aphanomyces. 

12.  Plectospira,  p.  167 

b.  Sporangium      cylindrical,      thread-like;      swarmspores 

arranged  in  a  single  row  in  the  sporangium. 

(1)  Swarmspores    encysting    at    the    mouth    of    the 

sporangium  as  in  Achlya. 

13.  Aphanomyces,  p.  167 

(2)  Swarmspores  escaping  separately  as  in  Saprolegnia. 

14.  Leptolegnia,  p.  170 

1.  Aplanes  de  Bary  (1888:  650). 

This  genus,  as  conceived  by  de  Bary,  is  characterized  by  the 
aplanetic  nature  of  the  sporangiospores,  which,  instead  of  leaving 
the  sporangium,  germinate  in  situ  by  germ  tubes.  In  other 
essential  respects  the  genus  as  described  by  de  Bary  resembles 
Achlya.  He  founded  the  genus  on  a  single  species,  Aplanes 
androgynus  (Archer)  Humphrey  (Fig.  55).  This  species  is  rela- 
tively rare,  and,  though  reported  five  times  from  various  parts  of 
Europe,  is  as  yet  unknown  from  North  America.  The  genus 
has  long  been  regarded  as  doubtful  (Weston,  1919:  289),  the 
sporangia  being  extremely  uncommon,  and  their  behavior  having 
been  variously  described. 

In  recent  years  Coker  (1923:  76;  1927:  216)  has  considerably 
modified  the  generic  concept,  and  has  included  two  additional 
species,  A.  treleaseanus  (Humphrey)  Coker  and  A.  turfosus 
(v.  Minden)  Coker,  representing  transfers  from  Achlya  and 
Saprolegnia.  He  feels  that  observations  made  on  the  sporangial 
stage  of  these  three  species  have  been  too  few  and  contradictory 
to  justify  conclusions,  but  regards  the  sexual  stage  as  distinctive. 
The  wall  of  the  oogonium  is  said  to  be  thicker  than  in  other 


SAPROLEGNIALES 


159 


members  of  the  family  (reaching  four  microns),  and  is  prom- 
inently pitted.  The  antheridial  branches  arise  immediately 
below  the  oogonium,  or  if  the  oogonia  occur  in  chains,  as  is  fre- 
quently the  case  in  A.  androgynus,  then  the  antheridial  branch 
arises  near  the  top  of  one  oogonium  and  applies  itself  to  the 
next  one  above.  Since  a  fourth  species,  Saprolegnia  hypogyna 
Pringsheim,  with  a  similar  sexual  stage  is  retained  by  Coker  in 


Fig.  55. —  (a-c)  Aplanes  androgynus  (Archer)  Humphrey,  (a)  Tip  of  oogon- 
ium showing  single  germinating  oospore.  (6)  Two  oogonia  with  oospores  and 
pitted  wails;  antheridial  branch  in  each  case  attached  to  the  cell  beneath,  (c) 
Sporangium  in  which  sporangiospores  are  germinating  in  situ;  and  two  oogonia 
each  accompanied  by  an  antheridial  branch,  (d)  Aplanes  treleasanus  (Hum- 
phrey) Coker.  Oogonium,  oospores,  and  antheridial  branches,  {a-c,  after 
deBary  1888;  d  after  Coker  19-23.) 

Saprolegnia  on  the  basis  of  sporangial  characters  the  status  of 
the  genus  Aplanes  would  seem  to  be  doubtful  at  best.  Coker 
states  in  the  case  of  A.  treleaseanus,  that  though  the  sporangio- 
spores usually  germinate  in  situ  by  tube,  they  sometimes  emit 
swarmspores  as  in  Achlya  or  more  rarely  as  in  Dictyuchus.  Fur- 
ther investigation  of  the  sporangial  stage  of  the  species  incorpo- 
rated in  Aplanes  is  desirable,  and  may  result  in  the  abandonment 


IGO 


THE  LOWER  FUNGI— PHYCOMYCETES 


of  the  genus  and  the  inclusion  of  these  species  in  Achlya  and 
Saprolegnia.  It  should  be  emphasized  in  this  connection  that 
the  sporangiospores  of  various  members  of  the  family  may  ger- 
minate in  situ  under  certain  adverse  environmental  conditions. 

2.  Thraustotheca  Humphrey  (1893:  131). 

Until  recently  the  type  species,  T.  clavata  (de  Bary)  Humphrey, 
comprised  the  genus.  Although  relatively  rare  it  occurs  both 
in  Elurope  and  America,  and  has  been  studied  by  various  investi- 
gators.    Earlier  workers   (Humphrey,    1893:   131)  believed  the 


Fig.  56. — Thraustotheca  clavata  (do  Bary)  Humphroy.      («)    Mature  sporangium. 
(b)   Escape  of  sporangiospores  (After  IVenton  1918.) 


sporangial  wall  to  be  very  fragile,  and  described  the  encysted 
sporangiospores  as  escaping  only  by  its  disintegration.  This  view 
has  been  taken  also  by  Coker  and  Hyman  (1912:  88).  On  the 
other  hand  Weston  (1918:  160)  finds  that  swelling  of  the  spores, 
due  to  imbibition  of  water,  causes  an  internal  pressure  which 
ruptures  a  normally  thick  sporangial  wall  (Fig.  56).  The  open- 
ing which  results  is  usually  large  and  may  occur  at  any  point. 
The  spores  thus  freed  then  germinate,  some  by  germ  tube,  others 
by  emission  of  a  reniform,  laterally  biciliate  zoospore  (Fig.  57). 
The  genus  at  present  contains  one  other  species,  T.  primoachlya 
Coker  &  Couch  (1924:  197).     In  it  the  sporangium  is  said  to 


SAPROLEGNIA  LES 


161 


function  at  times  as  in  Achlya.     A  third  species  referred  to  the 
genus  as   T.  achhjoides  Coker  &  Couch   (1923:  112)  has  since 


I-  no 


Fig.  57. —  Thraustothcca  clavata  (de  Bary)  Humphrey,  {a-c)  An  unusually 
small  sporangium,  showing  delimitation  and  escape  of  sporangiospores.  (d-f) 
Liberation  of  swarmspore  from  sporangiospore.  {g,  s)  Germination  of  cysto- 
spore  (encysted  swarmspore)  by  germ  tube,  {h)  Cystospore  forming  dwarf 
sporangium,  (n)  Two-spored  dwarf  sporangium,  (p)  Oogonium  accompanied 
by  antheridial  branch.      {After  Weston  1918.) 

been  made  the  basis  of  the  genus  Calyptraleg7iia  Coker  (1927: 
219);  while  a  fourth  species,   T.  unisperma  Coker  &  Braxton 


162  THE  LOWER  FUNGI— PHYCOMYCETES 

(1926:  140)  and  a  variety  T.  unisperma  var.  UtoraliH  Coker  & 
Braxton  (1926:  141)  have  been  transferred  to  Brevilegnia  (Coker 
1927:213). 

3.  Calyptralegnia  Coker  (1927:  219). 

This  most  recently  described  genus  of  the  family  is  based  on  a 
single  species,  C.  achlyoides,  which  had  been  described  earlier 
as  Thraustotheca  achlyoides  Coker  &  Couch  (1923:  112).  The 
species  was  isolated  from  the  soil.  Though  it  is  not  in  all 
respects  a  typical  Thraustotheca  it  would  seem  to  fall  very  near 
that  genus,  and  its  removal  will  be  questioned  by  some  students. 

In  Calyptralegnia,  as  the  genus  is  characterized  by  Coker,  the 
oosphere  is  typically  centric,  and  in  dehiscence  of  the  sporangium 
an  apical  cap  or  segment  falls  away  exposing  the  spores,  which 
then  swell  and  emerge  in  successive  groups.  Since  this  type 
of  dehiscence  has  not  been  previously  described,  and  may  prove 
inconstant,  the  validity  of  the  genus  is  in  question  until  the 
species  has  been  more  extensively  investigated. 

4.  Dictyuchus  Leitgeb  {Bot.  Zeitung,  26:  502,  1868). 

This  is  a  small  but  extremely  interesting  genus.  Four  named 
species,  D.  magnusii  Lindstedt  (Humphrey,  1893:  132),  D.  sterile 
Coker  (1923:  151),  D.  achlyoides  Coker  (1927:  218),  and  D.  mono- 
sporus  Leitgeb  (Couch,  1924  b:  116)  as  well  as  two  unnamed 
species  (Fig.  58)  studied  by  Weston  (1919:  287)  and  Coker  and 
Braxton  (1926:  144)  respectively  have  been  reported  from  North 
America.  The  genus  is  discussed  by  Coker  (1923),  and  reference 
made  to  a  few  additional  forms  known  abroad.  Except  in  the 
doubtful  species,  D.  polysporus  Lindstedt  the  oogonia  are  mono- 
sporic.  The  genus  is  outstanding  from  the  fact  that  both 
heterothalHc  (Couch,  1924  b:  116)  and  homothalhc  (Coker  and 
Braxton,  1926:  144)  strains  have  been  demonstrated  to  exist. 
The  work  of  Couch  on  heterothalhsm  is  being  continued  and  may 
be  expected  to  result  in  a  better  understanding  of  forms  known 
thus  far  only  in  the  sporangial  condition.  In  other  genera  of 
the  family  heterothalhsm  is  as  yet  unknown  except  in  a  single 
species  of  Achlya  (Coker,  1927:  207). 

The  genus  Dictijuchus  is  characterized  chiefly  by  the  behavior 
of  the  sporangiospores  which  after  encysting  in  the  sporangium, 
escape  from  the  cysts  through  individual  pores  in  the  sporangial 
wall  and  swim  away  as  reniforni  laterally  biciliate  zoospores. 


SAPROLEGNIALES 


163 


The  empty  polyhedral  cyst  walls  give  the  emptied  sporangium 
the  aspect  of  a  net ;  hence  the  genus  name.  The  sporangia  are 
usually  fusiform,  new  ones  being  formed  in  basipetal  succession 


Fig.  oS.^Dictyuchus  sp.  (a)  Two  successively  formed  sporangia,  the  terminal 
one  empty  and  showing  the  "cell  net"  structure,  the  second  still  containing  the 
spores,  (b)  An  atypical  sporangium  developed  from  a  starved  hypha,  showing 
incomplete  contact  of  adjacent  spores,  (c)  Germination  of  sporangiospores 
in  situ,  (d-p)  A  series  of  drawings  illustrating  "successive  zoospore"  emer- 
gence, (d,  e)  Escape  from  sporangium.  (/,  g)  First  motUe  period;  spore 
reniform  and  biciliate.  {h)  Encysted  zoospore.  (A;)  Second  emergence, 
(m,  n)  Second  swarming  period;  same  type  as  first,  (p)  Final  encystment  and 
germination.      {After  Weston  1919.) 

or  by  sympodial  branching.  It  is  of  interest  to  note  that  they 
frequently  fall  away  from  each  other  and  from  the  hypha,  and 
he  free  in  the  water.  This  deciduous  character  of  the  sporangium 
unusual   in   this   order,   though   common   in   the   next.     Its 


IS 


164  THE  LOWER  FUNGI— PHYCOMYCETES 

function  in  this  case  is  not  clear.  In  D.  achhjoides  the  sporangia 
which  appear  first  are  said  by  Coker  to  free  their  spores  as  in 
Achlya,  while  those  which  form  later  are  typical  of  Dictyuchus. 
The  achlyoid  condition  has  not  been  reported  in  other  species. 

5.  Brevilegnia  Coker  &  Couch  (Coker,  1927:  207). 

In  addition  to  the  type  species,  B.  subclavata  Couch  (1927:  229) 
the  genus  at  present  includes  B.  unisperma  Coker  &  Braxton 
(Coker,  1927:  213),  B.  unisperma  var.  litoralis  Coker  &  Braxton 
(Coker,  1927:  213),  B.  unisperma  var.  montana  Coker  (1927:  213) , 
B.  unisperma  var.  delica  Coker  (1927:  214),  B.  linearis  Coker 
(1927:  214),  B.  bispora  Couch  (1927:  228),  and  B.  diclina  Harvey 
(1927:  245).     All  of  these  have  been  found  only  in  the  soil. 

As  indicated  in  the  key  to  genera  this  genus  differs  from 
Thrav^totheca  chiefly  in  that  the  oogonium  is  monosporic.  The 
sporangial  stage  here  is  essentially  the  same  as  in  that  genus 
though  the  sporangiospores  are  strikingly  variable  in  size  and 
shape.  The  mycelium  forms  a  dense  opaque  mat;  the  well  devel- 
oped growth  typical  of  water  moulds  having  been  lost,  presumably 
as  a  result  of  the  changed  environment.  The  sporangiospores 
germinate  in  some  cases  by  germ  tube.  In  one  species,  B. 
bispora,  the  sporangia  first  formed  germinate  as  in  Achlya.  In 
view  of  the  variation  which  exists  in  the  family  some  students 
will  prefer  to  widen  the  limits  of  Thraustotheca  to  include  these 
forms  rather  than  to  recognize  this  new  genus. 

6.  Geolegnia  Coker  (in  Harvey  1925:  153). 

The  genus  contains  only  the  two  species  on  which  it  was 
based,  G.  injiata  Coker  &  Harvey  and  G.  septisporangia  Coker 
&  Harvey  (Harvey,  1925:  153;  1928:  552),  both  isolated  from 
the  soil.  The  mycelium  forms  a  dense  opaque  mat  as  in  the  pre- 
ceding genus.  The  sporangial  stage  is  characteristic,  zoospores 
being  wholly  unknown. 

Very  large  thick-walled  sporangiospores  lie  encysted  in  a 
single  row  giving  in  early  stages  an  aspect  recalling  Leptolegnia. 
The  sporangium  is  inflated  at  intervals  or  collapsed  between 
contiguous  spores  in  such  a  manner  as  to  appear  almost  monili- 
form  at  maturity.  The  spores  are  freed  by  disintegration  of 
the  sporangial  wall,  and  germinate  by  tube.  The  oogonium  is 
monosporic,  the  oosphere  is  eccentric,  and  the  antheridia  are 
androgynous. 


SAPROLEGNIALES 


165 


7.  Pythiopsis  de  Bary  (1888:  632). 

The  type  species,  P.  cymosa  de  Bary  (Fig.  59),  has  been  studied 
in  North  America  by  Humphrey  (1893:  113)  and  Coker  (1923: 
18).  Two  other  species,  P.  humphreyana  Coker  (1914:  292) 
and  P.  intermedia  Coker  &  Harvey  (Harvey  1925:  157)  have 
been  added  to  the  genus  in  recent  years.  The  sporangia  of  P. 
cymosa  are  ovoid  and  recall  those  of  Pythium,  but  in  the  other 
species  great  variation  occurs,  the  sporangium  sometimes  being 
leongate  as  in  Ac.hlya.     The  swarmspores  as  they  emerge  from  the 


Fig.  59.^ — Pythiopsis  cymosa  de  Bary.  (a)  Cymose  development  of  swarm- 
sporangia,  (b)  Oogonium  accompanied  by  antheridia.  (c)  Mature  oospore. 
(After  de  Bary  1888.) 


sporangium  in  this  genus  are  pyriform  and  terminally  biciliate. 
While  monoplanetic  as  regards  form  they  apparently  have  been 
observed  to  swim  twice  in  P.  intermedia,  thus  recalling  the 
phenomenon  of  repeated  zoospore  emergence  described  in  Dicty- 
iichus  by  Weston. 

The  genus  differs  from  Pijthium  in  the  form  of  the  swarmspore, 
which  is  reniform  and  laterally  biciliate  in  that  genus,  in  the  fact 
that  the  oogonia  though  typically  monosporic  sometimes  contain 
two  or  more  oospores,  in  the  much  broader  hyphae,  and  in  the 
manner  of  sporangial  germination. 


166 


THE  LOWER  FUNGI— PHYCOMYCETES 


Fig.  60. — Saprolegnia  spp.  (a)  Proliferation  of  sporangia,  (b)  An  oogonium 
encased  in  the  walls  of  two  emptied  sporangia:  a  less  common  phenomenon  of 
proliferation,  (c)  Mature  swarmsporangium.  (d)  Swarmspores  escaping  from 
a  terminal  pore,  (e)  Six  successive  stages  (from  top  to  bottom)  in  diplanetism. 
(h)  Chlamydospores.  (o,  h,  and  h,  after  Coker  192S;  c  and  d,  after  Atkinson  1909; 
e,  after  Marshall  Ward  1883.) 


SAPROLEGNIALES  167 

8.  Saprolegnia  Nees  von  Esenbeck  (in  Carus  1823:  514). 

The  genus  contains  about  twenty  species  some  of  which  are 
common  and  widely  distributed  (Fig.  60).  Keys  for  specific 
separation  are  given  by  Humphrey,  Coker,  and  von  Minden. 
Consult  these  authors  for  more  detailed  information. 

9.  Isoachlya  Kauffman  (1921:  231). 

This  genus  was  recently  erected  to  include  several  puzzling 
species  whose  characters  place  them  on  the  border  line  between 
Achlya  and  Saprolegnia.  The  secondary  sporangia  arise  either 
by  proliferation  or  by  lateral  branching,  both  modes  not  infre- 
quently being  represented  on  the  same  main  hypha.  The 
swarmspores  are  definitely  diplanetic.  As  constituted  by  Kauff- 
man the  genus  included  I.  toruloides  I\auff.  &  Coker  (Fig.  61), 
/.  paradoxa  (Coker)  Kauff,  (Achlya  paradoxa  Coker  1914),  and 
7.  fnonilifera  (de  Bary)  Kauff.  (Saprolegnia  monilifera  de  Bary, 
1888:  629).  Coker  (1923:  85)  has  added  two  new  species,  7. 
unispora  Coker  &  Couch  and  7.  eccentrica  Coker.  Moreover, 
he  has  removed  the  species  7.  paradoxa,  making  it  the  basis 
of  the  new  genus  Protoachlya  Coker. 

10.  Achlya  Nees  von  Esenbeck  (in  Carus  1823:  514). 

This  is  the  largest  genus  of  the  family,  embracing  twenty-five 
or  thirty  species  (Fig.  61).  For  specific  separations  consult  the 
keys  given  by  Humphrey,  Coker,  and  von  Minden. 

11.  Protoachlya  Coker  (1923:  90). 

This  genus  is  based  on  a  single  species,  P.  paradoxa  Coker, 
removed  by  him  from  Isoachlya. 

12.  Plectospira  Drechsler  (1927:  294). 

This  genus  includes  P.  myriandra  Drechsler  and  P.  gemmifei'a 
Drechsler  (1929),  weakly  parasitic  on  tomato  and  sugar  cane 
rootlets  in  the  greenhouse.  The  oogonium  is  terminal  or  inter- 
calary, and  may  be  accompanied  by  as  many  as  sixty-five  anther- 
idia.  The  sexual  and  asexual  organs  are  well  figured  by  the 
author. 

13.  Aphanomyces  de  Bary  (Jahrh.  Wiss.  BoL,  2:  179,  1860). 

In  the  taxonomic  treatment  by  Coker  (1923:  160)  eight  species 
are  described.  Of  these  A .  laevis  de  Bary  is  the  best  known.  The 
genus  corresponds  to  Achlya  in  the  same  sense  in  which  Leptoleg^iia 


168 


THE  LOWER  FUNGI—PHYCOMYCETES 


Fig.  61. —  (a-f)  AchJya  spp.  g.  IsoaMya  toruloides  Kauffman  and  Coker. 
(a-c)  Oogonia  and  antheridia:  diffonuit  stages  in  delimitation  of  oospheres. 
(d)  Oogonium  with  only  a  single  oospliere.  (e)  Sporangium  freeing  its  spores 
through  an  apical  pore;  the  spores  encysting  there  and  later  escaping  from  the 
cyst  walls  as  reniform,  biciliate,  naked  swarmsjiores.  (/)  Mature  sporangium 
with  spores  already  delimited,  (g)  A  cluster  of  empty  sporangia  which  devel- 
oped in  the  cymose  manner  with  an  accompanying  instance  of  proliferation. 
{a~d,  after  Cornu  1872;  e  and  /,  after  de  Bary  1887;  g,  after  Coker  1923.) 


SAPROLEGNIALES 


169 


corresponds  to  Saprolegnin.  The  thread-like  sporangium,  con- 
taining a  single  row  of  elongate  zoospores,  and  the  one-sporcd 
oogonia  constitute  the  chief  points  of  difference  (Figs.  62  and  63). 
A  parasitic  tendency  in  the  genus  is  pronounced.  Several 
species  are  facultative  parasites,  and  A.  phycophilus  de  Bary, 
occurring  in  Spirogyra  and  Zygnema  is  apparently  obligate  in  its 


Fig.  62.- — Aphanomyccs  stellatus  de  Bary.  (a)  Portion  of  mature  swarmspo- 
rangium  showing  plasma  portions  forming  swarmspores.  (h)  Plasma  portions 
escaping  and  collecting  as  spherical  encysted  spores  at  the  apex  of  the  sporan- 
gium, (c)  Spherical  mass  of  spores  at  apex  of  emptied  sporangium,  (d) 
Later  stage;  most  of  the  spores  gone  leaving  emptied  cyst  walls,  (e)  Mature 
swarmspores.  (/)  Double  swarmspores  dividing,  (g)  Germination  of  spore 
at  close  of  second  encystment  to  form  mycelium.     {After  de  Bary  1860.) 


parasitism.  Many  papers  have  appeared  in  recent  years  in 
reference  to  the  parasitic  habit  of  A.  euteiches  Drechsler  which 
causes  a  root  rot  of  various  plants.  This  species  has  been 
reported  on  peas  (Haenseler,  1926:  467;  Jones  and  Drechsler, 
1925:  293),  tomatoes  (Drechsler,  1927:  287),  and  other  hosts 
(Linford,  1927:  133).  Recently  another  speces,  A.  raphani  Ken- 
drick  (1927:   19),  has  been  reported  as  parasitic  in  roots  of 


170 


THE  LOWER  FUNGI— PHYCOMYCETES 


radish.  Another,  A.  parasiticus  Coker  (1923:  165),  attacks 
Achlya,  and  others  have  been  described  by  Drechsler  (1928;  1929) 
from  oats,  tomatoes,  and  beets. 

Two  somewhat  imperfectly  known  genera,  Aphanomycopsis 
Scherffel  (1925)  and  Sommerstorffia  Arnaudow  (1923),  fall  near 
Aphanomyces.  In  both  of  these  genera  the  intramatrical 
mycehum  is  characteristically  swollen  and  distorted,  and  both 
are  based  on  parasitic  species. 


Fig.  63. — Aphanomyces  steUatus  de  Bary.  (o)  Hyphae  bearing  oogonia 
and  antheridia.  (6)  Stellate  oogonium  with  a  single  spherical  oosphere.  (c) 
Germinating  oospores.     {After  de  Bary  1860.) 

The  genus  Aphanomycopsis  contains  the  single  species,  A. 
bacillariacearum  Scherffel,  occurring  in  Pinnularia,  one  of  the 
diatoms. 

The  genus  Sommerstorffia  was  based  on  S.  spinosa  Arnaudow 
parasitic  in  the  body  of  Rotiferae.  The  fungus  has  been  collected 
in  America  and  has  been  discussed  and  figured  by  Sparrow  (1929). 

14.  Leptolegnia  de  Bary  (1888:  631). 

Until  recently  the  type  species,  L.  caudata  de  Bary  constituted 
the  genus.  It  has  been  reported  from  America  only  by  Coker 
(1923:  158),  but  has  been  studied  in  Europe  by  several  investi- 


SAPROLEGNIALES  1 7 1 

gators  since  de  Bary.  (v.  Minden,  1912:  533.)  Two  additional 
species  isolated  from  the  soil,  L.  subterranea  Coker  &  Harvey 
(Harvey,  1925:  158)  and  L.eccentrica  Coker  (1927:  215)  have  been 
recently  described. 

Doubtful  Genus 

Jaraia  Nemec  (1913). 

This  very  imperfectly  understood  genus  is  known  only  from 
the  original  paper  of  Nemec.  It  was  based  by  him  on  a  single 
species,  J.  salicis  Nemec,  isolated  from  enlargements  on  hving 
roots  of  Salix,  and  is  regarded  by  him  as  an  undoubted  member 
of  this  family.  The  sporangia  and  oogonia  are  extremely 
irregular  in  form.  The  sporangia  are  provided  with  several  exit 
tubes.  The  oogonia  are  many-spored.  Further  study  will  be 
necessary  before  the  relationships  of  the  form  are  clearly  under- 
stood. It  is  placed  in  the  Blastocladiaceae  by  Gaumann  (1926: 
58). 

Leptomitaceae 

This  relatively  small  family,  embracing  approximately  fifteen 
species  in  six  genera,  includes  such  a  wide  diversity  of  forms 
that  doubt  to  its  phylogenetic  unity  will  probably  arise  in  the 
mind  of  the  student.  The  members  of  the  group  agree,  never- 
theless, in  several  seemingly  essential  respects.  Their  mem- 
branes are  of  cellulose,  their  zoospores  are  biciliate,  and  their 
hyphae  are  quite  definitely  and  characteristically  constricted. 
As  a  result  of  the  presence  of  the  constrictions  the  hyphae  have  a 
segmented  appearance.  Strongly  refractive  granules  of  cellulin, 
a  carbohydrate  material  probably  allied  to  cellulose,  are  present 
in  the  protoplasm  and  provide  one  of  the  most  characteristic 
features  of  the  group.  These  granules  are  especially  prominent 
near  the  constrictions,  and  at  times  pass  into  them  forming 
definite  plugs  with  the  aspect  of  thick  septa.  This  occurs 
particularly  in  the  cutting  off  of  the  sporangia  and  sexual  organs. 
Later  the  plugs  may  disappear.  True  septa  are  not  formed.  In 
the  genus  Gonapodya  wholly  similar  constrictions  and  cellulin 
plugs  occur,  and  by  some  authors  the  genus  is  incorporated 
in  this  family.  A  consideration  of  all  the  characters  of  the 
genus  indicates  that  it  is  intermediate  in  type  between  the 
Leptomitaceae  and  Blastocladiaceae,  and  in  the  present  treat- 
ment it  is  placed  in  the  latter  family  on  account  of  its  non- 


172  THE  LOWER  FUNGI— PHYCOMYCETES 

cellulose  membranes  and  uniciliate  zoospores.  As  it  is  known 
only  in  the  sporangial  condition  it  cannot  be  assigned  to  either 
family  with  certainty  (see  p.  130). 

In  the  habit  of  growth  and  general  morphology  of  the  thallus 
the  family  is  allied  on  one  side  through  Leptomitus  and  Apodachlya 
to  the  Saprolegniaceae,  and  on  the  other  through  Rhipidium  and 
Araiospora  to  the  Blastocladiaceae.  In  its  sexual  stage  the 
group  shows  relationship  with  the  Pythiaceae.  The  protoplasm 
of  the  oogonium  is  differentiated  into  ooplasm  and  periplasm, 
fertilization  occurs,  and  a  single  oospore  is  formed. 

The  members  of  the  family  are  typically  aquatic,  and  occur 
as  saprophytes  on  vegetable  substrata.  Few  students  have  con- 
cerned themselves  with  the  group,  the  species  being  in  general 
infrequently  collected  though  apparently  not  uncommon.  The 
monographic  treatment  of  the  group  given  by  Kanouse  (1927) 
is  the  most  complete. 

Key  to  Genera  of  Leptomitaceae 

I.  Thallus  not  differentiated  into  a  stout  trunk  and  slender  l^ranchcs; 
composed  of  cylindrical  hyphae  which  are  definitely  and  characteristi- 
cally constricted  at  intervals,  and  have  consequently  a  segmented 
appearance. 

A.  Zoosporangia   cyHndrical,  not  differing  in  form  from  the  hyphal 

segments;  zoospores  escaping  singly  from  the  sporangium  as  in 

Saprolcgnia. 

1.  Leptomitus,  p.  173 

B.  Zoosporangia  ellipsoidal  to  pyriform  ,  considerably  broader  than 

the    segments    of    the    hyphae;    zoospores    encysting    at   the 
mouth  of  the  sporangium  as  in  Achlya. 

2.  Apodachlya,  p.  173 

II.  Thallus  differentiated  into  a  stout  trunk  and  slender  branches;  the 
latter  usually  definitely  constricted. 

A.  Trunk  more  or  less  definitely  cylindrical,  corresponding  in  form  to 
the  narrower  apical  branches. 

1.  Diameter  of  trunk  not  strikingly  greater  than  that  of  the 

branches;  sporangia  of  one  sort,  smooth  and  broadly 
clavate;    oogonia    pyriform;    oospore    lacking    a    cellular 

envelope. 

3.  Sapromyces,  p.  175 

2.  Diameter  of  trunk  much  greater  tlian  that  of  the  branches; 

sporangia  of  two  sorts,  one  smooth,  the  other  more  or  less 
ornamented  with  spines  or  finger-like  processes;  oogonia 
spherical;  oospore  surrounded  by  a  cellular  envelope. 

4.  Araiospora,  p.  177 


SAPROLEGNIALES  173 

B.   Trunk  not  cj'lindrical. 

1.  Trunk  more  or  less  irregularly  lobed  or  branched,  the  apical 

branches  slender  and  bearing  the  reproductive  cells. 

5.  Rhipidium,  p.  180 

2.  Trunk    broadly    club-shaped    and    essentially    unbranched; 

reproductive  cells  borne  over  its  broadened  distal  end  on 
short  pedicels. 

6.  Mindeniella,  p.  180 

1.  Leptomitus  Agardh  {Sy sterna  Algarum,  p.  47,  1824). 

syn.  Apodija  Cornu  (Bull.  Soc.  Bot.  France,  18:  53,  1871). 

This  genus  contains  a  single  well  known  species,  L.  lacteus 
(Roth.)  Agardh  (Fig.  64),  occurring  usually  in  waters  strongly 
polluted  by  organic  material.  In  favorable  locations,  such  as 
the  drains  from  sugar  factories  or  breweries,  it  often  forms  dense 
masses  of  closely  felted  threads  covering  surprisingly  large  areas. 

The  hyphae  are  of  somewhat  smaller  diameter  at  their  tips 
than  at  their  point  of  attachment  to  the  substratum,  but  are 
essentially  cylindrical.  They  are  constricted  deeply  at  rather 
regular  intervals,  and  appear  consequently  to  be  composed  of 
definite  long  segments.  Branching  occurs  usually  immediately 
below  the  constrictions.  Though  actually  monopodial  it  may 
later  appear  dichotomous. 

The  most  characteristic  feature  of  the  species  is  the  trans- 
formation in  basipetal  succession  of  its  hyphal  segments  to 
sporangia.  The  terminal  segment  frees  zoospores  through  a 
terminal  pore,  the  constriction  at  its  base  being  temporarily 
closed  by  a  cellulin  plug.  Subterminal  segments  in  turn  function 
as  sporangia  freeing  their  zoospores  through  the  constriction 
into  the  previously  emptied  adjacent  segment  from  which  they 
finally  reach  the  outside.  Sometimes  the  subterminal  sporangia 
are  provided  with  lateral  exit  papillae.  Sporangia  differing 
in  form  from  the  segments  do  not  occur.  Sexual  organs  are 
unknown.  The  zoospores  are  freed  as  in  Saprolegriia,  and 
apparently,  as  there,  are  diplanetic 

2.  Apodachlya  Pringsheim  (1883). 

The  hyphae  resemble  those  of  the  preceding  genus,  but  con- 
strictions occur  at  more  frequent  intervals.  Definite  pyriform 
to  broadly  ovoid  sporangia,  considerably  broader  than  the  hyphal 
segments,  are  borne  terminally  (Fig.  65).  Secondary  sporangia 
are  formed  by  sympodial  budding  as  in  Achlya.     Rarely  inter- 


174 


THE  LOWER  FUNGI— PHYCOMYCETES 


calary  sporangia  occur.     The  papilla  of  dehiscence  is  terminal 
or  lateral.     Antheridia  are  unknown  but  monosporous  oogonia 


Fig.  64.- — Leptomitus  lacteus  (Roth.)  Agardh.  (a)  Regularly  constricted 
thread,  showing  three  consecutive  segments  which  have  functioned  as  swarm- 
sporangia;  the  swarmspores  shown  in  motile,  encysted,  and  germinating  stages. 
(6)  Constricted  hypha  showing  swarmspores,  cellulin  plugs,  and  absence  of 
septa.      {After  Pringsheim  1860.) 

apparently  occur.     They  have  not  been  satisfactorily  studied, 
and   are   usually   referred   to   as   "resting   spores."     They   are 


SAPROLEGN I ALES 


175 


terminal  or  intercalary,  and,  in  some  cases  at  least,  germinate 
by  germ  tube.  The  genus  is  small,  embracing  in  the  treatment 
of  Kanouse  (1927:  335)  only  three  species.  The  inclusion  of 
A.  cornpleta  Hymphrey  is  avoided  in  that  its  sporangia  have  not 
been  seen. 


Fig.  65. — Apodachlya  pyrifera  (Zopf)  Pringsheim.  (a)  Constricted  hyphae 
bearing  pyriform  sporangia;  swarmspores  encysting  as  in  Achlya.  {b)  Sporangia 
developed  sympodially.  (c)  Sporangium  with  swarmspores.  {d)  Young 
resting  spore,      (e)  Mature  resting  spore.      {After  Zopf  1888.) 


3.  Sapromyces  Fritsch  (1893;  see  also  1892). 

syn.  Naegelia  Reinsch  (1878);  see  also  Thaxter  (1894). 
Naegeliella  Schroter  (1893). 

In  this  genus  the  thallus  is  differentiated  into  a  trunk  and 
branches,  but  the  trunk  corresponds  in  shape  with  the  branches 
and  is  of  only  slightly  greater  diameter.  It  is  attached  at  its 
base  to  the  substratum,  rhizoids  being  poorly  developed  or  even 
absent.  The  branches  are  definitely  constricted  at  intervals, 
secondary  branches  arising  at  the  apices  of  the  segments.  A 
spreading  thallus  results  which  is  often  extensive.     The  sporangia 


176 


THE  LOWER  FUNGI— PHYCOMYCETES 


are  clavate  to  nearly  cylindrical,  arise  at  the  apices  of  the  segments 
and  appear  single  or  in  whorls.  The  zoospores  are  apparently 
nionoplanetic,  and  usually  escape  directly  through  a  terminal 


Fig.  66. — Sapromyces  androgyriua  Thaxter.  (a)  General  habit  of  small 
plant  bearing  sexual  organs  and  swarmsporangia.  {h)  Swarmsporangia.  (c) 
Two  Gogonia  with  oospores  accompanied  by  antheridia  on  twisted  branches. 
(After  Thaxter  189G.) 


pore.  At  times  a  tendency  toward  the  formation  of  a  thin-walled 
vesicle,  such  as  that  in  Rhipidium,  is  noted,  but  the  membrane 
ruptures  early.  The  oogonium  is  typically  pyriform,  tapering  to 
a  narrowed  base,  and  is  separated  from  the  hyphal  segment  by  a 


SAPROLEGN 1  ALES  177 

prominent  cellulin  plug.  The  oogonial  wall  is  characteristically 
encrusted  with  a  dark-colored  flaky  material.  The  antherid- 
ial  branches  are  characteristically  twisted.  In  *S.  reinschii 
(Schroter)  Fritsch  they  are  diclinous  being  long  and  winding, 
in  S.  androgynous  Thaxter  (Fig.  66)  they  are  androgynous  and 
short.  These  two  species  constitute  the  genus.  The  antherid- 
ium  is  terminal,  and  sends  a  fertilization  tube  to  the  solitary 
spherical  oosphere. 

4.  Araiospora  Thaxter  (1896:  326). 

In  Araiospora  the  thallus  is  definitely  tree-like  (Fig.  67).  A 
prominent  cyhndrical  trunk  of  broad  diameter  is  attached  to 
the  substratum  by  rhizoids,  and  bears  at  its  apex  a  number  of 
relatively  slender  cylindrical  branches  which  in  turn  branch 
repeatedly  in  a  definitely  umbellate  fashion.  The  branches  are 
constricted  at  intervals,  the  secondary  branches  arising  at  the 
distal  end  of  the  segment.  Two  types  of  sporangia  are  formed, 
one  smooth,  the  other  more  or  less  ornamented  with  spines  or 
finger-like  processes.  The  two  differ  also  somewhat  in  shape 
and  size,  the  smooth  type  tending  to  appear  first  and  being  the 
more  slender.  The  genus  at  present  contains  three  species, 
A.  pulchra  Thaxter,  A.  spinosa  (Cornu)  Thaxter,  and  A.  coronnta 
Linder  (1926:  176).  In  the  first  two  species  the  second  type  of 
sporangium  is  barbed  over  its  surface  with  sharp  spines.  In 
A.  coronata  it  is  provided  merely  with  a  crown  of  finger-like 
processes  at  its  apical  end,  and  has  somewhat  the  aspect  of  a 
basidium.  Zoospore  emergence  occurs  as  in  the  preceding  genus, 
a  thin-walled  vesicle  being  sometimes  formed  at  the  mouth  of 
the  sporangium  and  existing  for  a  brief  period.  Oogonia  and 
sporangia  are  often  found  associated,  and  both  occur  in  whorls  or 
umbels.  They  are  separated  from  the  hyphal  segment  by  a 
definite  constriction.  The  oogonium  is  spherical  and  mono- 
sporic.  At  maturity  the  oospore  is  surrounded  by  a  layer  of 
cell-like  compartments  which  gives  it  a  very  characteristic  aspect. 
Antheridal  branches  arise  from  special  segments  and  may  be 
branched.  The  antheridium  is  apphed  near  the  base  of  the 
oogonium.  King  (1903)  studied  A.  pulchra  in  stained  prepara- 
tions and  describes  fertihzation  of  a  uninucleate  oosphere  as 
resulting  from  the  entrance  of  a  single  antheridial  nucleus.  The 
genus  is  considered  taxonomically  by  von  Minden  (1912:  588) 
and  Kanouse  (1927:345). 


178 


THE  LOWER  FUNGI— PHYCOMYCETES 


Fig.  67. — Araiospora  pulchra  Thaxter.  (o)  Plant  bearing  only  oogonia  and 
antheridia.  (b)  Segment  bearing  three  sporangia,  two  of  them  spinose,  the 
other  smooth,  (c)  Two  oogonia,  one  shown  in  optical  section,  the  other  in 
surface  view,  (d)  Oogonium  showing  envelope  of  peripheral  cells  in  process 
of  formation.     (After  Thaxter  1896.) 


SAPROLEGNIALES 


179 


Fig.  68. — Rhipidium  americanum  Thaxter.  (a)  Typical  plant,  the  branches 
showing  occasional  segmentation,  (^e)  Sporangium  with  papilla  of  dehiscence 
extruding  swarmspores  into  a  thin-walled  vesicle  which  finally  ruptures  freeing 
biciliate  swarmspores.  (/)  Oogonium  in  which  the  exospore  is  being  formed 
by  the  periplasm,     (g)  Mature  oospore.     {After  Thaxter  1S96.) 


180  THE  LOWER  FUNGI— PHYCOMYCETES 

5.  Rhipidium  Cornu  (Bui.  Soc.  Bot.  France,  18:  53,  1871). 

In  this  genus,  the  basal  segment  of  the  thallus  is  attached  to 
the  substratum  by  rhizoids,  and  is  often  very  irregular  in  form, 
being  variously  lobed  or  branched  (Fig.  68).  The  lobes  in  turn 
give  rise  to  numerous  slender  cylindrical  branches  which  bear 
the  sporangia  and  sexual  organs.  These  slender  branches  are 
definitely  constricted  at  their  point  of  origin  and  elsewhere, 
especially  in  connection  with  delimitation  of  the  reproductive 
cells.  They  may  be  sympodially  branched  below  the  originally 
terminal  sporangia.  The  form  of  the  sporangium  varies  in  the 
different  species  from  nearly  spherical  to  long  ellipsoidal,  the 
cell  being  always  markedly  broader  than  the  hypha  which  bears 
it.  The  zoospores  pass  from  the  sporangium  into  a  thin-walled 
vesicle  which  tends  to  elongate  and  become  cylindrical  before 
rupturing.  They  are  monoplanetic  and  reniform.  The  oogo- 
nium is  usually  borne  terminally  and  is  fertilized  by  an  anther- 
idium  applied  near  its  base.  The  oospore  is  prominently  areolate 
at  maturity.  The  genus  contains  at  present  four  species,  R.  ameri- 
canum  Thaxter  (1896:  320),  R.  thaxteri  v.  Minden  (1912:  600), 
R.  europaeum  (Cornu)  v.  Minden  (1912:  597),  and  R.  partheno- 
sporum  Kanouse  (1927:  344). 

6.  Mindeniella  Kanouse  (1927:  301). 

The  basal  segment  or  main  axis  of  the  thallus  in  this  genus 
is  broadly  club-shaped  and  essentially  unbranched.  Over  its 
broadened  distal  end  sporangia  and  oogonia  occur  on  short 
pedicels.  They  are  really  sessile  inasmuch  as  they  are  separated 
from  the  basal  segment  only  by  a  constriction  closed  by  a  cellulin 
plug.  The  sporangium  is  large,  pyriform  to  ovoid,  and  some- 
times is  ornamented  with  a  circle  of  spines  about  the  papilla 
of  dehiscence.  The  oogonia  appear  after  the  sporangia  have 
freed  their  zoospores.  They  are  spherical,  thick-walled,  and 
spiny  over  the  entire  surface.  The  oospore  is  spherical,  smooth- 
walled,  and  nearly  fills  the  oogonium.  Antheridia  are  unknown. 
The  genus  was  based  on  a  single  species,  M.  spinospora  Kanouse, 
and  was  referred  by  its  author  to  the  Blastocladiaceae.  She 
states  that  zoospore  formation  is  "as  in  the  genus  Saprolegnia," 
but  does  not  say  definitely  that  biciliate  spores  are  formed.  The 
membranes  are  composed  of  true  cellulose.  Knowledge  of  the 
genus  is  confined  entirely  to  the  original  description  and  figures. 


SAPROLEGNIALES  181 


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Proc.  Bost.  Soc.  Nat.  Hist.,  31:  211-245,  pis.  11-15,  1903. 
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Saprolegniaceae.     New  Phytologist,  10:  167-203,  1911. 
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Sei.,  23:  539-549,  pi.  1-3,  1927. 
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Bui.  Intern.  Accad.  Sci.  Boheme,  18:  1-12,  12  fig.,  1913. 
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Ann.  Mycol,  8:  421-443,  1910. 
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Jour.  Elisha  Mitchell  Sci.  Soc,  43 :  108-122,  pi.  8-10,  1927. 
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biological  and  systematical  remarks.     Ann.   Mycol.,  8:  494-560,  fig. 

1-27,  1910. 
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1915a. 
,  The  ferax  group  of  the  genus  Saprolegnia.     Mycologia,  7 :  307,  pi. 

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184  THE  LOWER  FUNGI— PHYCOMYCETES 

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287-296,  pi.  23,  fig.  1,  1919. 


CHAPTER  VIII 
PERONOSPORALES 

The  highest  point  of  development  attained  in  the  Oomycetes 
is  reached  in  this  order.  The  aquatic  habit  typical  of  the 
Saprolegniales  and  other  lower  forms  has  been  largely  abandoned, 
and  most  of  the  higher  members  of  the  order  lead  a  terrestrial 
existence  as  parasites  in  the  tissues  of  higher  plants.  Correlated 
with  this  change  in  habit  has  occurred  a  pronounced  alteration 
in  the  character  of  the  asexual  stage.  The  sporangia  are  typically 
deciduous,  and  in  the  highest  genera  of  the  order  germinate 
directly  by  germ  tubes  instead  of  by  swarmspores.  In  general 
they  are  borne  in  the  air  on  specialized  hyphae  termed  spo- 
rangiophores,  and  are  commonly  disseminated  by  the  wind.  In 
the  lower  members  of  the  group  they  usually  germinate  by 
swarmspores,  though  in  some  cases  the  type  of  germination  is 
dependent  on  environmental  factors.  In  a  few  of  the  most 
primitive  forms,  they  develop  under  aquatic  conditions  and 
remain  attached.  When  swarmspores  occur  they  are  of  the 
reniform,  laterally  biciliate  type. 

The  term  conidium  is  applied  by  many  writers  to  the  sporan- 
gium in  this  group,  but  usage  is  extremely  varied.  Some  authors 
prefer  the  term  sporangium  in  all  cases  in  which  germination  is 
by  swarmspores.  Others  use  conidium  wherever  the  cell  is 
deciduous,  regardless  of  the  method  of  germination.  It  is  clear 
that  from  the  morphological  and  phylogenetic  points  of  view  only 
a  single  structure  is  present,  and  the  writer  has  found  it  desirable 
for  the  sake  of  clarity  and  uniformity  of  usage  to  avoid  the 
apphcation  of  the  term  conidium  in  the  Oomycetes. 

Mycelium  is  profusely  developed  throughout  the  entire  order, 
and  consists  of  more  or  less  cylindrical,  repeatedly  branched 
hyphae  of  relatively  small  diameter  as  compared  with  those  of 
the  Saprolegniales.  Septa  are  usually  absent  but  may  form  in 
old  hyphae.  The  mycelium  of  parasitic  species  is  usually  inter- 
cellular, the  host  cells  being  entered  only  by  short  lateral  branches 
termed  haustoria.     These  differ  in  form  in  the  various  genera, 

185 


186  THE  LOWER  FUNGI— PHYCOMYCETES 

being  globose  knobs  in  Albugo  and  elongate  branching  threads 
in  Peronospora.  In  some  cases  (e.g.,  Phytophthora)  the  mycelium 
may  be  also  intracellular,  the  hyphae  entering  and  passing 
directly  through  the  host  cells.  Species  characterized  by  inter- 
cellular mycelium  are  usually  obligate  parasites,  while  those 
with  intracellular  hyphae  exhibit  facultative  parasitism  and  tend 
to  develop  well  in  artificial  culture  media.  In  some  species  the 
myceUum  is  perennial  in  the  host,  hibernates  in  the  roots,  and 
results  in  systemic  infection  of  the  parts  above  ground  in  the 
spring. 

Oogonia  and  antheridia,  resembling  in  general  those  of  the 
preceding  order  are  formed,  but  here  they  seem  to  be  functional 
in  all  cases.  The  content  of  the  oogonium  is  differentiated  at 
maturity  into  a  peripheral  zone  of  protoplasm  (periplasm)  and  a 
single  central  oosphere.  After  fertilization  the  oosphere  is  trans- 
formed into  an  oospore,  the  oogonium  being  monosporic  through- 
out the  group.  The  oospore  usually  lies  free  in  the  oogonium. 
It  germinates  in  some  forms  by  swarmspores,  in  others  by  a  germ 
tube. 

The  order,  Peronosporales,  as  here  constituted,  contains  three 
families,  Albuginaceae,  Pythiaceae,  and  Peronosporaceae.  The 
Pythiaceae  are  clearly  the  most  primitive  of  the  forms  included, 
and  were  incorporated  by  Schroter  (1893)  in  the  Saprolegniales. 

Key  to  Families  of  Peronosporales 

A.  Sporangia  borne  in  a  chain  at  the  apex  of  a  short,  clavate,  usually 

unbranched    sporangiophore.     Sporangiophores    forming    a    limited 
sorus  beneath  the  host  epidermis,  and  exposed  by  its  rupture. 

1.  Albuginaceae,  p.  186 

B.  Sporangia  usually  borne  singly  at  the  tips  of  a  branching  sporangiophore, 

sometimes  intercalary,  rarely  in  chains.     Sporangiophores  not  forming 
a  sorus  within  the  host. 

1.  Sporangiophore  usually  not  sharply  differentiated  from  the  hyphae 

of  the  mycelium.     Sporangia  borne  successively. 

2.  Pythiaceae,  p.  193 

2.  Sporangiophore   sharply   differentiated   from    the   hyphae   of   the 

mycelium,  and  bearing  the  sporangia  simvdtaneously  at  the  tips 
of  its  branches. 

3.  Peronosporaceae,  p.  210 

Albuginaceae 

The  members  of  this  family  occur  as  parasites  on  flowering 
plants,  and,  as  far  as  is  known,  their  parasitism  is  in  all  cases 


PERONOSPORALES  187 

obligate.  The  mycelium  is  strictly  intercellular  except  for  the 
production  of  small  knob-like  haustoria  which  lie  just  within 
the  host  cells.  The  sporangiophores  are  short,  broadly  clavate, 
and  usually  unbranched  (Fig.  69).  They  are  developed  in  a 
compact  group  just  beneath  the  epidermis,  and  form  there  a 
definite  palisade  layer.  At  the  tip  of  each  sporangiophore 
sporangia  are  abstricted  in  basipetal  succession,  and  remain 
attached  forming  a  chain.  The  outward  growth  of  these  chains 
exerts  sufficient  pressure  to  rupture  the  epidermis,  and  an  open 
sorus  resembling  that  of  the  caeoma  stage  of  certain  rusts,  except 
in  color  which  is  here  white,  results.  Early  investigators  called 
the  members  of  the  family  "white  rusts."  A  superficial  resem- 
blance to  the  rusts  is  noted  not  only  in  the  aspect  of  the  sori,  but 
also  in  the  striking  similarity  of  the  chains  of  sporangia  to  chains 
of  aecidiospores.  Even  an  intercalary  cell  seems  to  be  present 
between  each  pair  of  sporangia  in  the  chain.  This  appearance 
is,  however,  an  illusion  resulting  from  the  gelatinization  of  the 
outer  layer  of  the  walls  of  the  sporangia  at  their  point  of  contact, 
with  the  consequent  formation  of  a  small  gelatinous  disc  between 
them.  Complete  gelatinization  of  the  disc  results  in  the  falling 
apart  of  the  sporangia.  True  intercalary  cells  such  as  exist  in 
the  rusts  are  absent.  Though  the  sporangia  tend  to  hang 
together  for  a  time  in  rather  long  chains,  they  finally  separate 
and  form  a  dry  white  powder  easily  disseminated  by  the  wind. 
The  sporangium  germinates  by  means  of  swarmspores. 

The  sexual  organs  are  formed  in  the  intercellular  spaces  of 
the  host.  The  oogonium  is  globose  and  develops  from  a  terminal 
or  intercalary  swelling  of  the  mycelium.  Its  contents  are  clearly 
differentiated  into  a  peripheral  zone  of  periplasm  and  a  single 
central  spherical  oosphere.  The  antheridium  is  clavate,  and 
applies  itself  to  the  side  of  the  oogonium.  A  fertilization  tube 
enters  the  oogonium,  reaches  the  oosphere,  and  ruptures,  intro- 
ducing one  or  more  male  nuclei.  A  true  fertilization  occurs,  and 
a  single  oospore  is  matured.  Germination  of  the  oospore  is  by 
swarmspores. 

The  limits  of  the  family  are  sharply  defined,  there  being  no 
close  relatives  in  neighboring  groups.  The  development  of  the 
sporangia  in  chains  in  a  definite  sorus  beneath  the  surface  of 
the  host  furnishes  a  striking  point  of  difference  between  this 
group  and  the  two  other  families  of  the  order.  While  more 
highly  developed  in  certain  respects  than  the  Pythiaceae  it  is 


188 


THE  LOWER  FUNGI— PHYCOMYCETES 


here  treated  first,  since  a  position  between  the  Pythiaceae  and 
Peronosporaceae  would  fail  completely  to  indicate  the  natural 
relationships. 

The  members  of  the  family  are  all  embraced  in  the  single 
genus  Albugo. 

1.  Albugo  (Persoon)  Gray  (1821:  540). 
syn.  Cystopus  Lev.  (1847:  371). 

About  twenty-five  species  have  been  described  in  this  genus 
for  the  world.  Wilson  (1907  a;  1908  a)  in  his  monograph  of  North 
American  forms  includes  fifteen.     Several  of  these  are  common 


Fig.  69. — (a)  Albugo  portulacac  (DC.)  Kuntze,  showing  sporangiophores  and 
chains  of  sporangia,  (b-f)  A.  Candida  (Pers.)  Kuntze.  (6)  Swarmspores.  (c) 
Young  oogonium  and  antheridium.  (d)  Mature  oospore  in  oogonium,  (e-/) 
Germinating  oospore,  (gf)  A.  tragopogonis  (DC.)  Gray;  mature  oospore,  {g, 
after  Schwarze  1917;  others  after  de  Bary  1887.) 

and  almost  cosmopolitan  in  distribution.  The  species  may  be 
separated  into  two  groups  on  the  basis  of  the  character  of  the 
markings  of  the  outer  wall  of  the  oospore  (Fig.  69).  Some 
{e.g.,  A.  Candida,  A.  ipomoeae-panduranae)  have  a  definitely 
tuberculate  epispore,  while  in  others  {e.g.,  A.  bliti,  A.  tragopogonis, 
A.  portulacae)  it  is  reticulate.  Cytological  studies  have  demon- 
strated that  differences  in  life-histories  are  correlated  with  this 
difference  in  epispore  markings,  the  group  characterized  by  the 
tuberculate  epispore  containing  the  more  highly  developed 
species.  This  fact  will  be  clearly  indicated  in  the  following 
discussion  of  the  sexual  process. 


PERONOSPORALES  189 

The  sexual  organs  of  Albugo,  on  account  of  their  hidden 
position  in  the  interior  of  the  host,  were  discovered  much  later 
than  the  sporangia.  They  were  first  noted  by  de  Bary  in  A. 
Candida.  He  saw  the  penetration  of  the  fertilization  tube  to  the 
oosphere,  but,  failing  to  observe  its  rupture,  felt  that  it  effected 
fertilization  by  contact  only.  His  view  was  doubtless  influenced 
by  his  earlier  work  on  Saprolegnia  where  he  had  found  partheno- 
genetic  species.  Subsequently,  other  investigators,  using  modern 
cytological  technique,  have  examined  A.  Candida  and  several 
other  species  of  the  genus,  and  have  found  a  true  sexuality  in  all. 
Their  discussions  indicate  such  a  great  diversity  in  the  details 
of  the  sexual  process  in  the  different  species  that  the  genus  must 
be  regarded,  from  the  standpoint  of  the  cytologist,  as  one  of  the 
most  remarkable  and  interesting  in  all  the  fungi.  It  will  be 
necessary  to  summarize  the  results  on  several  forms  in  order 
to  give  a  clear  conception  of  the  situation  in  the  genus  as  a  whole. 

In  all  of  the  species  the  young  sexual  organs  are  cut  off  by 
transverse  septa  from  the  main  body  of  the  hypha  after  the 
flowing  in  of  the  cytoplasm  and  nuclei.  Both  organs  are  multi- 
nucleate from  the  beginning.  At  about  the  time  that  the 
antheridium  comes  in  contact  with  the  oogonium  a  differentiation 
of  the  protoplasm  of  the  latter  into  a  peripheral  zone  of  periplasm 
and  a  central  spherical  oosphere  begins  to  take  place.  The 
majority  of  the  nuclei  are  left  within  the  limits  of  the  oosphere. 

In  A.  Candida  the  oogonium  contains  approximately  one 
hundred  nuclei,  the  antheridium  six  to  twelve,  and  these  undergo 
one  simultaneous  division  throughout  both  organs  before  the 
oosphere  is  formed.  At  the  point  of  contact  of  the  oogonium 
and  antheridium  the  wall  becomes  very  thin,  and  the  oogonium 
pushes  through  forming  a  slight  prominence  within  the  antherid- 
ium. This  has  been  termed  the  receptive  spot  (Wager,  1896  b) 
or  the  receptive  papilla  (Stevens,  1899;  1901).  It  seems  to  be 
functionless,  and  its  formation  may  be  due  merely  to  the  existence 
of  a  higher  state  of  turgor  in  the  oogonium  than  in  the  antherid- 
ium. It  soon  disappears,  and  the  fertilization  tube  from  the 
antheridium  enters  through  the  resultant  thin  spot  in  the  wall,  and 
advances  to  the  oosphere.  After  completion  of  differentiation 
of  the  protoplasm  of  the  oogonium  into  periplasm  and  ooplasm 
all  of  the  nuclei,  both  in  the  antheridium  and  in  the  ooplasm, 
undergo  a  second  mitosis,  while  those  in  the  periplasm  remain 
inactive   and   soon   disorganize.     Coincident   with   this   second 


190  THE  LOWER  FUNGI— PHYCOMYCETES 

mitosis  a  sphere  of  dense,  deeply  staining,  slightly  granular 
cytoplasm,  several  times  the  diameter  of  a  single  nucleus,  appears 
in  the  center  of  the  ooplasm.  This  structure  has  been  termed 
the  central  body  or  coenocentrum.  It  is  sometimes  surrounded 
by  a  zone  of  lighter  staining  ooplasm  through  which  delicate 
astral  radiations  pass.  Though  not  a  permanent  structure 
in  the  cell  it  is  prominent  for  a  period  immediately  preceding 
fertilization.  Shortly  after  its  appearance  a  single  female 
nucleus  is  attracted  by  it  to  the  center  of  the  oosphere  and 
remains  there  while  the  other  nuclei  of  the  oosphere  pass  out 
into  the  periplasm  where  they  form  a  sphere  about  the  ooplasm. 
The  fertilization  tube  carrying  a  single  male  nucleus  and  a 
small  amount  of  cytoplasm  then  penetrates  to  the  center  of  the 
oosphere,  reaches  the  coenocentrum,  and  ruptures.  The  male 
nucleus  comes  in  contact  with  the  female  nucleus  and  fuses  with 
it,  the  fertilization  tube  collapses,  is  withdrawn  from  the  oosphere 
leaving  a  large  vacuole,  and  the  wall  of  the  oospore  is  laid  down. 
The  endospore  is  thin;  the  exospore  is  thick  and  at  completion 
definitely  tuberculate.  The  supernumerary  nuclei  in  the 
antheridium  and  in  the  periplasm  disintegrate  following  fertiliza- 
tion, and  the  coenocentrum  disappears.  The  fusion  nucleus  soon 
divides  and  repeated  mitoses  result  in  the  formation  of  about 
thirty  nuclei.  Since  the  number  of  uninucleate  zoospores  formed 
later  in  germination  is  slightly  in  excess  of  one  hundred.  Wager 
regards  the  thirty  nuclei  as  spore-mother  nuclei,  and  feels  that 
they  undergo  the  maturation  divisions  immediately  before 
swarmspore  formation.  There  is,  however,  as  much  reason  to 
regard  the  two  simultaneous  mitoses  which  occur  in  the  game- 
tangia  preceding  fertilization  as  the  reducing  divisions;  or  from 
analogy  with  other  fungi  the  first  two  mitoses  of  the  fusion 
nucleus  may  well  be  regarded  as  accomplishing  reduction.  In 
any  case  in  the  absence  of  more  complete  knowledge  only  specu- 
lation is  possible. 

In  A.  hliti  a  wholly  different  type  of  fertilization  has  been 
described.  In  this  species  the  oogonium  contains  about  three 
hundred  nuclei,  and  the  antheridium  about  thirty-five.  The 
receptive  papilla  extends  far  into  the  antheridium,  and  is  much 
more  prominent  than  in  A.  Candida.  As  the  content  of  the 
oogonium  begins  to  differentiate  into  ooplasm  and  periplasm  all 
of  the  nuclei  migrate  to  the  periphery  undergoing  a  mitosis  as 
they  pass  outward.     Soon  they  are  arranged  in  a  hollow  sphere 


PERONOSPORALES  191 

bordering  the  ooplasm.  A  section  through  the  oogonium  at 
this  stage  shows  the  vacuoUite  periplasm  at  the  periphery,  a  circle 
of  nuclei  next  within  in  the  later  stages  of  mitosis,  and  at  the 
center  the  sphere  of  homogeneous  ooplasm.  Stevens  calls  this 
the  stage  of  zonation.  The  division  figures  of  certain  of  the 
nuclei  in  this  division  lie  across  the  hne  of  demarcation  between 
the  periplasm  and  the  ooplasm,  and  in  the  completion  of  these 
divisions,  one  daughter  nucleus  in  each  case  enters  the  ooplasm. 
Thus  approximately  fifty  nuclei  enter  the  oosphere.  It  becomes 
consequently  a  coenocytic  structure  and  is  termed  by  Stevens 
the  compound  oosphere.  The  nuclei  in  the  antheridium  divide 
simultaneously  with  those  in  the  oogonium,  resulting  there  in 
about  seventy  at  this  stage.  The  receptive  papilla  ruptures  or 
is  withdrawn,  and  the  fertihzation  tube  enters  the  oogonium 
and  penetrates  to  the  oosphere.  A  relatively  small  and  incon- 
spicuous coenocentrum  is  developed,  but  fails  to  function  in 
attracting  the  sex  nuclei,  and  disappears  before  fertilization 
occurs.  A  second  division  of  all  the  nuclei  in  the  antheridium 
and  oosphere  now  takes  place.  Those  in  the  periplasm  fail  to 
divide  and  soon  disintegrate.  This  division  results  in  the 
presence  of  about  one  hundred  nuclei  in  the  oosphere  and  one 
hundred  and  forty  in  the  antheridium.  The  fertihzation  tube 
then  ruptures,  and  the  majority  of  the  antheridial  nuclei  pass 
into  the  oosphere  where  the  male  and  female  nuclei  fuse  in  pairs, 
approximately  one  hundred  fusion  nuclei  resulting.  The  super- 
numerary male  nuclei  disintegrate,  and  the  oospore  wall  is 
formed,  the  epispore  being  strongly  reticulate.  The  multi- 
nucleate oospore  then  hibernates,  the  fusion  nuclei  passing  the 
winter  without  change. 

Reviewing  the  situation  we  see  that  in  A.  Candida  a  single 
male  nucleus  fuses  with  a  single  female  nucleus  in  a  uninucleate 
oosphere,  the  receptive  papilla  is  small,  the  coenocentrum  is 
highly  developed,  the  fusion  nucleus  divides  rapidly  to  form 
about  thirty  nuclei  before  hibernation,  and  the  epispore  is  tuber- 
culate.  In  A.  bliti  many  male  nuclei  fuse  in  pairs  with  female 
nuclei  in  a  multinucleate  oosphere,  the  receptive  papilla  is  long 
and  prominent,  the  coenocentrum  is  relatively  inconspicuous 
and  functionless,  the  fusion  nuclei  do  not  divide  before  the  period 
of  rest,  and  the  epispore  is  reticulate. 

The  sexual  process  in  A.  portulacae  is  very  similar  to  that  in 
A.  bliti,  while  that  in  A.  lepigoni  (Ruhland,  1903)  is  practically 


192  THE  LOWER  FUNGI— PHYCOMYCETES 

identical  with  that  in  A.  Candida.  In  A.  traqopogonis  a  multi- 
nucleate oospherc  develops  as  in  A.  bliti,  but  while  all  the  nuclei 
in  the  oospherc  may  be  termed  potentially  sexual,  they  are  not 
all  functional.  Following  the  two  divisions  in  the  oogonium, 
resulting  in  a  multinucleate  oospherc,  all  but  one  of  the  nuclei 
disorganize.  The  antheridium  empties  several  nuclei  into  the 
oosphere,  but  all  but  one  of  these  also  disorganize.  The  remain- 
ing pair  of  nuclei  fuse.  The  fusion  nucleus  undergoes  repeated 
divisions  at  once,  the  oospore  entering  the  winter  in  the  multi- 
nucleate condition.  The  coenocentrum  is  almost  as  highly 
developed  as  in  A.  caiidida,  but  the  receptive  papilla  is  relatively 
inconspicuous.  In  A.  ipomoeae-'panduranae  there  are  apparently 
a  few  supernumerary  female  nuclei  which  disintegrate  in  the 
oosphere,  but  the  fertilization  tube  discharges  only  a  single  male 
nucleus.  Stevens  regards  the  multinucleate  condition  in  A.  bliti 
and  A.  portulacae  as  primitive,  and  the  uninucleate  condition  in 
A.  Candida  as  a  higher  development.  Arranging  the  species  in 
a  series  and  passing  from  A.  portulacae  at  one  extreme  to  A. 
Candida  at  the  other  it  will  be  noted  that  the  coenocentrum 
increases  in  height  of  development  and  the  receptive  papilla 
decreases  in  size  as  the  number  of  functional  sex  nuclei  passes 
from  many  to  one  and  the  epispore  changes  from  reticulate  to 
tuberculate. 

The  species  enumerated  below  are  the  common  representatives 
of  the  genus  in  North  America.  For  technical  descriptions  the 
papers  of  Wilson  (1907  a;  1908  a)  should  be  consulted. 

A.  Candida  (Pers.)  Kuntze — On  many  genera  and  species  of  the  mustard 
family;  probably  best  known  on  shepherd's  purse   (Capsella). 

A.  bliti  (Biv.)  Kuntze — Common  on  various  species  of  Amaranlhus 
(pigweed)  and  on  a  few  related  plants. 

A.  ijjomoeae-panduranae  (Schw.)  Swing. — On  various  Convolvulaceae. 
The  form  on  Ipomoea  batatas  has  been  named  A.  minor  (Speg.)  Cif.  (Nuovo. 
(iior.  Bot.  Ital.  n.  s.  35:  132,  1928.) 

A.  portulacae  (DC.)  Kuntze — Restricted  to  the  common  purslane, 
Portulaca  'oleracea  L. 

A.  tragopogonis  (DC.)  S.  F.  Gray — Attacking  a  wide  variety  of  Compositae 
(common  on  ragweed,  Canada  thistle,  and  salsify). 

Recently  Wakefield  (1927)  has  revived  the  name  Cystopus,  and 
applies  it  to  the  genus  in  preference  to  Albugo.  She  does  this 
in  an  attempt  to  follow  the  International  Rules  of  Nomenclature 
(art.  49  bis),  which  state  that,  in  the  case  of  fungi  having  a 
pleomorphic  life  cycle,  only  names  applied  to  the  perfect  stage 


I'EliONOSPOUALES  193 

may  be  recognized.  Since  the  oospores  of  this  genus  were  first 
described  by  de  Bary  (1863)  under  the  name  Cydopus  she 
attributes  the  genus  to  him  rather  than  to  Leveille  who  first 
used  the  name  Cystopus  for  the  sporangial  stage  alone. 

The  wording  of  the  rule  is  such  as  to  leave  open  to  question 
the  necessity  of  its  application  to  the  Phycomycetes,  and  in 
other  respects  its  meaning  is  not  clear.  Some  workers  (e.g., 
Murphy  1918)  have  interpreted  it  as  excluding  the  Phycomycetes. 
Until  it  is  further  elucidated  the  writer  prefers  to  retain  the 
name  Albugo,  now  well  established  in  the  American  literature. 

Pythiaceae 

The  members  of  this  family  are  clearly  the  most  primitive 
of  the  Peronosporales,  and  in  certain  respects  stand  as  an  inter- 
mediate group  between  the  Saprolegniaceae  and  Leptomitaceae 
on  the  one  hand,  and  the  Peronosporaceae  on  the  other.  In  the 
lower  members  of  the  group  the  habit  is  aquatic,  the  sporangia 
remain  attached,  and  swarmspores  constitute  the  usual  method 
of  asexual  propogation.  In  the  higher  members  the  habit  is 
terrestrial,  the  sporangia  are  deciduous,  and  germination  is 
sometimes  by  germ  tube.  Intermediate  species  exemplify  inter- 
mediate conditions.  Parasitism  is  less  highly  developed  through- 
out the  group  than  in  the  Peronosporaceae,  and  apparently  is 
never  obligate.  In  some  of  the  most  highly  developed  forms 
(e.g.,  Phytophthora  infestans)  a  definite  sporangiophore  is  devel- 
oped, but  in  most  cases  the  hyphae  which  bear  the  sporangia 
are  not  sharply  differentiated  from  those  of  the  vegetative 
mycelium.  Even  when  a  specialized  sporangiophore  is  pres- 
ent it  does  not  mature  its  sporangia  simultaneously  at  the 
tips  of  its  branches  as  in  the  Peronosporaceae.  Instead,  they  are 
developed  successively,  sporangia  of  different  ages  existing 
together  on  the  same  sporangiophore.  Moreover,  the  spo- 
rangiophore m.ay  develop  extensively  even  after  some  of  the 
sporangia  have  reached  maturity.  The  mycelium  in  the  Pythia- 
ceae is  of  small  diameter  (S-A/jl,  rarely  7ai),  is  abundantly  and 
irregularly  branched  in  most  species,  and  may  be  septate  at 
maturity.     (See  Jour.  Agric.  Res,  40:  557,  for  "diplanetism.") 

The  family  was  placed  by  Schroter  (1893)  in  the  Saproleg- 
niales,  but  most  authors  have  included  it  in  the  Peronosporales. 
Its  intermediate  character  has  rendered  difficult  the  task  of 
finding  a  satisfactory  basis  for  a  taxonomic  separation  of  the 


194  THE  LOWER  FUNGI— PHYCOMYCETES 

two  orders.  On  the  one  hand,  the  highest  of  the  Pythiaceae 
provide  a  series  of  closely  intergrading  forms  connecting  the 
family  with  the  Peronosporaceae,  while  on  the  other,  the  lowest 
of  the  Pythiaceae  are  so  similar  in  various  respects  to  members  of 
the  Saprolegniales  that  the  two  groups  tend  to  merge  at  the 
border  line.  The  sexual  stage  corresponds  to  that  of  the  Pero- 
nosporaceae rather  than  to  that  of  the  Saprolegniaceae,  but  does 
not  differ  essentially  from  that  of  the  Leptomitaceae.  In  general, 
the  mycelium  corresponds  to  that  of  the  Peronosporaceae  in  its 
small  diameter  and  tendency  to  irregularity. 

Key  to  Genera  of  Pythiaceae 

I.  Sporangium  much  broader  than  the  mycehum,  strikingly  asymmetrical 
in  form,  and  standing  usually  with  its  long  axis  at  right  angles  to  that 
of  the  sporangiophore. 

1.  Pythiogeton,  p.  194 

II.  Sporangium  not  standing  with  its  long  axis  at  right  angles  to  that  of  the 
sporangiophore,  in  most  species  broader  than  the  mycelium  and 
symmetrical  (oval,  spherical,  obpyriform,  etc.),  in  a  few  cases  (sub- 
genus Aphragmium  of  Pythium)  filamentous. 

A.  Sporangial  wall  smooth. 

1.  Sporangium,  in  germination,  discharging  the  swarmspores  in 

an  imperfectly  differentiated  state  into  a  thin-walled 
vesicle,  which  later  ruptures  allowing  the  fully  formed 
spores  to  escape. 

2.  Pythium,  p.  195 

2.  Swarmspores    sometimes    discharged    fully    formed    into    a 

vesicle,  but  usually  freed  directly  through  a  pore  in  the 
sporangial  wall. 

3.  Phytophthora,  p.  199 

B.  Sporangial  wall  echinulate;  germination  by  germ  tube;  swarm- 

spores unknown. 

4.  Trachysphaera,  p.  209 

1.  Pythiogeton  v.  Minden  (1916:  228). 

This  genus  includes  three  species,  P.  uiriforme,  P.  transversum, 
and  P.  ramosum,  all  of  them  described  by  von  Minden.  It  is 
closely  related  to  Pythium,  differing  chiefly  in  that  the  sporangium 
has  the  aspect  of  being  attached  at  its  side  to  the  sporangiophore 
instead  of  at  its  base.  The  long  axis  of  the  sporangium  hes  at  a 
right  angle  to  that  of  the  sporangiophore,  and  germination 
takes  place  at  one  end  of  this  axis  instead  of  opposite  the  point 
of  attachment  (Fig.  70).  In  germination,  the  undifferentiated 
plasma  of  the  sporangium   flows  into  a  thin-walled,   tubular, 


PERONOSPORALES 


195 


often  much  elongate  vesicle,  accumulates  at  its  tip,  and  at 
its  rupture  passes  as  an  undifferentiated  mass  into  the  water, 
finally  breaking  up  there  into  swarmspores.  Proliferation  of 
sporangia  is  of  frequent  occurrence.  Their  germination  by  germ 
tube  is  unknown.  The  branch  bearing  the  oogonium  is  charac- 
teristically coiled  around  that  bearing  the  antheridium.  The 
oogonium  is  globose  or  polygonal,  and  is  almost  completely 
filled  by  the  oospore  which  has  a  thick,  hyaline,  concentrically 


m^§[ 


Fig.  70.- — Pythiogeton  transversum  v.  Minden.  (a)  Mycelium  bearing  three 
sporangia,  one  empty  and  another  showing  the  extrusion  of  the  contents  into  a 
tubuhir  vesicle  (fe).  (c)  Undifferentiated  plasma  after  rupture  of  vesicle,  {d) 
Partially  formed  swarmspores.  (e)  Mature  ciliated  swarmspores.  {After  v. 
Minden  1916.) 

stratified  wall.  The  method  of  oospore  germination  is  unknown. 
The  mycelium  is  of  small  diameter  and  is  saprophytic  in  vegetable 
substrata  in  the  water. 

2.  Pythium  Pringsheim  (1858). 

The  genus  Pythium  was  erected  by  Pringsheim  on  two  aquatic 
species,  P.  monospermum  Pringsheim  and  P.  entoyhytuvi  Prings- 
heim. The  latter  species  was  later  transferred  to  Lagenidium 
of  the  Ancylistales  by  Zopf.  In  Pringsheim's  account  the  genus 
is  a  member  of  the  Saprolegniaceae,  and  as  such  was  placed  by 
him  in  the  algae.  Other  species  were  soon  discovered  and 
described;  P.  grmcz7e Schenk  in  IS59, P. proliferimi  de  Bary  in  1860, 


196  THE  LOWER  FUNGI— PHYCOMYCETES 

P.  cystosiphon  (Roze  &  Cornu)  Lindstedt  in  1872,  P.  deharyanum 
Hesse  in  1874,  and  P.  vexans  de  Bary  in  1876.  The  economic 
importance  of  the  genus  was  first  reahzed  with  the  appearance 
of  the  paper  of  Hesse  (1874).  In  1881  de  Bary  transferred  the 
genus  to  the  Peronosporaceae,  placed  near  it  his  own  genus 
Phytophthora,  and  described  several  additional  species,  P.  ferax 
de  Bary,  P.  megalacanthum  de  Bary,  P.  intermedium  de  Bary,  and 
P.  artotrogus  (Montagne)  de  Bary. 

In  1892  Fischer  followed  de  Bary  in  placing  Pythium  in  the 
Peronosporaceae,  but  split  the  genus  into  three  subgenera, 
Sphaerosporangium,  in  which  the  sporangia  are  typically  more 
or  less  spherical,  and  Aphragmium  and  Nematosporangium,  in 
which  they  are  filamentous.  As  treated  by  him  Nematospo- 
rangium embraces  only  a  single  species,  P.  monosperrmtm,  which 
he  states  differs  from  Aphragmium  in  that  a  septum  cuts  off  the 
sporangium  from  the  remainder  of  the  hypha.  In  Aphragmium 
the  sporangium  is  indeterminate  in  extent,  a  septum  being 
lacking. 

Schroter  (1893)  raised  Nematosporangium  to  the  rank  of  a 
genus,  and  extended  its  limits  to  embrace  A  phragmium,  thus  leav- 
ing  Pythium  equivalent  to  Sphaerosporangiu7n  of  Fischer.  More- 
over, he  created  a  new  family,  Pythiaceae,  to  include  the  two 
genera  and  placed  it  in  the  Saprolegniales.  In  this  manner, 
Pythium  and  Phytophthora  came  to  lie  in  different  orders,  the 
latter  genus  being  retained  in  the  Peronosporaceae.  The  inclu- 
sion of  Pythium  in  the  Saprolegniales  is  clearly  illogical,  and 
Schroter's  classification  in  this  regard  differs  from  those  of  other 
modern  authors. 

In  1907  Butler  published  a  monographic  treatment  oi  Pythium, 
based  on  extensive  research  on  the  group  in  India,  and  presented 
a  separation  of  seventeen  species  which  has  stood  for  twenty  years 
as  essentially  satisfactory.  Meanwhile,  no  other  comprehensive 
discussion  of  the  genus  has  appeared.  In  Butler's  account  Nema- 
tosporangium and  Aphragmium  are  merged  as  one  subgenus  under 
the  latter  name,  his  monograph  covering  the  entire  genus  Pythium 
as  understood  by  Fischer. 

In  Aphragmium  the  sporangium  is  filamentous  and  often 
branched.  It  is  e\ddently  merely  an  indeterminate  portion 
of  the  mycelium  functioning  as  a  sporangium.  It  is  not 
separated  from  the  remainder  of  the  hypha  by  a  septum,  and 
portions   of   the   protoplasm    which   remains   may   form   other 


PERONOSPORALES 


197 


Fig.  71.- — (a-/)  Pythium  debaryanum,  Hesse,  ig-s)  P.  intermedium  de  Bary. 
(o)  Oogonium  with  fully  formed  oosphere  before  fertilization,  {b)  Same  after 
fertilization,  (c)  Oogonium  before  fertilization,  accompanied  by  two  antheridia 
in  which  differentiation  into  gonoplasm  and  periplasm  has  occurred,  (d)  Same 
after  fertilization,  (e)  Young  oogonium.  (/)  Oogonium  with  a  pair  of  anther- 
idia. (g)  Chain  of  sporangia,  {h)  Sporangia  formed  successively  and  becoming 
lateral  by  further  elongation  of  the  hypha.  (A;)  Intercalary  sporangium,  (m-p) 
Steps  in  phenomenon  of  extrusion  of  contents  of  sporangium  into  vesicle,  (s) 
Swarmspore  formation.     {After  Atkinson  1895.) 


198  THE  LOWER  FUNGI— PHYCOMYCETES 

sporangia  which  discharge  through  other  branches.  The  spo- 
rangia are  thus  terminal  or  intercalary,  and  ultimately  may  form 
throughout  the  entire  mycelium.  Here,  as  in  the  remainder  of 
the  genus,  the  swarmspores  pass  out  incompletely  differentiated 
into  a  spherical,  thin-walled  vesicle  which  later  bursts  allowing 
their  escape.  Germination  of  the  sporangium  by  a  germ  tube 
has  not  been  observed,  i.e.,  so  called  conidia  are  lacking.  The 
antheridia  and  oogonia  are  cut  off  by  septa  except  in  a  single 
species,  P.  tenue  Gobi,  where  the  septum  is  absent  at  least  in 
the  antheridial  branch.  As  treated  by  Butler  the  subgenus 
includes,  P.  teiiue,  P.  gracile  Schenk,  P.  monospertmim  Prings., 
P.  indigoferae  Butler,  and  P.  didyospermum  Racib.  The  species 
are  chiefly  parasites  in  aquatic  algae.  More  recently  other 
species  have  been  described.  The  fungus  Rheosporangium 
aphanidermatum  Edson  (1915),  cause  of  a  disease  of  radish  known 
as  black-root  and  damping-off  of  beet  seedlings  has  been  shown 
to  belong  here  (Fitzpatrick,  1923).  It  is  stated  by  Carpenter 
(1921)  to  be  the  same  as  P.  butleri  Subramaniam  (1919)  which 
causes  a  disease  of  ginger,  tobacco,  papaya,  and  sugar  cane.  Also 
P.  afertile  Kanouse  &  Humphrey  (1928)  falls  in  this  group. 

The  subgenus  Sphaerosporangium  contains  a  larger  number  of 
species.  Butler  recognizes  thirteen,  and  others  have  been 
described  since,  including  P.  graminicolum  Subramaniam  (1928), 
P.  torulosum  Coker  &  Patterson  (1927),  P.  irregular e  Buisman 
(1927),  P.  arrhenomanes  Drechsler  (1928),  P.  mamillatum  Meurs 
(1928),  and  others.  No  paper  has  yet  appeared  giving  a  separa- 
tion of  all  the  described  species. 

The  sporangium  in  Sphaerosporangium  is  usually  spherical  to 
ovoidal,  but  may  have  the  obpyriform  shape  more  typical  of 
species  of  Phijtophthora.  It  is  cut  off  from  the  fertile  hypha  by 
a  septum.  Definite  sporangiophores  are  lacking,  the  sporangia 
arising  throughout  the  mycelium  from  undifferentiated  hyphae. 
Though  usually  terminal  the  sporangia  are  sometimes  intercalary, 
and  may  exist  in  chains.  When  developed  in  the  air  they  may 
be  deciduous,  but  when  submerged  usually  remain  attached. 
Germination  takes  place  either  by  swarmspores  or  by  germ  tube, 
and  in  some  species  it  is  possible  to  predict  one  type  or  the  other 
in  cultures  under  controlled  environmental  conditions  (Fig. 
70).  The" conidia"  of  Butler  and  other  writers  are  merely 
sporangia  undergoing  direct  germination. 

In  swarmspore  formation,  as  in  Aphragmium,  a  thin-walled 
vesicle  is  extruded,  and  the  protoplasm  passes  out  into  it  before 


PERONOSPORALES  199 

the  swarmspores  are  fully  formed.  The  vesicle  may  arise  at  the 
apex  or  at  the  side  of  the  sporangium.  Frequently  it  is  initiated 
as  a  cylindrical  tube  which  may  attain  considerable  length 
before  becoming  inflated  at  the  tip  to  form  a  globose  bladder. 
The  recent  use  of  the  term  emission  collar  by  Sideris  (1929) 
for  the  tubular  or  attenuated  portion  of  the  vesicle  lying  next 
the  sporangium  seems  unfortunate.  The  swarmspores  escape 
by  the  rupture  of  the  vesicle,  and  are  then  seen  to  be  reniform  and 
laterally  biciliate  (not  uniciliate  as  usually  pictured  for  P. 
deharyanum).  Some  writers  apply  the  term  sporangium  to  the 
vesicle  which  frees  the  spores,  and  designate  the  primary  cell 
from  which  it  arises  the  prosporangium  (presporangium  of  Edson, 
1915).  This  terminology  is  confusing  and  in  any  case  cannot 
be  appUed  in  the  related  genus  Phytophthora,  where  in  a  given 
species  the  vesicle  is  sometimes  formed  and  sometimes  absent. 

The  oogonia  and  antheridia  of  species  of  Pythium  are  developed 
on  either  the  intra-  or  extramatrical  mycelium.  The  sexual 
process  corresponds  in  general  to  that  described  for  Peronospora 
parasitica.  Differentiation  into  ooplasm  and  periplasm  occurs,  a 
coenocentrum  is  present,  fusion  of  one  male  with  one  female 
nucleus  takes  place,  and  the  oospore  germinates  usually  by  a  germ 
tube.  The  details  of  the  process  are  given  by  Trow  (1901) 
for  P.  ultimum,  by  Miyabe  (1901)  for  P.  deharyanum,  by  Pat- 
terson (1927)  for  P.  torulosum,  and  by  Edson  (1915)  for  P. 
aphanidermatum. 

The  genus  Zoophagus  Sommerstorff  (1911),  based  on  Z. 
insidians  Som.,  a  species  attacking  rotifers,  is  apparently  too 
close  to  the  subgenus  Aphragmium  of  Pythium  to  permit  of  its 
recognition  as  a  separate  genus.  This  species  has  been  discussed 
by  Arnaudow  (1918;  1925),  Gicklhorn  (1922),  Mirande  (1920), 
and  Sparrow  (1929).  The  latter  writer,  basing  his  observations 
on  American  material,  gives  us  a  clear  conception  of  the  species. 
The  fungus  differs  from  Aphragmium,  as  thus  far  described,  in 
possessing  "gemmae"  in  addition  to  the  filamentous  sporangia. 
The  swarmspores  are  said  to  be  diplanetic,  and  the  species  is 
heterothallic. 

3.  Phytophthora  de  Bary  (1876:  240). 

Although  most  authorities  on  the  Phycomycetes  have  included 
Phytophthora  in  the  Peronosporaceae,  it  is  here  removed  from 
that  family  and  incorporated  in  the  Pythiaceae  because  of  the 


200  THE  LOWER  FUNGI— PHYCOMYCETES 

indefinite  character  of  its  sporangiophore  and  the  successive 
development  of  its  sporangia.  In  these  respects  it  differs 
strikingly  from  such  genera  as  Peronospora,  Plasmopara,  and 
Sclerospora.  Its  close  relationship  to  Pythium  forbids  the 
treatment  of  the  two  genera  in  different  families  as  advocated 
by  Schroter  (1893).  In  fact  the  two  genera  stand  so  close 
together  that  at  present  no  satisfactory  basis  for  a  generic 
separation  is  known  (Fitzpatrick,  1923).  The  recognition  of 
Phytophthora  as  a  genus  distinct  from  Pythium  is  chiefly  in 
deference  to  precedent.  The  merging  of  the  two  genera  under 
the  older  name  Pythium  will  probably  take  place  in  time  unless 
future  research  on  the  group  reveals  a  more  tangible  basis  for 
their  separation  than  any  known  at  present. 

De  Bary,  in  founding  the  genus  Phytophthora,  realized  its 
close  relationship  with  Pijthium,  but  felt  that  the  difference 
in  sporangial  germination  existing  in  the  species  known  to  him 
served  to  separate  the  two.  Butler  (1907),  the  foremost  student 
of  the  Pythiaceae,  has  accepted  de  Bary's  point  of  view  as  a 
basis  for  retention  of  the  two  generic  concepts.  He  emphasizes 
the  fact  that  in  Pythium  germination  is  always  accomplished  by 
the  extrusion  of  the  contents  of  the  sporangium  into  a  thin-walled 
vesicle  which  finally  bursts  freeing  the  spores.  Later  work  by 
Rosenbaum  and  others  demonstrated  that  a  vesicle  is  not  infre- 
quently formed  in  Phytophthora,  though  it  is  true  that  the  swarm- 
spores  of  this  genus  usually  escape  directly  from  the  sporangium. 
When  a  vesicle  is  formed  in  Phytophthora  the  swarmspores  are 
said  to  be  fully  formed  before  their  migration  into  the  vesicle 
begins.  In  Pythium,  according  to  Butler,  they  flow  out  in  an 
incompletely  differentiated  state  and  attain  their  final  form  in 
the  vesicle.  Unfortunately,  the  determination  of  the  exact  point 
at  which  the  final  fashioning  of  the  swarmspores  is  accomplished 
often  proves  difficult  if  not  actually  impossible.  Moreover,  in 
at  least  one  species  {Phy.  palmivora  Butler)  germination  may  be 
at  times  typical  of  Pythium,  while  at  others  a  vesicle  is  absent 
and  the  swarmspores  escape  directly  from  the  sporangium.  It 
is  clear  that  this  character  used  alone  provides  at  best  an  unsatis- 
factory separation  of  the  two  genera. 

The  shape  of  the  sporangium  in  most  species  of  Pythium  may 
be  said  to  be  characteristically  more  nearly  spherical  than  in 
Phytophthora  where  it  is  usually  oval  to  obpyriform  and  papillate, 
but  so  many  intergrading  conditions  exist  that  shape  has  only 


PERONOSPORALES 


201 


relative  diagnostic  value.     Buisman  summarizes  the  situation 
with  the  statement  that  although  theoretically  no  sharp  line  can 


Fig.  72.- — Phytophthora  spp.  (a-e)  Germination  of  sporangium  by  swarmspores, 
the  spores  passing  first  into  a  vesicle.  (/)  Sporangiospores  which  failed  to 
escape  germinating  by  germ  tubes  in  the  sporangium,  (g)  Secondary  sporangia 
developed  at  tip  of  germ  tube  of  primary  sporangium,  (h)  Sporangiophores  of 
Ph.  phaseoli  arising  from  a  stomate  of  lima  bean,  (m)  Sporangiophore  of  Ph. 
infeatans.  (n)  Oospore  germinating  by  a  germ  tube  on  which  sporangia  then 
form,  (.s)  Oogonium,  basal  antheridium,  and  oospore  in  Ph.  erythro.^cptica. 
(t)  Oogonium,  lateral  antheridium,  and  oospore  in  Ph.  cactorum.  (u)  Germina- 
tion of  oospore  by  simple  germ  tube.  (/(,  after  Thaxter  1889;  m,  after  Schwarzc 
1917;  others  after  Rosenbaum  1917.) 


be  drawn  between  the  two  genera  it  is  usually  possible  in  practice 
to  determine  whether  a  given  form  belongs  to  the  Phytophthora 
type  or  to  the  Pythium  type. 


202  THE  LOWER  FUNGI— PHYCOMYCETES 

The  species  included  in  Phytophthora  arc  more  typically  para- 
sitic in  their  natural  habitat  than  those  embraced  in  Pythium, 
but  nearly  all  of  them  will  grow  on  artificial  culture  media.  In 
the  host  the  hyphae  are  intra-  as  well  as  intercellular,  and  in  the 
latter  case  bear  haustoria.  Usually  on  the  host  the  branches 
which  bear  sporangia  (Fig.  72)  protrude  from  the  stomates,  but 
in  culture  they  are  developed  indefinitely  over  the  surface  of  the 
medium.  Though  these  branches  are  termed  sporangiophores 
they  differ  little  if  any  from  the  vegetative  hyphae.  Their 
branching  is  sympodial  in  type,  terminally  produced  sporangia 
coming  to  occupy  a  lateral  position  due  to  further  apical  growth 
of  the  hypha.  The  production  of  sporangia  is  thus  successive 
and  differs  essentially  from  the  simultaneous  maturation  of 
sporangia  at  the  tips  of  a  specialized  sporangiophore  as  seen 
in  the  Peronosporaceae.  In  several  species  (Phy.  infestans, 
Phy.  phaseoli,  Phy.  thalictri)  a  slight  thickening  of  the  hypha 
occurs  immediately  below  the  point  of  attachment  of  the  spo- 
rangium, and  gives  it  a  characteristic  aspect,  but  this  is  absent 
in  other  species.  Germination  of  the  sporangium  by  means  of 
one  or  more  germ  tubes  may  occur,  and  in  some  cases  secondary 
and  even  tertiary  sporangia  may  be  formed  on  these  tubes. 
When  germination  by  swarmspores  takes  place  a  part  or  all  of  the 
spores  may  round  up  while  still  within  the  sporangium  and  ger- 
minate in  situ  by  germ  tubes.  The  sporangia  developed  in  the  air 
in  nature  fall  away  and  are  wind  borne,  but  those  developed  in 
culture  usually  germinate  while  still  attached  to  the  sporangio- 
phore. The  term  conidium  is  frequently  encountered  in  the 
literature  of  this  genus  and  has  been  applied  to  the  sporangium 
without  reference  to  its  method  of  germination.  Spherical, 
smooth,  thick-walled,  terminal  or  intercalary  spores,  usually 
yellowish  or  brownish  in  color,  are  sometimes  found  and  have  been 
termed  chlamydospores.  Investigators  have  interpreted  them 
in  different  ways :  as  resting  conidia,  as  parthenogenetic  oospores, 
etc. 

The  sexual  process  in  the  genus  is  in  one  respect  remarkable. 
Pethybridge  (1913  h)  demonstrated  that  in  some  of  the  species, 
designated  by  him  the  infestans  group,  the  antheridium  exists 
at  maturity  as  a  collar  around  the  base  of  the  oogonium.  The 
oogonium  is  initiated  beneath  the  antheridium,  perforates  its 
wall,  passes  into  its  interior,  grows  entirely  through  it,  emerges 
at  its  summit,  and  swells  out  there  to  form  the  spherical  portion  in 


PERONOSPORALES  203 

which  later  the  oospore  develops.  The  mature  sexual  apparatus 
thus  consists  of  a  balloon-shaped  oogonium  with  a  thick-walled 
oospore  in  its  upper  swollen  portion  and  with  its  funnel-shaped 
base  within  and  surrounded  by  the  antheridium.  Murphy 
studied  cytologically  a  member  of  this  group,  Phy.  erythroseptica, 
and  demonstrated  that,  following  the  protrusion  of  a  receptive 
papilla  (manocyst)  into  the  antheridium,  a  fertilization  tube 
enters  the  oogonium  and  discharges  into  it  a  single  male  nucleus 
which  later  fuses  with  a  nucleus  in  the  oosphere.  In  other 
species  of  the  genus,  designated  the  cadorum  group,  sexual 
organs  of  the  usual  oomycetous  type  are  developed,  the  antherid- 
ium being  applied  more  or  less  laterally  and  sending  into  the 
oogonium  a  fertilization  tube  as  in  Pythium.  Pethybridge, 
impressed  by  the  unique  type  of  sexuality  in  the  infestans  group, 
split  the  genus  PJujtophthora  into  two  and  applied  the  generic 
name  Nozemia  to  the  members  of  the  cadorum  group,  retain- 
ing Phytophthora  for  the  infestans  group  because  he  regarded 
Phy.  infestans  as  the  type  species  of  the  genus.  Wilson  went 
even  farther  and  suggested  the  recognition  of  a  new  family 
Phytophthoraceae  and  a  new  order  Phytophthorales  for  the  infes- 
tans group.  Since  the  sporangial  stage  is  wholly  similar  in  the  two 
groups,  and  since  this  vagary  of  the  sexual  process  constitutes 
the  only  difference  between  them,  the  spHtting  of  the  genus  was 
questionable  and  proved  to  be  premature.  Later  Lafferty  and 
Pethybridge  found  that  in  some  species  both  basal  (amphigynous) 
and  lateral  (paragynous)  antheridia  are  produced.  The  separa- 
tion of  tJie  groups,  therefore,  can  no  longer  be  justified  and 
Nozemia  has  been  abandoned.  Species  in  which  the  basal  type 
of  antheridium  is  known  include  Phy.  infestans,  Phy.  phaseoli, 
Phy.  erythroseptica,  Phy.  parasitica,  Phy.  arecae,  Phy.  cryptogea 
and  others  Only  the  lateral  type  has  been  observed  in  certain 
others. 

Although  the  observations  of  Pethybridge  concerning  the 
penetration  of  the  antheridium  by  the  oogonium  were  at  first 
received  with  scepticism,  the  observations  of  other  workers  and 
in  particular  the  cytological  study  by  Murphy  (1918)  have  cor- 
roborated his  statements.  Moreover,  Tabor  and  Bunting  (1923) 
have  described  and  figured  the  same  phenomenon  in  a  new  genus, 
Trachysphaera  Recently  Rose  and  Lindegren  (1925)  have 
figured  for  Phy.  cactoruni  oogonia  bearing  both  amphigynous 
and   paragynous   antheridia;   and   one   oogonium   bearing   two 


204  THE  LOWER  FUNGI— PHYCOMYCETES 

amphigynous  antheridia  is  pictured.  Such  cases  have  not  yet 
been  explained.  The  latter  case  would  appear  to  be  inexplicable 
in  the  light  of  Murphy's  account,  and  the  question  is  raised 
whether  the  amphigynous  antheridium  has  that  position  because 
the  oogonium  has  grown  through  it  or  for  some  other  reason 
such  as  the  coiling  of  the  antheridium  around  the  base  of  the 
oogonium  (Cooper,  1928;  Cooper  &  Porter,  1928).  No  cyto- 
logical  evidence  has  been  advanced  to  refute  the  observations  of 
Murphy,  who  in  the  study  of  serial  sections,  found  the  base  of 
the  oogonium  within  the  antheridium. 

A  satisfactory  basis  for  separation  of  species  within  the 
genus  Phytophthora  has  not  yet  been  found.  Many  species  have 
been  described,  but  the  identification  of  an  unknown  form  is  often 
difficult  if  not  actually  impossible.  A  number  of  specific  names 
at  present  applied  will  doubtless  in  time  be  place  in  synonymy. 
Tangible  morphological  characters  are  few  and  variable,  while 
separations  based  on  host  relationships  and  cultural  characters 
have  proved  inadequate.  A  thorough  taxonomic  revision  of  the 
genus  and  its  close  relatives  is  now  imperative. 

Considerable  taxonomic  work  has  been  done  on  the  genus  by 
Rosenbaum  (1915;  1917)  andLeonian  (1925).  The  former  author 
presents  a  key  separating  eleven  species.  In  his  studies  he  uses 
biometrical  methods,  and  bases  his  spore  and  sporangia!  measure- 
ments on  the  examination  of  hundreds  of  individuals.  His 
method,  while  perhaps  sound,  is  extremely  laborious  in  applica- 
tion. Leonian  presents  a  key  separating  eighteen  species  on  cul- 
tural characters.  The  presence  or  absence  of  sporangia  or  oogonia 
on  specified  media  afford  the  basis  for  separation.  Leonian 
(1927)  also  states  that  remarkable  modifications  in  the  mor- 
phology of  the  sporangium  take  place  when  a  given  species  is 
grown  on  various  hosts.  He  concludes  that  material  taken 
directly  from  the  host  for  identification  is  less  desirable  than 
that  developed  under  controlled  cultural  conditions  in  the 
laboratory.  More  recently  Leonian  and  Geer  (1929)  have  made 
a  comparative  study  of  the  size  of  sporangia  in  many  species, 
and  conclude  that  many  specific  names  now  used  must  be  thrown 
into  synonymy.  Workers  in  general  have  stressed  host  rela- 
tionships in  delimiting  species,  and  in  a  number  of  cases  new 
species  have  been  erected,  chiefly  because  new  hosts  were  involved. 

In  no  published  paper  have  all  the  described  species  been 
discussed  together.     At  present  thirty  or  more  species  exist  in 


PERONOSPORALES  205 

the  literature.  It  is  hoped  that  the  following  resume  will  serve 
to  put  the  reader  in  touch  with  the  general  situation. 

Phytophthora  infesians  (Mont.)  de  Bary  (1876)  is  the  cause  of 
the  widely  disseminated  and  extremely  destructive  late  blight  of 
potato,  and,  from  the  economic  standpoint,  is  the  outstanding 
species  of  the  genus.  It  is  now  found  wherever  the  host  is  grown. 
The  early  home  of  the  potato  is  not  certainly  known.  When 
first  introduced  into  Europe  it  was  apparently  free  from  the  blight 
but  later  the  disease  appeared  there  in  epiphytotic  form,  and  two 
outbreaks,  one  in  1845  (cause  of  the  Irish  Famine)  and  another 
in  1875  are  now  historical.  In  the  latter  year  the  celebrated 
German  mycologist  Anton  de  Bary  undertook  the  study  of  the 
disease,  and  the  pubhcation  (1876)  of  his  results  constitutes  the 
first  paper  of  importance  on  any  species  of  the  genus.  In  it  he 
erects  the  genus  Phytophthora  on  this  species.  He  describes  the 
sporangial  stage,  but  did  not  find  oospores.  He  states  that  the 
fungus  hibernates  in  the  tuber  in  the  mycelial  condition,  and 
grows  up  through  the  young  shoots  the  following  spring  giving 
a  systemic  infection  of  the  plant  above  ground.  The  English 
mycologist,  Worthington  G.  Smith  (1875;  1876  a,  b,  c)  described 
and  figured  the  oospores  stating  that  he  had  discovered  them  in 
the  leaves.  His  observations  were  not  substantiated  by  others 
and  his  account  fell  into  disrepute.  For  many  years  mycologists 
regarded  the  species  as  lacking  the  sexual  stage.  Finally  Clinton 
(1911  a,  6)  announced  that  he  had  obtained  oospores  in  pure 
culture  on  oat  agar,  and  others  have  since  succeeded  in  duplicat- 
ing his  results  (Briiyn,  1923).  Clinton  also  obtained  hybrid 
oospores  between  mycelia  of  Phy.  infestans  and  Phy.  phaseoli 
Thaxter.  More  recently  Murphy  (1927)  has  found  oospores  on 
the  surface  of  tubers  in  nature  The  species  is  not  confined  to 
the  potato.  It  occurs  also  on  tomato,  eggplant,  and  other  solana- 
ceous  hosts.  According  to  Berg  (1926)  the  fungus  on  tomato  is  a 
different  biological  strain  from  that  on  potato.  Important  papers 
on  the  species  have  been  published  by  Jones  (1912),  Clinton  (1905 
6;  1906  a),  Melhus  (1915  b),  and  Pethybridge  (1911  a;  1912; 
1913  c).  Although  Phy.  infestans  is  grouped  with  the  species 
characterized  by  amphigynous  antheridia,  the  oospores  are  in 
fact  usually  developed  in  the  complete  absence  of  antheridia. 
The  spores  are  then  termed  by  some  authors  chlamydospores. 

Phytophthora  phaseoli  Thaxter  (1889)  parasitic  on  the  lima 
bean,  Phaseolus  lunatus,  is  fully  treated  by  Clinton  (1906  b). 


206  THE  LOWER  FUNGI— PHYCOMYCETES 

The  fungus  attacks  the  pod  especially,  producing  a  woolly  white 
growth  of  sporangiophores  over  its  surface  (Fig.  77,  c).  The 
oospores  are  developed  in  the  seed  of  the  host.  Leonian  (1925) 
regards  the  species  as  a  variety  of  Phy.  infestans. 

Phyfophfhora  omnivora  de  Bary  (1881)  represents  the  merging 
and  treatment  under  a  new  name  of  three  previously  described 
species.  These  include  Peronos'pora  cactorum  Lebert  &  Cohn 
(1871),  described  as  causing  a  rot  in  two  species  of  cactus, 
Perofwspora  fagi  Hartig  (1876),  cause  of  damping-off  of  beech 
seedlings,  and  Peronospora  sempervivum  Schenk  (1875),  parasitic 
on  Sempervivum.  The  new  specific  name  omnivora  was  used  by 
de  Bary  without  regard  to  priority,  and  alludes  to  the  occurrence 
of  the  species  on  many  hosts.  Schroter  (1889)  revived  the 
older  name  cactorum,  and  is  responsible  for  the  binomial,  Phy~ 
tophthora  cactorum  (Lebert  &  Cohn)  Schroter.  At  present, 
in  the  absence  of  uniformity  of  opinion  concerning  specific 
limits,  Phy.  cactorum,  Phy.  fagi,  and  Phy.  om^iivora  may  be  found 
in  the  literature  treated  as  distinct  species  or  merged  in  various 
ways  with  each  other  or  with  still  other  forms.  Leonian  (1925) 
recognizes  Phy.  omnivora,  but  merges  with  it  Phy.  colocasiae, 
Phy.  palmivora,  Phy.  faheri,  Phy.  parasitica,  Phy.  terrestria, 
and  Phy.  parasitica  var.  rhei,  while  recognizing  Phy.  cactorum  as 
a  distinct  species.  In  England  a  rot  of  apples  and  pears  is 
attributed  by  Wormald  to  Phy.  o7nnivora.  Drechsler  states 
that  the  species  is  the  cause  of  a  foot  rot  of  lilies,  and  other  authors 
report  it  on  ginseng  (Rosenbaum,  1915),  strawberries,  rhubarb, 
and  other  plants. 

Phytophthora  palmivora  Butler  (1919)  cause  of  the  well  known 
bud  rot  of  Palmyra  palms  in  India  is,  perhaps,  not  specifically 
distinct  from  Phy.  meadii  McRae  (1918  a,  b)  and  Phy.  faheri 
Maublanc  (1909)  reported  from  Hevea  (rubber),  cocoa,  coconut, 
and  other  tropical  plants.     See  Gadd  (1927). 

Phytophthora  erythr  aseptic  a  Pethybridge  (1913  6;  1914)  causes 
a  pink  rot  of  potato  tubers  and  has  been  reported  from  Ireland, 
England,  Holland,  Switzerland,  and  Java. 

Additional  published  species  are  Phytophthora  agaves  Gandara 
(1909), PA?/,  alia  Sawada  (1915), P/i?/.  arecae  Pethybridge  (1913  h), 
Phy.  capsici  Leonian  (1922),  Phy.  carica  (Hara)  Hori  (in  Sawada, 
1919),  Phy.  citri  Rau  (1916),  Phy.  cinnamomi  Rand  (1922),  Phy. 
cryptogea  Pethybridge  &  Lafferty  (1919),  Phy.  colocasiae 
Raciborski  (1900),  Phy.  fici  Hori  (1915  in  Japanese:  see  Sawada, 


PERONOSPORALES  207 

1919),  Phy.  hihernalis  Came  (1927),  Phy.  hydrophila Curzi  (1927), 
Phy.  jatrophae  Jensen,  Phy.  lepironiae  Sawada  (1919),  Phy. 
melongenae  Sawada  (1915),  Phy.  mexicana  Hotson  &  Hartge 
(1923),  Phy.  nicoiianae  Breda  de  Hahn  (1896),  Phy.  paeoniae 
Cooper  &  Porter  (1928),  Phy.  parasitica  Dastur  (1913),  Phy. 
pini  Leonian  (1925),  Phy.  richardiae  Buisman  (1927),  Phy. 
syringae  Klebahn  (1909),  Phy.  thalidri  Wilson  &  Davis  (in 
Wilson,  1907  h),  and  Phy.  theohromae  Coleman  (1910). 

Several  genera  have  been  erected  on  species  which  do  not  seem 
to  differ  generically  from  Phytophthora.  One  of  these,  Phythia- 
cystis  Smith  &  Smith  (1906:  221)  was  founded  on  the  causal 
organism  of  the  destructive  brown  rot  of  lemon,  Pyth.  ciirophthora 
Smith  &  Smith,  and  has  remained  monotypic.  The  sexual 
stage  of  the  organism  has  not  been  observed,  but  the  characters 
of  its  mycehum  and  sporangia  show  it  to  be  intermediate  in 
many  respects  between  Pythium  and  Phytophthora;  the  habit 
being  as  in  the  former  and  the  morphology  as  in  the  latter  in  as  far 
as  differences  may  be  said  to  exist.  The  mycelium  in  the  para- 
sitic phases  on  the  host  plant  is  always  sterile.  In  the  soil  or 
in  soil  water  sporangia  occur  in  abundance.  Definite  sporangio- 
phores  are  not  formed.  The  sporangia  germinate  by  swarm- 
spores  or  by  germ  tubes,  in  the  former  case  deUmitation  taking 
place  in  the  sporangium  and  a  vesicle  being  absent.  The 
sporangia  are  frequently  asymmetrical,  and  two  or  more  papillae 
of  germination  are  sometimes  formed.  The  authors  of  the  genus 
and  others  (Barrett,  1917;  Leonian,  1925)  have  concluded  that 
the  species  may  well  be  incorporated  in  Phytophthora.  Leonian 
has  recently  made  the  transfer,  and  the  name  now  stands,  Phy. 
citrophihora  (Smith  &  Smith)  Leonian. 

The  genus  Kawakamia  Miyabe  (1903:  306)  was  estabhshed  in 
Japan  on  a  single  species,  K.  cyperi  (Miy.  &  Ideta)  Miyabe, 
found  on  Cyperus.  A  second  species,  K.  carica  Hara,  on  Ficiis 
carica,  was  described  later,  and  Phytophthora  colocasiae  Racib. 
was  transferred  to  the  genus  by  Sawada  (1919).  The  author  of 
the  genus  regarded  it  as  differing  from  Phytophthora  in  that  the 
sporangium  in  falling  away  carries  with  it  a  small  portion  of  the 
sporangiophore.  He  regarded  this  as  a  separate  cell  and  termed 
it  the  pedicel  cell.  The  sporangiophore  was  stated  by  him  to  be 
unbranched  or  only  slightly  and  indefinitely  branched.  As  the 
original  account  was  inadequate,  Sawada  (1919)  reinvestigated 
the  species,  and  gives  figures  which  show  the  genus  to  agree 


208  THE  LOWER  FUNGI— PHYCOMYCETES 

essentially  with  Phytophthora.  The  sporangiophore  branches  as 
in  that  genus,  and  sporangia  arise  successively.  The  pedicel 
cell  is  regarded  by  Sawada  (in  Tanaka,  1920)  as  being  merely  a 
thickening  of  the  wall  at  the  basal  end  of  the  sporangium. 
Earlier  Wilson  (1914  b)  had  treated  Kawakamia  as  a  well  defined 
genus  showing  relationship  with  Basidiophora.  The  writer  feels 
that  there  is  no  basis  for  separating  it  from  Phytophthora. 

The  genus  Blepharospora  Petri  (1918;  1924)  was  founded  on 
B.  camhivorai  Petri,  cause  of  the  inky  spot  disease  of  chestnuts 
in  Italy.  The  species  is  said  by  Petri  to  possess  a  long, 
unbranched  sporangiophore  terminated  in  a  single  sporangium. 
Further,  the  sporangiophores  are  said  to  develop  only  in  a  liquid 
medium.  Peyronel  (1920)  tr^nsierreA  Phy.  terrestria  ^hevhoko^ 
to  the  genus  as  B.  terrestris  (Sherb.)  Peyronel.  Other  species  of 
Phytophthora  are  closely  related  to  it.  Buisman  (1927)  advocates 
the  merging  of  Blepharospora  with  Phytophthora,  pointing  out  that 
there  is  in  fact  no  tangible  basis  of  separation.  She  uses  the 
binomial,  Phy.  camhivora  (Petri)  Buisman. 

The  genus  Pythiomorpha  Petersen  (1910)  founded  on  the  single 
species  Pythiomorpha  gonapodioides  Petersen  (Fig.  73),  is  made  the 
sole  representative  of  a  new  family,  Pythiomorphaceae,  by  Peter- 
sen. It  is  discussed  at  length  by  von  Minden  (1916),  Buisman 
(1927),  and  Kanouse  (1925).  The  vegetative  mycelium  occurs 
in  plant  substrata,  twigs,  fruits,  etc.,  immersed  in  the  water,  and 
forms  a  prominent  floating  white  mat.  The  hyphae  are  of  small 
diameter  and  are  provided  with  numerous  small  protuberances 
which  give  them  a  characteristically  irregular  appearance. 
Highly  refractive  granules,  believed  by  Petersen  to  be  cellulin, 
are  present  in  the  cytoplasm.  The  presence  of  these  granules 
and  the  somewhat  constricted  aspect  of  the  hyphae  have  led 
some  workers  to  regard  the  species  as  intermediate  between  the 
Pythiaceae  and  Leptomitaceae.  The  extramatrical  hyphae 
bearing  the  sporangia  are  cylindrical,  straight,  and  unbranched. 
The  sporangia  are  terminal,  ovate,  broader  below  and  somewhat 
narrowed  above,  and  have  a  definite  papilla  of  dehiscence.  They 
proliferate  repeatedly,  the  sporangia  which  foUow  the  primary 
being  developed  either  within  it  or,  by  further  growth  of  the 
hypha,  at  a  considerable  distance  beyond  its  mouth.  According 
to  von  Minden  the  swarmspores  are  delimited  in  a  thin-walled 
vesicle  at  the  apex  of  the  sporangium.  The  formation  of  the 
vesicle  is  denied  by  Kanouse.     The  swarmspores  are  reniform 


PERONOSPORALES 


209 


and  laterally  biciliate.  After  encyst ment  the  spore  may  emerge 
and  undergo  a  second  period  of  motility.  Oogonia  and  oospores 
resembling  those  of  Phytophthora  are  described  by  Kanouse.  The 
oospore  is  sometimes  developed  parthenogenetically.  Antheridia , 
when  present,  are  paragynous.  Although  the  irregular  hyphae, 
proliferating  sporangia,  repeated  swarmspore  emergence,  and 
saprophytic  and  aquatic  habit  are  characters  not  outstanding 
in  all  species  of  Phytophthora  they  occur  individually  in  various 
species  of  the  genus.     There  seems  to  be  no  tangible  basis  for 


Fig.  73. — Phytophthora  gonapodioidis  (Petersen)  Buisman.  (a)  Nested 
aspect  of  sporangia  resulting  from  proliferation,  {h)  Secondary  sporangium 
formed  beyond  primary,  the  inner  wall  of  the  latter  having  been  pulled  upward, 
(c)  Delimitation  of  swarmspores.  (d)  Swarmspore.  (e)  Mycelium.  (After 
Kanouse  1925.) 

separation  of  the  two  genera.  The  species  has  been  transferred 
to  Phytophthora  by  Buisman.  Recently  Apinis  (1930:  234) 
has  transfered  Pythium  undulatum  Petersen  to  Pythiomorpha. 

The  genus  Siigeosporium  West  (1916;  1917)  based  on  S.  marat- 
iiacearum  West,  having  a  mycorrhizal  relation  with  certain  ferns, 
is  as  yet  imperfectly  understood.  Though  regarded  by  its  author 
as  related  to  Phytophthora  it  seems  to  be,  in  fact,  wholly  dissimilar. 
The  peculiar  thick-walled  resting  spores  figured  by  West  recall 
those  of  Blastodadia  and  AUomyces. 

4.  Trachysphaera  Tabor  &  Bunting  (1923) 

This  extremely  interesting  genus  was  recently  founded  on  a 
single  species,  T.  fructigena  Tabor  &  Bunting  (Fig.  74),  cause 
of  a  disease  of  cocoa  and  coffee  fruits  in  the  Gold  Coast  Colony 
in  Africa.  The  sexual  stage  is  similar  to  that  of  the  //i/e.sta//.s' 
group  of  Phytophthora.  The  antheridium  forms  a  collar  about 
the  base  of  the  oogonium,  but  the  latter  is  ornamented  with 


210 


THE  LOWER  FUNGI— PHYCOMYCETES 


prominent  wart-like  or  sac-like  protuberances  which  give  it  a 
striking  appearance.  The  oospore  is  thin-walled.  Its  method 
of  germination  is  unknown.  The  asexual  stage  as  described  is 
unlike  that  of  any  other  member  of  the  order.  Hyphae  form  a 
subiculum  beneath  the  epidermis  of  the  host  from  which  a  dense 
mass  of  sporangiophores  arises.  The  epidermis  is  ruptured  and 
mealy  masses  of  sporangia  are  formed  on  the  surface  of  the  host. 
The  sporangiophore  is  variable  in  form.  In  its  simplest  type  it  is 
merely  an  erect  hypha  terminated  by  a  single  sporangium.  The 
tip  of  the  sporangiophore  is  usually  enlarged,  however,  to  form 


Fig.  74.^ — Trachysphaera  fructigcna  Tabor  &  Bunting,  (a)  Sporangiophore 
with  swollen  vesicle  (1)  bearing  a  whorl  of  spherical  cchinulate  sporangia  and 
two  other  vesicles  (2  and  3)  which  have  not  yet  borne  sporangia,  {b)  Rough- 
walled  oogonium  accompanied  by  an  amphigynous  antheridium.  (c)  Oogonium 
and  oospore  in  longitudinal  section.      (After  Tabor  and  Bmiting  1923.) 

a  more  or  less  globose  vesicle  from  which  a  number  of  sterigmata 
arise,  each  terminated  by  a  sporangium.  Some  of  the  sterigmata 
may  grow  farther  and  form  other  vesicles  bearing  additional 
sporangia.  The  sporangia  ("conidia")  are  spherical,  strikingly 
echinulate,  and  germinate  by  germ  tubes. 

The  presence  here  of  the  amphigynous  type  of  antheridium, 
hitherto  known  only  in  Phytophthora,  gives  the  genus  unusual 
interest.  This  is  especially  true  in  view  of  the  fact  that  the 
asexual  stage  is  unhke  that  of  other  members  of  the  Oomycetes 
and  recalls  that  of  certain  of  the  Mucorales.  The  proper  position 
of  the  genus  in  the  classification  is  perhaps  in  doubt. 


Peronosporaceae 

Mycehum  intercellular  in  higher  plants;  haustoria  developed 
and  variously  shaped  in  different  genera;  sporangiophores  definite 


PERONOSPORALES  2 1 1 

in  form,  branched,  arising  from  endophj^tic  mycelium,  protruding 
through  the  stomates,  and  bearing  the  sporangia  in  the  air; 
sporangia  deciduous,  disseminated  by  the  wind,  germinating  by 
swarmspores  or  germ  tubes;  sexual  organs  developed  in  the 
intercellular  spaces;  oogonia  monosporic;  oospore  germinating 
by  a  germ  tube. 

The  sporangiophores,  protruding  in  great  numbers  from 
the  stomates,  form  definite,  whitish,  grayish,  or  violet,  mouldy 
patches  on  the  surface  of  the  host.  The  same  thing  occurs  in 
some  species  of  Phytophthora  of  the  preceding  family.  The 
common  name  downy  mildews  was  applied  to  these  forms  to 
distinguish  them  from  the  powdery  mildews,  an  ascomycetous 
group  (Erysiphaceae). 

The  sexual  process  in  the  family  has  been  studied  cytologically 
in  several  species  representing  the  genera  Sclerospora,  Plasmopara, 
and  Peronospora.  In  general,  it  does  not  differ  strikingly  from 
that  described  above  for  Albugo  Candida.  A  receptive  papilla 
is  formed,  a  coenocentrum  is  differentiated,  and  a  true  fertiliza- 
tion, terminated  by  a  single  nuclear  fusion,  occurs.  A  critical 
consideration  of  the  details  of  the  process  in  the  various  forms 
studied  indicates  a  close  relationship  between  the  Albuginaceae 
and  Peronosporaceae,  and  suggests  the  probabihty  that  the  latter 
family  is  the  more  recently  developed  (Wager,  1900;  Stevens, 
1902;  Rosenberg,  1903;  Kriiger,  1910). 

Key  to  Genera  of  Peronosporaceae 

I.  Oospore   wall   confluent   with   that   of   the   oogonium;   sporangiophore 
typically  stout  with  heavy  branches  clustered  at  its  apex. 

1.  Sclerospora,  p.  212 

II.  Oospore  wall  not  confluent  with  that  of  the  oogonium;  sporangiophore 
typically  more  slender. 

A.  Sporangiophore  consisting  of  a  clavate  or  cylindrical  trunk  pro- 

vided  with    a   swollen    apex    from   which   short   sterigma-like 
branches  arise,  each  bearing  a  sporangium. 

2.  Basidiophora,  p.  214 

B.  Sporangiophore  provided  with  prominent  branches. 

1.   Branching  monopodial  to  subdichotomous. 

a.  Tips  obtuse;  branches  arising  more  or  less  at  right 

angles. 

3.  Plasmopara,  p.  215 

b.  Tips  more  acute;  branches  forming  more  or  less  acute 

angles. 

4.  Peronoplasmopara,  p.  218 


212  THE  LOWER  FUNGI— PHYCOMYCETES 

2.  Branching  dichotomoiis. 

a.  Tips  enlarged;  sporangia  apically  papillate. 

(1)  Tips  disc-like,   bordered   by  sterigmata  bearing 

sporangia. 

5.  Bremia,  p.  219 

(2)  Tii)s  merely  swollen. 

fi.  Bremiella,  p.  220 
b.   Tips  acute;  sporangia  not  papillate. 

7.  Peronospora,  p.  221 

1.  Sclerospora  Schroter  (1889:  236). 

Mycelium  intercellular,  bearing  small,  usually  knob-like, 
unbranched  haustoria;  sporangiophores  typically  stout  (Fig.  75), 
composed  of  a  main  trunk  and  a  compact  group  of  rather  short 
apical  branches  which  are  once  to  several  times  divided ;  branch- 
ing dichotomous  to  indefinite;  germination  of  sporangia  by  one 
or  more  germ  tubes  or  by  swarmspores;  oospores  unlike  those  of 
other  genera  of  the  family  in  that  the  exospore  is  confluent  with 
the  wall  of  the  oogonium;  method  of  oospore  germination 
undetermined  (Weston  and  Weber,  1928:  957;  Melhus,  Van 
Haltern,  and  Bliss,  1928:  335). 

The  genus  includes  about  twelve  species.  They  are  more  com- 
monly found  in  the  Orient  than  elsewhere.  Several  species  occur 
in  the  United  States.     The  majority  are  parasitic  on  Gramineae. 

The  type  species,  S.  graminicola  (Sacc.)  Schroter,  is  common  in 
the  United  States  on  various  species  of  foxtail  grass  {Setaria  or 
Chaetochloa)  and  has  been  reported  (Melhus,  Van  Haltern,  and 
Bhss,  1928:  304)  on  Zea  mays  (maize),  Euchlaena  mexicana  (teo- 
sinte),  Panicum  miliaceum,  and  Saccharum  officinarum.  In  other 
parts  of  the  world  its  host  range  is  similar.  The  species  is 
characterized  by  abundant  development  of  oospores  (estimated  at 
three  and  one-half  million  in  a  medium  sized  leaf)  and  a  poorly 
developed,  evanescent  sporangial  stage.  The  sporangia  are 
broadly  ellipsoidal  to  globose  and  germinate  by  swarmspores. 
The  sporangiophore  is  stouter  than  in  some  other  species,  the 
main  branches  being  few  and  stout,  and  the  terminal  branches 
conical.  In  later  stages  of  the  disease  the  terminal  portion  of  the 
host  plant  tends  to  take  on  a  characteristic  shredded  aspect.  This 
is  due  to  the  disintegration  of  the  tissue  between  the  vascular 
bundles  and  the  consequent  development  of  fibrous  tangles 
of  dry  bundles  from  which  the  oospores  are  gradually  scattered. 
The  inflorescence  is  often  transformed  by  the  development  of 
elongate,  leaf-like  bracts  which  replace  the  usual  floral  parts. 


PERONOSPORA  LES 


213 


The  whole  head  may  be  sterile  and  abnormally  green,  i.e., 
virescent.  (Stevens,  1902;  Butler,  1907;  Kulkarni,  1913;  Wilson, 
1907  6;  Weston  and  Weber,  1928;  Melhus,  Van  Haltern,  and 
Bliss,  1928,  Weston,  1929  a,  h,  c.) 

In  1921  S.  macroi^pora  Sacc.  long  known  in  Europe,  was  found 
on  wheat  in  Kentucky  and  Tennessee  (Weston,  1921  b).  It  has 
been  reported  also  on  Bronius  covinmtatus  in  America  and  on 
various  hosts  abroad.     Its  life  history  is  poorly  understood. 


Fig.  75.- — (a)  Sclerospora  spontanea  Weston,  (b-e)  S.  graniinicola  (Sivco.) 
Schrot.  (J-o)  S.  philippinensia  Weston,  (o)  Sporangiophore.  (6)  Sporansio- 
phores  emerging  from  stomate.  (c)  Young  sporangiophore.  {d)  Sporangiophore 
hearing  sporangia,  (e)  Oogonium  containing  oospore.  (/)  Intercellular  myce- 
lium with  haustoria.  {g)  Germinating  sporangium,  (e,  after  A.  Fischer;  others 
after  Weston.) 

Two  species  common  in  the  Philippines  on  maize,  S.  philippin- 
ensis  Weston  and  S.  spontanea  Weston,  have  been  studied 
critically  by  Weston  (1920;  1921  a;  1923  a,  h).  In  these  forms 
the  sporangiophore  is  more  slender  than  in  S.  graniinicola  and 
the  sporangia  much  more  elongated.  The  species  are  character- 
ized by  abundance  of  sporangia  and  absence  of  oospores,  the 
reverse  of  the  situation  in  S.  graminicola.  The  sporangia  ger- 
minate, moreover,  by  germ  tubes  instead  of  by  swarmspores  as  in 
that    species.     In    this   they   resemble   several   other   Oriental 


214 


THE  LOWER  FUNGI— PHYCOMYCETES 


species  (Butler,  1913  h)  also  found  on  maize.  The  relation  of 
sporangial  production  to  environmental  conditions  is  interesting. 
Sporangiophores  develop  only  at  night  and  protrude  through 
the  stomates  while  the  surface  of  the  host  is  covered  with  dew. 
Dispersal  of  sporangia  also  occurs  at  night,  and  seems  to  be 
accomplished  by  forcible  ejection  from  the  sterigmata. 

A  chart  listing  the  known  species  of  the  genus  and  indicating 
geographical  distribution,  host  range,  and  other  data  is  given  by 
Melhus,  Van  Haltern,  and  Bliss  (1928:  304). 


Fig.  76. — Ba^idiophora  eyitospora  Roze  &  Cornu.  (a)  Sporangiophores 
arising  from  stomate.  (6)  Oogonium  with  mature  oospore,  (c)  Sporangium 
liberating  swarmspores.     {After  Cornu  1869.) 


2.  Basidiophora  Roze  &  Cornu  [Ann.  Sci.  Nat.  (ser.  5),  11 :  84, 
1869]. 
Mycelium  intercellular;  haustoria  small  and  knob-like;  spo- 
rangiophore  consisting  of  a  cylindrical  unbranched  stalk  termi- 
nating in  a  clavate  enlargement  over  the  surface  of  which  short,. 


PERONOSPORALES  215 

cylindrical,    delicate    sterigmata    protrude    bearing    sporangia 
(Fig.  76). 

The  sporangium  is  almost  globose,  possesses  a  definite  apical 
papilla,  and  germinates  by  swarmspores.  Two  species  occur  in 
North  America,  B.  entospora  Roze  &  Cornu  on  Aster,  Solidago, 
Erigeron,  and  Leptilon,  and  B.  kellermanii  (Ellis  &  Halsted) 
Wilson  on  Iva  xanthifolia. 

3.  Plasmopara  Schroter  (1889:  236). 

Mycelium  intercellular;  haustoria  unbranched  and  knob-like; 
sporangiophores  (Fig.  78)  protruding  from  the  stomates,  erect, 
solitary  to  densely  fasciculate,  monopodially  branched,  the 
branches  arising  more  or  less  definitely  at  right  angles  to  the  main 
axis;  secondary  branches  also  at  right  angles;  the  terminal 
branches  apically  obtuse;  sporangia  small,  hyaUne,  papillate, 
germination  sometimes  by  germ  tube,  but  in  the  majority  of  cases 
by  swarmspores;  oospores  yellowish  brown;  the  epispore  wrinkled 
and  sometimes  somewhat  reticulate;  the  oogonial  wall  persistent, 
but  not  fused  with  the  epispore  as  in  Sclerospora  (Wartenweiler, 
1917;  1918  a,  b). 

Oospore  germination  has  been  observed  in  but  few  species. 
Gregory  (1912)  pictures  it  for  P.  viticola  (B.  &  C.)  Berl.  & 
De  Toni  (Fig.  77,  a,  b).  In  this  species  the  oospore  wall  cracks 
open  and  a  germ  tube  protrudes.  At  its  end  a  sporangium 
similar  to  the  summer  sporangium  is  cut  off,  and  germinates  by 
swarmspores.  A  similar  method  of  germination  is  to  be  expected 
in  other  species. 

The  genus  is  spht  by  Wilson  (1907  b)  into  two,  Rhysotheca 
Wilson  and  Plasmopara  (sensu  strictu).  The  majority  of  the 
species  are  incorporated  in  Rhysotheca.  One,  P.  pygmaea  (Unger) 
Schroter,  is  retained  in  Plasmopara.  In  it,  according  to  Wilson, 
swarmspores  are  not  produced.  Instead  the  sporangial  wall 
ruptures,  and  the  entire  protoplasmic  content  escapes  in  a  mass, 
forming  a  non-motile  protoplast  (perhaps  enveloped  in  the  endo- 
spore)  which  later  germinates  by  a  germ  tube.  Since  the  tips 
of  the  branches  of  the  sporangiophore  are  obtuse,  the  branching 
not  definitely  dichotomous,  and  the  sporangia  hyaline,  this 
pecuharity  of  germination  is  the  only  essential  point  in  which 
this  species  differs  from  those  assigned  to  Rhysotheca. 

The  genus  Pseudoplasmopara  Sawada  (1922:  77)  based  on 
Pseud,  jusliciae  Sawada  on  Justicia  procumbens  in  P'orniosa  is 


216 


THE  LOWER  FUNGI— PHYCOMYCETES 


Fig.  77.- — (a,  h)  Plasmopara  viticola  (Berk.  &  Curt.)  Berl.  &  dc  Toiii,  on  grape, 
(c)   Phylophthora  phaseoli  Thaxter,  on  lima  bean.     {Qriginal.) 


PERONOSPORALES 


217 


described  as  having  sporangia  and  sporangiophores  like  those  of 
Plasmopara  but  with  germination  always  by  germ  tube. 

As  the  method  of  germination  throughout  the  family  is  some- 
what inconstant  and  to  a  degree  dependent  on  the  conditions  of 
the  emdronment  it  seems  better  to  place  the  emphasis  in  generic 
separation  on  morphology  rather  than  on  differences  in  germina- 
tion. On  this  basis  the  genera  Rhysotheca  and  Pseudoplasmopara 
are  here  merged  with  Plasmopara. 


Fig.     78.- — Plasmopara     australis     Swingle.     Sporangiophore 
(After  Schwarze  1917.) 


and     sporangia. 


Approximately  fifteen  species  of  Plasmopara  are  known  for 
North  America.  Of  these  P.  viticola  (Berk.  &  Curtis)  Berl.  & 
De  Toni.,  cause  of  downy  mildew  of  cultivated  and  wild  grapes,  is 
best  known.  This  species  was  first  reported  from  the  United 
States  by  Schweinitz  in  1834.  It  apparently  originated  in  this 
country  on  the  wild  species  of  Vitis.  It  was  well  described  by 
Farlow  in  1876.  Two  years  later  it  was  discovered  in  the  vine- 
yards of  southern  France  and  very  quickly  became  a  menace  to 
the   grape   industry.     Its  rapid   spread   over  Europe   and  Asia 


218  THE  LOWER  FUNGI— PHYCOMYCETES 

Minor,  the  strenuous  efforts  to  stop  its  ravages,  and  the  incident 
and  accidental  discovery  of  bordeaux  mixture  are  now  well 
known  to  all  students  of  plant  pathology.  The  species  also 
occurs  on  the  Virginia  creeper  {Psedera  quinquefolia)  and  related 
plants.     Other  well  known  species  of  the  genus  are: 

PI.  geranii  (Peck)  Berl.  &  De  Toni — on  wild  Geranium. 

PI.  obducens  Schroter — on  Impatiens. 

PI.  halstedii  (Farlow)  Berl.  &  De  Toni — on  Ambrosia,  Bidens,  Erigeron, 
Eupatorium,  Helianthus,  Rudbeckia,  Silphium,  and  other  members  of  the 
Carduaceae.  This  species  has  not  been  sufficiently'  studied  taxonomicaUy 
and  perhaps  should  be  subdivided  into  several.  It  has  been  studied  cytolog- 
ically  by  Nishimura  (1926). 

PI.  viburni  Peck — on- Viburnum. 

PL  ribicola  Schroter — on  Ribes. 

PI.  pygmaea  (Unger)  Schroter — ^n  various  genera  of  the  Ranunculaceae. 

PI.  nivea  (Unger)  Schroter — on  various  genera  of  the  Umbelliferae.  It 
occurs  on  carrot  and  parsnip  and  has  been  reported  in  America  from 
(California. 

4.  Peronoplasmopara  Berlese,  in  Clinton  (1905  a:  329). 
syn.  Pseudopero7iospora  Rostowzew  (1903:  422). 

In  the  earlier  investigations  of  the  Peronosporaceae  two 
species,  Peronospora  cuhe^isis  B.  &  C.  and  Peronospora  celtidis 
Waite,  were  recognized  as  noteworthy  in  that  their  characters 
show  them  to  be  intermediate  between  Peronospora  and  Plasmo- 
para.  The  first  of  these  is  the  well  known  and  common  mildew 
of  cucurbits.  The  other  occurs  on  Celtis  occidentalis.  In  the 
monographic  treatment  of  the  family  by  Berlese  (1902:  123) 
both  species  are  incorporated  in  the  genus  Plasmopara,  a  new 
subgenus,  Peronoplasmopara,  being  established  there  for  their 
reception.  In  these  species,  the  sporangiophore  branches  in  a 
subdichotomous  manner,  the  branches  arise  at  acute  angles,  and 
the  terminal  branchlets  have  subacute  tips.  The  sporangia  are 
large  and  tinted  as  in  Peronospora,  but  have  a  prominent  papilla 
and  germinate  chiefly  by  swarmspores  as  in  Plasmopara. 

The  year  following  the  erection  of  the  subgenus  Peronoplas- 
7nopara  Berlese,  the  cucurbit  organism  Peronospora  cuhensis 
B.  &  C.  was  critically  studied  by  Rostowzew.  He  pubUshed  an 
extensive  discussion  of  it,  expressed  the  belief  that  it  represents 
a  distinct  genus  intermediate  between  Peronospora  and  Plasmo- 
para, and  applied  to  it  the  new  name  Pseudoperonospora  (Rostow- 
zew 1903:  422).  Although  he  contrasted  the  species  with  those 
of  Peronospora   and  Plasmopara,   he  failed   to   give   a   generic 


PERONOSPORALES  2 1 9 

diagnosis,  and  the  reader  is  left  in  some  doubt  as  to  the  essential 
characters  of  the  genus.  Article  38  of  the  International  Rules  of 
Botanical  Nomenclature  requires  that  a  diagnosis  accompany 
a  new  name  in  publication  Since  Rostowzew  made  no  reference 
to  the  subgeneric  diagnosis  of  Berlese  he  may  be  assumed  to  have 
been  ignorant  of  its  existence,  and  consequently  article  49  of  the 
Rules  relating  to  the  elevation  of  a  subgenus  to  generic  rank  does 
not  apply  (see  Curzi,  1926).  In  1905  CUnton,  reaUzing  this 
situation  and  feeling  that  Pseudoperonospora  would  not  stand, 
raised  the  subgeneric  name  Peronoplasmopara  Berlese  to  generic 
rank  and  pubhshed  a  generic  diagnosis.  CUnton  (1905  a:  334) 
discusses  the  situation  at  length,  and  the  writer  agrees  with  his 
conclusions.  The  name  Pero7ioplasmopara,  attributed  by  CUnton 
to  Berlese,  is,  therefore,  applied. 

Since  the  erection  of  the  genus  on  the  two  above  named  species, 
several  others  have  been  incorporated.  These  include  P.  humuli 
Miyake  &  Tak.,  the  hop  mildew,  and  P.  canahina  (Otth) 
PegUon,  the  mildew  of  hemp.  A  recently  described  species, 
P.  porioricensis  Lamkey  (see  Stevens,  1920)  differs  in  that  the 
sporangia  are  small  and  hyaline.  It  is  not  unlikely  that  the 
limits  of  the  genus  will  be  stiU  further  altered  to  include  other 
species.  Clinton  has  already  pointed  out  that  a  critical  study 
of  all  the  species  of  Plasmopara  and  Peronospora  may  show 
that  these  genera  grade  into  each  other  through  so  many  forms 
that  the  attempt  to  recognize  an  intermediate  genus  such  as 
Peronoplasmopara  will  only  add  to  the  difficulty  of  maintaining 
generic  separations.  Nevertheless,  at  present,  recognition  of  the 
genus  seems  justified. 

5.  Bremia  Regel  (1843). 

Mycelium  intercellular,  sending  unbranched  clavate  to  globose 
haustoria  into  the  host  cells;  sporangiophores  protruding  from 
the  stomates,  where  two  or  three  have  a  common  origin  in  a 
bulbous  swelling  of  a  single  hypha;  branching  definitely  dicho- 
tomous;  each  terminal  branchlet  broadened  at  its  tip  to  form  a 
shallow  saucer-shaped  disc  from  the  edges  of  which  several  short 
sterigmata  arise  each  bearing  a  sporangium;  sporangium  hyaline, 
with  an  apical  papilla  through  which  a  germ  tube  is  usually 
protruded. 

Rarely  germination  is  by  swarmspores  (Milbrath,  1923).  The 
best  known  species  B.  lactucae  Regel  (Fig.  79)  occurs  on  lettuce 


220 


THE  LOWER  FUNGI— PHYCOMYCETES 


and  other  Compositae.  It  is  sometimes  very  destructive  on 
cultivated  lettuce,  especially  in  the  greenhouse.  The  literature 
on  the  genus  is  scanty.  Recently  several  species  have  been 
described  from  the  Orient  by  Sawada  (1919)  and  Tanaka  (1919). 


Fig.  "!). — Brcinia  laclucuc  Reg.  Sijorangiophoro  and  sporangia   {After  Schwarze 

1917.) 


6.  Bremiella  Wilson  (1914  h:  195). 

This  is  a  monotypic  genus  based  on  Plasmbpara  megasperma 
Berlese  (1903),  occurring  on  violets.  The  branching  of  the 
sporangiophore  is  typically  dichotomous,  each  ultimate  branch 
being  swollen  at  the  apex  to  form  an  apophysis  (Berlese,  1903  :^gr. 
16).     The  sporangium  is  papillate  and  germinates  by  swarm- 


PERONOSPORALES 


221 


spores.  The  genus  may  be  regarded  as  intermediate  between 
Plasmopara  and  Bremia,  but  the  enlarged  tips  of  the  branches  of 
the  sporangiophore  are  not  disc-Uke  as  in  Bremia.  Each  bears 
but  a  single  sporangium. 

7.  Peronospora  Corda  (1837:  20). 

Mycelium  intercellular;  haustoria  in  a  few  species  short  and 
knob-like  but  in  the  majority  filamentous  and  more  or  less 
branched;  sporangiophore  consisting  of  an  erect  trunk  several 
(approx.    2-10)    times   dichotomously   branched,    the   branches 


Fig.    80. — Peronospora    effusa    (Grev.)    Rab.    Sporangiophore    and    sporangia. 
{After  Schwarze  1917.) 

more  or  less  reflexed  and  the  terminal  branchlets  sharp  pointed; 
the  habit  consequently  more  graceful  than  in  Plasmopara;  spo- 
rangia typically  larger  than  in  that  genus,  colored,  lacking  an 
apical  papilla  and  germinating  from  an  indeterminate  point  on 
the  side  by  a  germ  tube;  oospores  more  or  less  globose,  smooth 
or  variously  marked,  germinating  by  germ  tubes. 

Eriksson  (1918  h:  19)  states  that  in  P.  spinaciae  Laubert 
[  =  p.  effusa  (Grev.)  Tub]  the  oospore  is  not  a  hibernating  spore, 
but  germinates  in  situ  in  the  green  leaf  by  several  germ  tubes 
which  push  out  through  the  stomates  and  develop  an  aerial 
mycelium  from  which  sporangia  are  cut  off  (Fig.  80).  He  says 
further  that  these  sporangia  germinate  by  swarmspores.     His 


222  THE  LOWER  FUNGI— PHYCOMYCETES 

study,  dealing  chiefly  with  the  mycoplasm  hypothesis,  is  based 
largely  on  stained  cytological  preparations  rather  than  on  living 
material,  and  is  not  convincing.  However,  since  swarmspore 
formation  has  been  recently  described  in  Bremia  (Milbrath, 
1923:  991)  the  demonstration  of  its  occurrence  in  one  or  more 
species  of  Peronos'pora  would  not  be  wholly  unexpected. 

Peronospora  is  by  far  the  largest  genus  of  the  order.  Although 
Wilson  has  not  yet  monographed  the  species  of  North  America 
he  cites  over  forty  of  them  in  his  host  index  (Wilson,  1908  b:  543). 
Gaumann  (1923)  in  a  monograph  of  the  species  of  Switzerland 
lists  one  hundred  and  forty-two  species  of  which  nearly  seventy 
are  described  as  new.  He  subdivides  the  genus  into  four  groups 
as  follows : 

I.  Subgenus   Leiothecae   Schroter — Epispore    of   the   oospore    smooth    or 
indefinitely  wrinkled,  never  reticulate  or  verrucose. 

A.  Group  Parasiticae  de  Bary — Oogonial  wall  thick,  of  two  layers, 

not  collapsing  after  the  spore  matures. 

B.  Group  Effusae  de  Bary — Oogonial  wall  thin,  collapsing  after  the 

spore  matures. 
II.  Subgenus  Calothecae  de  Bary — Epispore  verrucose  or  covered  with  ridges 
which  may  or  may  not  anastomose. 

A.  Group  Verrucosae  A.  Fischer — Oospore  with  more  or  less  hemi- 

spherical warts  or  with  ridges  which  do  not  anastomose. 

B.  Group  Reticulatae  A.  Fischer — Oospore  with  a  regular  network 

of  anastomosing  ridges. 

The  species  in  each  group  are  separated  primarily  on  the  basis 
of  host  range,  the  species  in  each  host  family  then  being  separated 
by  differences  in  sporangial  measurements.  One  old  species,  P. 
parasitica  (Pers.)  Fr.  is  broken  up  (Gaumann,  1917)  into  approx- 
imately twenty  new  species  some  of  which  are  limited  to  a  single 
host.  The  results  of  cross  inoculation  work  correlated  with  minor 
differences  in  sporangial  measurements  provide  the  bases  for 
separation.  A  number  of  other  older  species  are  similarly  spht. 
The  paper  contains  an  extensive  bibliography  and  a  wealth  of 
information.  The  monographic  treatises  of  Schroter  (1889), 
Fischer  (1892),  and  Berlese  (1903),  while  older,  are  useful. 

Two  doubtful  South  American  genera  are  included  here  for 
reference,  Chlorospora  Spegazzini  (Rev.  Argentin.  Hist.  Nat., 
1891:  29)  and  Drepanconis  Schroter  &  Hennings  {Hedw. 
1896:  211).  The  first  was  based  on  Ch.  vastatrix  Speg.  reported 
from  onion  bulbs,  the  second  on  D.  brasiliensis  Schroter  &  Henn. 
occurring  on  leaves  and  branches  of  Nectandra. 


PERONOSPORALES  223 

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CHAPTER  IX 
MUCORALES 

Mycelium  profusely  developed,  filamentous,  richly  branched, 
when  young  coenocytic,  in  age  frequently  provided  with  trans- 
verse septa,  terrestrial,  usually  saprophytic,  in  some  species  para- 
sitic, consisting  of  nutritive  hyphae  buried  in  the  substratum 
and  aerial  hyphae  on  which  the  reproductive  bodies  are  usually 
borne;  the  aerial  mycelium  usually  prominent,  the  group  having 
been  designated  in  consequence  the  moulds;  thick-walled,  inter- 
calary, globose  to  barrel-shaped  chlamydospores,  and  thin-walled 
oidia  not  infrequently  formed  on  the  mycelium  (Lendner  1908  b: 
Jigs.  16-18);  sporangia  borne  on  specialized  sporangiophores, 
sometimes  accompanied  by  or  replaced  by  few-spored  sporangiola 
or  unicellular  conidia;  sexual  reproduction  accomplished  by  the 
conjugation  of  similar  gametangia  (coenogametes),  and  resulting 
in  the  formation  of  a  thick-walled  zygospore ;  azygospores  some- 
times developed  in  the  absence  of  the  sexual  fusion;  zygospore 
germinating  by  a  germ  tube  which  usually  bears  a  single  large 
apical  germ  sporangium;  swarmspores  absent  throughout  the 
group. 

In  the  lower  members  of  the  group  asexual  reproduction  is 
accomplished  by  means  of  sporangiospores  borne  in  large,  globose 
to  pyriform,  many-spored  sporangia.  The  septum  which 
delimits  the  sporangium  is  often  strongly  convex,  and  appears 
as  a  more  or  less  columnar  protrusion  of  the  sporangiophore 
into  the  sporangium.  This  apparent  protrusion,  termed  the 
columella,  usually  remains  in  position  after  the  sporangial  wall 
has  disintegrated,  and  the  spores  are  sometimes  found  adhering 
to  it. 

The  columella  does  not  result  in  fact  from  a  bulging  upward 
into  the  sporangium  of  a  transverse  septum.  It  is  formed  in  the 
position  in  which  it  lies  at  maturity,  and  is  laid  down  along  a 
prominent  cleavage  plane  in  the  cytoplasm.  Similar  cleavage 
planes  run  progressively  in  all  directions,  arising  from  the  col- 
umella, sporangial  wall,  and  vacuoles,  and  finally  cut  the  proto- 

234 


MUCORALES  235 

plasm  into  small  usually  uninucleate  bits.  These  are  then 
invested  in  walls  and  become  the  sporangiospores.  This  method 
of  spore  formation  is  tj^pical  of  all  sporangia,  and  contrasts  with 
the  phenomenon  of  free  cell  formation  by  which  ascospores  are 
formed  in  the  Ascomycetes.  The  details  of  the  two  processes 
are  given  by  Swingle  (1903)  and  Harper  (1899). 

In  the  Mucorales  as  in  the  Peronosporales  a  gradual  transition 
from  the  sporangium  to  the  conidium  is  evident,  endogenous 
spores  being  no  longer  developed  in  the  higher  forms.  In  inter- 
mediate conditions  the  sporangium  exists  as  a  deciduous,  few- 
spored  body  to  which  the  special  name  sporangiolum  is  applied. 
Although  it  is  evident  that  the  conidium  is  the  homologue  of 
the  sporangium  and  has  been  derived  from  it  in  some  cases  at 
least  directly  through  the  sporangiolum,  the  apphcation  of  the 
three  terms  to  the  three  types  of  structure  can  be  accompUshed 
without  appreciable  ambiguity  inasmuch  as  in  this  group  few 
confusing  border  line  conditions  are  encountered.  The  transition 
from  sporangium  to  sporangiolum  can  be  demonstrated  (Thaxter 
1914:  353)  in  Blakeslea,  while  in  Chaetocladium  and  Haplo- 
sporangium  the  origin  of  the  conidium  from  the  monospored 
sporangiolum  is  evident. 

In  the  majority  of  species  the  zygospore  is  formed  as  the 
result  of  the  fusion  of  two  gametangia  essentially  identical  in 
size  and  shape.  The  conjugation  process  begins  when  two 
hyphae  lying  in  contact  are  stimulated  to  develop  a  pair  of  lateral 
branches,  progametangia  (incorrectly  termed  progametes),  at 
their  point  of  contact.  These  branches,  which  are  thus  from 
the  beginning  adherent,  swell,  and  a  transverse  septum  forms  in 
each.  The  terminal  cell,  thus  delimited  in  each,  functions  as  a 
gametangium,  the  remainder  of  the  progametangium  being 
termed  the  suspensor.  The  wall  separating  the  two  gametangia 
is  then  broken  down  and  a  fusion  cell  (coenozygote)  results.  The 
zygospore  is  usually  formed  in  this  cell,  the  wall  of  the  cell  finally 
forming  the  outer  wall  of  the  spore.  In  the  Piptocephalaceae  the 
zygospore  forms  in  a  bud  which  develops  from  the  fusion  cell. 

It  has  long  been  known  that  in  some  species  of  the  Mucorales 
zygospores  occur  commonly  in  nature,  while  in  others  they  are 
found  infrequently  if  at  all.  Their  production  in  the  latter 
forms  was  assumed  by  earlier  investigators  to  depend  on  some 
special  condition  of  environm-cnt,  and  various  methods  of  induc- 
ing their  formation  were  followed,  none  of  which  could  be  relied 


236  THE  LOWER  FUNGI— PHYCOMYCETES 

upon.  Teachers  of  botany  desiring  to  use  the  common  bread 
mould  in  their  laboratory  work  as  illustrative  of  the  Zygomycetes 
were  often  at  a  loss  to  obtain  zygospores,  and  subcultures  from 
zygospore  producing  material  were  in  demand.  Even  these 
frequently  failed  to  develop  zygospores.  The  spontaneous 
appearance  of  zygospores  on  a  variety  of  media  and  under  widely 
different  conditions  was  wholly  unexplained. 

The  key  to  this  mystery  of  zygospore  production  was  dis- 
covered by  Blakeslee,  and  the  explanation,  though  entirely 
unexpected  was  very  simple.  Blakeslee  (1904:  205)  was  working 
on  the  problem  of  zygospore  formation  in  Mucor  mucedo  and 
obtained  pure,  zygospore  producing  cultures  on  agar.  He  found 
that  cultures  from  single  sporangia  of  this  material  never  pro- 
duced zygospores,  but  that  if  a  mass  of  mycelium  was  transferred, 
zygospores  appeared  in  abundance  about  the  point  of  inoculation, 
decreasing  in  number  as  the  growth  widened.  It  was  found  also 
that  mixed  sporangial  transfers  from  the  center  of  the  mass  gave 
origin  to  zygospores,  while  similar  transfers  from  the  margin  of 
the  growth  failed  to  do  so.  The  culture  which  made  clear  the 
fundamental  nature  of  zygospore  production  was  prepared  in  the 
endeavor  to  discover  whether  the  tendency  to  develop  zygospores 
could  be  transmitted  through  the  mycelium  derived  from  the 
germination  of  a  single  sporangiospore.  For  this  purpose  dilution 
cultures  were  made  from  mixed  sporangial  transfers  from  the 
center  of  a  zygospore  group,  one  petri  dish  thus  prepared  contain- 
ing only  five  spores.  When  the  five  mycelia  which  developed 
from  these  spores  met,  it  was  seen  that  an  abundant  growth  of 
zygospores  occurred  along  the  line  of  apposition  of  certain  of  the 
myceha,  while  between  others  none  were  formed.  This  culture 
showed,  moreover,  that  a  given  mycelium  would  produce  zygo- 
spores when  meeting  a  second  mycelium,  and  fail  to  do  so  on 
meeting  a  third,  which  would  form  them  on  meeting  the  second. 
Thus  the  culture  indicated  not  only  that  two  mycelia  arising  from 
different  spores  are  necessary  for  the  production  of  zygospores, 
but  also  that  these  spores  are  developed  from  the  union  of 
mycelia  which  are  different  in  nature.  Blakeslee  confirmed  these 
results  by  numerous  observations  on  Mucor  mucedo,  and  extended 
his  investigation  to  other  members  of  the  order.  He  found  that 
the  majority  of  the  Mucorales  examined  are  of  the  type  of  Mucor 
mucedo,  and  he  designates  these  as  heterothallic  forms,  because 
two  different  thalli  are  necessary  for  zygospore  formation.     In 


MUCORALES  237 

these  forms  any  given  thallus  bears  sporangiospores  which  give 
rise  to  thalH  of  the  same  nature  as  the  parent  thallus.  He  has 
cultivated  the  opposite  strains  of  Phycomyces  nitens  and  Mucor 
mucedo  by  means  of  sporangiospores  for  more  than  one  hundred 
asexual  generations  without  any  apparent  change  in  their  sexual 
behavior.  The  two  different  strains  of  a  heterothallic  form  can 
sometimes  be  distinguished  by  a  slight  difference  in  the  luxuri- 
ance of  their  growth,  although  they  are  otherwise  morphologically 
indistinguishable.  On  account  of  this  distinction  the  terms  plus 
(+)  and  minus  (  — )  were  suggested  by  Blakeslee  for  the  two 
strains.  Although  he  believed  the  difference  to  be  a  sexual  one, 
he  was  unable  to  state  which  strain  was  male  and  which  female. 

In  a  few  species  of  the  Mucorales  the  zygospores  were  found 
to  arise  by  the  interaction  of  hyphae  of  a  single  mycehum  derived 
from  the  germination  of  a  single  spore.  Blakeslee  termed  such 
forms  homothallic.  To  this  group  belong  Sporodinia  grandis, 
Spinellusfusiger,  Zygorhynchus  spp.,  Dicranophora  fulva,  Absidia 
spinosa,  and  a  few  species  of  Mucor,  while  the  heterothalHc 
group  includes  Rhizopus  nigricans,  Mucor  mucedo,  Phycomyces 
nitens,  Absidia  caerulea  and  a  very  considerable  number  of  others. 

Blakeslee  made  the  further  very  interesting  observation  that 
imperfect  hybridization  (the  production  of  the  early  stages  of 
zygospores  which  never  mature)  will  take  place  between  opposite 
strains  of  different  heterothalHc  species  and  between  both 
(+)  and  (  — )  strains  of  heterothalHc  species  on  the  one  hand, 
and  homothallic  species  on  the  other.  A  homothalHc  species 
placed  between  the  two  strains  of  a  heterothalHc  species  may, 
therefore,  give  rise  to  two  lines  of  imperfect  zygospores.  This 
power  of  hybridization  between  different  species  of  the  Muco- 
rales has  made  it  possible  to  place  in  the  proper  category  of 
(_|_)  or  (  — )  the  strains  of  such  heterothallic  forms  as  Mucor 
mucedo  in  which  there  is  no  visible  difference  in  the  luxuriance 
of  the  two  strains.  It  also  makes  possible  the  determination 
of  the  (+)  or  (  — )  character  of  the  thalH  in  those  heterothallic 
species  in  which  only  one  strain  has  been  obtained  for  study. 

The  results  obtained  by  Blakeslee  (1906  a)  in  the  germination 
of  zygospores  have  proved  of  particular  interest.  In  the  Mucor- 
ales the  germ  tube  which  arises  from  the  zygospore  usually 
bears  a  single  sporangium  termed  the  germ  sporangium,  though  it 
may  occasionally  produce  a  branching  mycelium.  The  examina- 
tion of  the  spores  in  the  germ  sporangium  with  reference  to  their 


238  THE  LOWER  FUNGI— PHYCOMYCETES 

(+)  and  (  — )  character  is  especially  instructive.  The  conditions 
presented  in  the  germ  sporangium  as  determined  for  the  three 
species,  Mucor  mucedo,  Sporodinia  grandis,  and  Phycomyces  nitens 
represent  three  distinct  types.  The  conditions  are  summarized 
by  Blakeslee  as  follows: 

1.  The  germination  of  the  zygospores  of  the  homothallic  species,  Sporo- 
dinia grandis,  is  pure  homothalHc,  all  the  spores  of  the  germ  sporangium  on 
germination  developing  homothallic  mycelia. 

2.  The  germination  of  the  zygospores  of  the  heterothallic  species,  Mucor 
jnucedo,  gives  rise  to  germ  sporangia  in  which  all  the  spores  are  aUke,  either 
(  +  )  or  (— ).  Segregation  of  sex  is  accomplished  at  some  point  before  the 
formation  of  the  sporangiospores,  and  a  single  zygospore  produces  a  germ 
sporangium  containing  spores  of  but  one  sort. 

3.  In  the  germination  of  the  zygospores  of  the  heterothallic  species, 
Phycomyces  nilens,  segregation  of  se.x  occurs  preceding  the  formation  of  the 
sporangiospores  but  is  only  partial.  As  a  result  the  germ  sporangium  con- 
tains in  addition  to  (+)  and  (  — )  spores,  a  few  spores  which  on  germination 
give  rise  to  homothallic  mycelia  characterized  by  the  production  of  con- 
torted aerial  outgrowths  termed  pseudophores  and  the  occasional  forma- 
tion of  homothallic  zygospores.  The  sexual  character  in  these  homothallic 
mycelia  is  unstable  and  in  their  sporangia  segregation  again  occurs  and 
(+)  and  (  — )  spores  and  others  which  develop  homothallic  mycelia  are 
produced.  Finally  the  homothallic  condition  disappears.  It  is  interesting 
to  note  that  there  is  apparently  no  definite  numerical  ratio  between  the  (-)-) 
and  ( — )  spores  formed  in  the  germ  sporangium,  and  it  sometimes  even 
happens  that  all  the  spores  are  of  one  sort. 

If  from  analogy  with  other  fungi  segregation  of  sex  may  be 
assumed  to  occur  in  these  moulds  during  the  heterotypic  mitosis, 
it  is  evident  that  this  division  does  not  occur  at  the  same  point 
in  the  life  cycle  of  every  species;  nor  does  it  occur  in  all  of  the 
diploid  nuclei  of  a  given  species  at  the  same  time.  This  is 
evidenced  by  the  presence  of  (  +  ),  (  — ),  and  "bisexual"  spores  in 
the  same  germ  sporangium  in  Phycomyces.  If  a  number  of  pairs 
of  nuclei  fuse  in  the  mature  zygospore  of  Phycomyces  as  described 
by  Keene  (1919)  the  presence  of  "bisexual"  spores  in  the  germ 
sporangium  might  be  explained  as  due  to  the  fact  that  certain 
of  the  nuclei  retain  their  diploid  character  longer  than  others. 
This  assumption  has  not  as  yet  been  sustantiated  by  cytological 
observations. 

Blackman  (1906)  objects  to  the  use  of  the  term  sexual  in 
connection  with  the  fusion  of  the  gametangia  in  the  Mucorales. 
He  states  that  the  term  sex  as  applied  to  organisms  in  general 
cannot    be    used    where    the   fusing   cells   are    morphologically 


MU COR  ALES  239 

identical.  For  such  cases  he  prefers  the  term  syngamy  (syn- 
gametic).  Blakeslee  (1906  b)  feels  that  the  similarity  of  the 
gametangia  does  not  in  the  least  detract  from  his  conclusion  that 
the  differentiation  into  (+)  and  (  — )  strains  is  a  sexual  one.  He 
points  out  that  the  use  of  the  term  isogamy  (the  conjugation 
of  equal  gametes  in  which  no  differentiation  of  sex  can  be  dis- 
tinguished) has  only  a  morphological  application  among  the 
Mucorales,  since  sexually  the  two  gametangia  which  unite  have 
diametrically  opposite  characters.  The  mutual  indifference  of 
two  mycelia  of  the  same  sex  and  the  active  sexual  reaction 
between  mycelia  of  opposite  sex  which  leads  to  the  formation  of 
zygospores  when  the  mycelia  are  of  the  same  species,  indicate 
that  the  gametes  are  fundamentally  different.  In  no  species, 
however,  either  homothallic  or  heterothallic,  in  which  the 
process  of  conjugation  has  been  carefully  followed,  do  the 
progametangia  grow  toward  each  other  as  has  been  commonly 
believed.  They  arise  from  the  stimulus  of  actual  contact 
between  hyphae  which  touch  each  other,  and  are  from  the  very 
beginning  adherent. 

In  order  to  determine  the  sexual  identity  of  the  (  +  )  and  (  — ) 
strains,  and  to  enable  him  to  substitute  the  terms  male  and 
female,  Blakeslee  (1913;  1915)  has  performed  some  interesting 
experiments.  In  the  heterothallic  group  no  species  has  been 
discovered  in  which  the  gametangia  differ  constantly  in  mor- 
phology. The  differences  in  size  occasionally  noted  in  Rhizopus 
nigricans  and  others  are  neither  constant  nor  correlated  with 
the  (-(-)  and  (  — )  condition.  In  the  homothallic  group  several 
well  known  species  are  heterogametangic,  the  gametangia  differing 
strikingly  in  size  and  shape.  To  this  category  belong  Zygorhyn- 
chus  moelleri,  Zy.  heterogamus,  Absidia  spinosa,  and  Dicranophora 
fulva.  Blakeslee  feels  that  from  analogy  with  the  Oomycetes 
the  larger  gametangium  may  be  considered  female  and  the  smaller 
male.  Upon  this  basis  if  a  sexual  reaction  could  be  established 
between  these  unequal  gametangia  and  the  (  +  )  and  (  — )  strains 
of  a  heterothallic  species,  the  strain  reacting  with  the  larger 
female  cell  would  be  considered  male,  and  that  reacting  with 
the  smaller  male  cell  would  be  considered  female.  Only  a  single 
heterogametangic  species  (Absidia  spinosa)  was  found  which 
would  give  reactions  with  both  (  +  )  and  (  — )  strains,  and  only 
a  single  heterothallic  species  {Mucor  hiemalis)  which  would 
react  with  both  male  and  female  gametangia  of  this  heterogamic 


240  THE  LOWER  FUNGI— PHYCOMYCETES 

honiothallic  species.  The  difficulties  of  technique  encountered 
in  following  the  sexual  reactions  in  a  tangle  of  filaments 
were  overcome  by  growing  the  homothallic  species  in  a  petri 
dish  between  the  (  +  )  and  (-)  strains  of  the  heterothalhc 
species,  and  cutting  channels  in  the  agar  between  the  different 
thalH.  The  reacting  filaments  could  then  be  studied  in  mid-air 
in  the  channels.  It  was  found  that  the  sexual  reaction  occurs 
between  the  larger  female  gametangium  and  the  (  — )  strain 
on  the  one  hand,  and  between  the  smaller  male  gametangium 
and  the  (  +  )  strain  on  the  other.  Therefore  the  conclusion 
is  reached  that  the  (+)  strain  of  the  heterothalhc  species  is 
female  and  the  ( - )  strain  male.  Subsequently,  in  his  laboratory 
a  study  of  the  biochemical  differences  between  strains  has 
tended  to  substantiate  this  conclusion  (Satina  and  Blakeslee, 
1926  a,  h;  1927). 

A  good  resume  of  the  work  on  various  aspects  of  sexuality 
in  the  group  was  given  by  Blakeslee  (1920  b).  In  later  years 
other  investigators  have  somewhat  broadened  the  field  of  our 
knowledge  in  the  Mucorales,  and  Blakeslee's  prediction  that 
heterothalhc  forms  would  be  discovered  in  other  groups  of  the 
fungi  has  been  fulfilled  in  the  Saprolegniales,  Peronosporales, 
and  other  groups  both  of  the  lower  and  higher  fungi. 

In  several  genera  of  the  Mucorales  species  exists  which  are 
parasitic  on  other  members  of  the  order.  Burgeff  (1924)  has 
studied  several  of  these  forms  critically  and  advances  the  inter- 
esting hypothesis  that  they  have  become  parasitic  as  a  result 
of  attempts  at  hybridization.  He  found  that  in  the  case  of 
Mucor  (Parasitella)  simplex  the  (  +  )  strain  parasitizes  only  the 
(  — )  strain  of  the  host  Ahsidia  glauca,  while  the  (  — )  strain  para- 
sitizes only  the  (  +  )  strain.  In  other  cases  the  experimental 
results  are  less  conclusive,  and  Satina  and  Blakeslee  (1926  6) 
question  the  possibility  of  a  wide  application  of  the  theory. 

The  nuclear  phenomena  which  accompany  conjugation  of  the 
gaemtangia  and  maturation  of  the  zygospore  are  as  yet  imper- 
fectly understood.  The  small  size  of  the  nuclei  and  the  presence 
of  a  large  amount  of  oil  in  the  zygospore  render  the  problem 
of  staining  a  difficult  one.  A  considerable  number  of  forms 
have  been  investigated,  but  the  published  accounts  are  con- 
tradictory, incomplete,  and  unconvincing.  All  students  of  the 
group  have  agreed  that  the  progametangia  and  young  game- 
tangia  are  multinucleate,  and  several  describe  the  disintegration 


MUCORALES  241 

of  supernumerary  nuclei.  Dangeard  (1906  a,  b),  Moreau 
(1911  a,  b,  c;  1912  a,  b;  1913  a,  b),  and  Keenc  (1914;  1919) 
describe  nuclear  fusions  in  the  young  zygospore  between  many 
pairs  of  nuclei,  while  Lendner  (1908  a)  and  McCormick  (1912) 
find  evidence  indicating  that  only  a  single  nuclear  fusion  occurs. 
Dangeard  and  McCormick  describe  cytoplasmic  bodies  com- 
parable to  the  coenocentrum  of  the  Peronosporales,  and  the 
latter  author  states  that  the  two  nuclei  present  in  the  mature 
zygospore  lie  embedded  in  the  coenocentrum.  Keene,  on  the 
other  hand,  regards  these  bodies  as  undoubtedly  related  to  the 
elaioplasts  found  in  many  other  plants,  which  have  for  their 
function  the  elaboration  of  oil  for  reserve  food.  They  occur 
in  considerable  numbers  in  the  young  zygospore,  progressive 
fusions  resulting  ultimately  in  the  formation  of  one  or  two 
large  bodies  saturated  with  oil.  The  mature  zygospore  is  often 
practically  filled  with  oil,  the  cytoplasm  and  nuclei  being  confined 
to  a  thin  parietal  layer  next  to  the  wall.  Following  nuclear 
fusion  it  is  assumed  that  reduction  division  occurs  in  the  zygo- 
spore before  germination,  but  the  facts  have  not  been  determined. 
Perhaps,  as  described  for  Albugo,  some  species  characterized  by 
a  single  nuclear  fusion  and  others  by  a  multiple  fusion  occur  in 
this  group.  It  is  particularly  unfortunate  that  the  extremely 
interesting  and  suggestive  experimental  data  of  Blakeslee  can- 
not now  be  explained  from  cytological  data. 

The  order,  Mucorales,  as  here  constituted  contains  seven 
families,  approximately  thirty  genera,  and  about  four  hundred 
described  species.  The  most  satisfactory  general  taxonomic 
treatments  of  the  group  are  those  of  Fischer  (1893)  and  Lendner 
(1908  b). 

Key  to  Families  of  Mucorales 

I.  Sporangium  when  present  globose  to  pyriform,  many-spored,  in  some 
genera  accompanied  by,  in  others  replaced  by,  few-spored  sporangiola 
or  unicellular  conidia;  zygospore  formed  in  the  fusion  cell  which  results 
from  the  copulation  of  the  gametangia. 

A.  Sporangium  when  present  containing  a  columella;  zygospore  not 
enveloped  by  a  layer  of  interwoven  hyphae. 
1.  Sporangium  always  formed;  sporangiola  and  conidia  lacking. 

a.  Sporangial  wall  thin,  not  cutiiiizod. 

1.  Mucoraceae,  p.  242 

b.  Sporangial  wall  heavily  cutinized  in  the  upper  portion. 

2.  Pilobolaceae,  p.  251 


242  THE  LOWER  FUNGI— PHYCOMYCETES 

2.  Sporangium  either  accompanied  bj-  or  replaced  by  sporan- 
giola  or  conidia. 

a.  Sporangium  present,  accompanied  by  sporangiola,  both 

usuall}-  formed  on  the  same  sporangiophore. 

3.  Thamnidiaceae,  p.  253 

b.  Sporangia   often    absent;    when    present   sohtary,    not 

borne  on  the  same  sporangiophore  with  sporangiola  or 
conidia. 

(1)  Sporangium  absent;  conidia  covering  sub-termi- 

nal enlargements  of  branches  of  the  conid- 
iophore. 

4.  Chaetocladiaceae,  p.  257 

(2)  Sporangium  present  in   some  genera,   absent  in 

others;  sporangiola  or  conidia  present  in  all 
cases,  and  covering  terminal  capitate  enlarge- 
ments of  the  branches  of  the  sporangiophore  or 
conidiophore. 

5.  Choanephoraceae,  p.  258 
B.   Sporangium  when  present  lacking  a  columella;  zygospore  where 

known  enveloped  by  a  thick  layer  of  interwoven  hyphae;  spo- 
rangiola and  conidia  formed  in  some  cases,  when  present  isolated, 
not  covering  an  enlargement  on  the  sporangiophore  or 
conidiophore. 

6.  Mortierellaceae,  p.  264 
II.  Sporangium    narrowly    cylindrical   or   rod-like,    relatively    few-spored; 

sporangiospores  arranged  in  a  single  row,  at  maturity  having  the 
aspect  of  a  chain  of  conidia  due  to  the  dissolution  of  the  sporangial 
wall;  zygospore  usually  formed  in  a  bud  put  out  by  the  fusion  cell 
which  results  from  the  copulation  of  the  gametangia. 

7.  Piptocephalaceae,  p.  270 


Mucoraceae 

Large,  globose  to  pyriform,  multispored  sporangia  formed  in 
all  genera,  not  shot  away;  sporangiola  and  conidia  lacking; 
sporangial  wall  thin,  not  cutinized;  zygospore  not  enclosed  in  a 
definite  hyphal  envelope. 


Key  to  Genera  of  Mucoraceae 

Sporangiophore  indeterminate,  elongating  indefinitely,  branching  in  a 
cymose  manner,  not  bearing  a  terminal  sporangium;  branches  circi- 
nate;  sporangial  wall  persistent. 

A.  Sporangium  pvriforni;  columella  liourglass  shaped. 

1.  Pirella,  p.  243 

B.  Sporangium  globose;  columella  cylindrical  to  conical. 

2.  Circinella,  p.  244 


MU  COR  ALES  243 

II.  Sporangiophore  determinate,  simple  or  branched,  terminal  sporangium 
always  formed;  branches  only  rarely  circinate;  sporangial  wall 
evanescent. 

A.  Sporangiophores  arising  from  aerial,  arching  stolons  which  develop 

rhizoids  at  points  of  contact  with  the  substratum. 

1.  Sporangiophores   borne   on   the   arching   internodes   of   the 

stolons    between    the    rhizoid-bearing    nodes;    sporangia 
pyriform. 

a.  Suspensors  of  the  zygospore  provided  with  prominent 
circinate  outgrowths. 

3.  Absidia,  p.  244 
h.   Suspensors  lacking  outgrowths. 

4.  Mycocladus,  p.  245 

2.  Sporangiophores  arising  in  a  fascicle  from  the  node  of  the 

stolon  opposite  the  tuft  of  rhizoids;  sporangia  globose. 

5.  Rhizopus,  p.  245 

B.  Sporangiophores  arising  directly  from  the  mycelium. 

1.  Aerial  mycelium  ornamented  with  short,  lateral,  thorn-like 

branches. 

6.  Spinellus,  p.  246 

2.  Aerial  mycelium  lacking  such  thorn-like  branches. 

a.  Sporangiophore  branching  repeatedly  at  the  apex  in  a 
dichotomous  fashion;  zygospores  borne  on  similarly 
branched  aerial  zygophores. 

7.  Sporodinia,  p.  247 

h.  Sporangiophore  unbranched,  or  branching  in  a  monopo- 
dial  or  sympodial  manner;  zygospores  borne  on  the 
mycelium. 

(1)  Sporangiophore   unbranched,    stiffly   erect,    with 

metallic  iridescence;  suspensors  of  zygospore 
provided  with  rigid  dichotomously  branched 
outgrowths. 

8.  Phycomyces,  p.  248 

(2)  Suspensors  lacking  definite  outgrowths. 

(a)  Gametangia  strikingly  dissimilar. 

9.  Zygorhynchus,  p.  249 

(b)  Gametangia  essentially  alike. 

10.  Mucor,  p.  250 

1.  Pirella  Bainier  (1883:  84). 

Sporangiophore  elongating  indefinitely,  not  bearing  a  terminal 
sporangium,  branching  in  a  cymose  manner;  the  branches  cir- 
cinate, terminated  by  pyriform  sporangia;  sporangial  wall 
persistent,  incrusted  with  crystals  of  calcium  oxalate;  columella 
very  large,  shaped  like  an  elongate  hourglass;  zygospores 
unknown. 

The  genus  is  imperfectly  known,  containing  only  the  type 
species,  P.   circinans  Bainier.     It   corresponds   with   Circinella 


244  THE  LOWER  FUNGI— PHYCOMYCETES 

except  in  the  shape  of  the  sporangium  and  columella,  and  may 
represent  merely  an  atypical  member  of  that  genus. 

2.  Circinella  van  Tieghem  &  le  Monnier  (1873:  298). 
Sporangiophore  elongating  indefinitely,  not  bearing  a  terminal 

sporangium,  branching  in  a  cymose  manner;  the  branches 
circinate,  single  or  in  groups,  terminated  by  globose  sporangia; 
sporangial  wall  persistent,  incrusted  with  crystals  of  calcium 
oxalate,  finally  rupturing  in  such  a  manner  as  to  leave  a  promi- 
nent collar  at  the  base  around  the  columella;  columella  large, 
cylindrical  to  conical. 

Lendner  (1908  h:  101)  includes  seven  species  in  the  genus,  and 
others  have  been  described  since  {Saccardo  Syll.  Fung.,  24 :  1926). 
In  C.  iimbellata  zygospores  are  described  by  Bainier  (1903:  170). 

3.  Absidia  van  Tieghem  (1876:  350). 

Mycelium  forming  repeatedly  branched,  arching  stolons, 
rooted  at  points  of  contact  with  the  substratum;  sporangiophores 


Fig.  81. — Absidia  glauca  Hagem.     Zygospore  with  circinate  outgrowths  arising 
from  the  suspensors.      {After  Lendner  190S.) 

erect,  straight,  usually  in  fascicles,  more  rarely  single,  arising 
from  the  elevated  arching  internodes  of  the  stolons,  not  opposite 
the    rhizoids;    sporangia    terminal,    pyriform;    sporangial    wall 


MUCO  RALES  245 

neither  incrusted  nor  thickened,  thin,  soon  disintegrating; 
columella  conical  to  hemispherical,  with  a  papillate  apical 
prolongation  which  is  sometimes  drawn  out  into  a  rather  long 
spine;  sporangiospores  small;  zygospores  borne  on  the  stolons; 
one  or  both  suspensors  provided  with  prominent  circinate  out- 
growths which  tend  to  envelope  the  zygospore  (Fig.  81). 

The  genus  contains  about  twenty  species.  In  its  sporangial 
characters  it  corresponds  with  Mycocladus,  and  in  its  possession 
of  stolons  recalls  Rhizopus.  The  genera  Tieghemella  Berlese 
&  de  Toni  (Saccardo  Syll.  Fung.,  7:  215,  1888),  Proabsidia 
Vuillemin  (1903  h:  119),  Pseudoabsidia  Bainier  (1903:  153), 
and  Lichtheimia  Vuillemin  (1903  6:  119)  are  here,  as  in  Lendner 
(1908  b:  129),  merged  with  Absidia. 

4.  Mycocladus  Beauverie  (Ann.  bniv.  Lyon,  3:  1900). 
Corresponding  with  Absidia  in  mycelial  and  sporangial  char- 
acters, but  differing  in  that  the  suspensors  of  the  zygospore  lack 
circinate  outgrowths. 

The  genus  contains  only  the  type  species,  M.  verticellatus 
Beau  v.,  but  species  tentatively  included  in  Absidia,  in  which 
zygospores  are  as  yet  unknown,  may  later  be  found  to  belong  here. 
The  genus  is  merged  with  Absidia  by  Lendner  (1908  b:  129). 

5.  Rhizopus  Ehrenb.  (Nova  Acta  Acad.  Leopold.,  10:  198,  1820). 
Aerial  arching  stolons  developed  from  the  nutritive  mycelium 

as  in  Absidia,  at  points  of  contact  with  the  substratum  forming 
a  tuft  of  repeatedly  branched  rhizoids  (Fig.  82) ;  sporangiophores 
arising  from  the  stolon  exactly  opposite  the  point  of  origin  of  the 
rhizoids,  usually  unbranched  and  fasciculate;  sporangia  terminal, 
large,  globose,  many-spored;  columella  prominent,  more  or  less 
hemispherical;  sporangial  wall  not  cutinized,  at  maturity  almost 
wholly  disappearing;  sporangiospores  globose  to  oval  or  angular, 
smooth  or  marked  by  longitudinal  striations,  rarely  echinulate; 
zygospores  formed  from  the  nutritive  mycelium  or  from  the 
stolons;  suspensors  lacking  outgrowths  (Fig.  83). 

A  rather  large  genus  containing  approximately  thirty  species 
the  best  known  of  which  is  R.  nigricans  Ehrenberg,  type  of  the 
genus.  In  the  papers  of  Pound  (1894:  98),  Wilson  (1906:  560), 
Sumstine  (1910:  129),  and  Povah  (1917:  248)  the  nomenclatorial 
problem  presented  by  this  species  is  discussed.  In  the  treatment 
of  Sumstine  it  is  made  the  type  of  the  genus  Mucor,  the  name 


246 


THE  LOWER  FUNGI— PHYCOMYCETES 


Rhizopus  disappears  entirely,  and  Hydrophora  Tode  includes  the 
species  usually  placed  in  Mucor. 


Fig.  82. — Rhizopus  nigricans  Ehrenberg.  (a)  Fascicle  of  eporangiophores 
arising  opposite  the  rhizoids,  and  connected  by  a  stolon  with  another  group. 
(6)  Sporangium  enlarged  to  show  columella  and  spores.      {After  Atkinson  1908.) 


Fig.  83.^ — Rhizopus  nigricans  Ehrenberg.  (a)  Adjacent  hyphae  united  by 
young  progametangia.  {b)  Progametangia.  (c)  Gametangia  and  suspensors. 
{d)  After  fusion  of  gametangia.      (e)  Mature  zygospore.      {Original.) 

For  a  taxonomic  separation  of  species  consult  Lendner  (1908) 
and  Hanzawa  (1914:  230). 

6.  Spinellus  van  Tieghem  (1875:  66). 

Vegetative  mycelium  buried  in  the  substratum,  consisting  of 
delicate,  hyaline  hyphae;  aerial  mycelium  well  developed,  brown, 


MUCORALES 


247 


profusely  branched,  ornamented  with  short,  lateral,  thorn-like 
branches;  sporangiophore  erect,  unbranched,  usually  tapering  to 
a  swollen  base,  bearing  a  single,  terminal,  globose  sporangium; 
sporangial  wall  delicate,  hyaline,  not  incrusted;  columella 
rounded  to  nearly  cylindrical;  zygospores  borne  only  on  the 
thorny  mycelium;  suspensors  not  thorny,  having  the  appearance 
of  tongs,  not  twining,  developing  the  zygospore  between  their 
ends. 


Fig.  84. — SpineUus  macrocarpus  Corda  on  Mycvna  pradonga  Peck.   {Original.) 

A  small  genus  of  four  or  five  species,  parasitic  on  Agaricaceae 
and  other  higher  fungi  (Fig.  84).  It  is  incorporated  in  Mucor  by 
Schroter  (1893:  125),  but  is  given  generic  rank  by  Fischer  (1892: 
220)  and  Lendner  (1908  6:  51). 

7.  Sporodinia  Link,  in  Linnaeus  Species  Plantarum  (4  edit.) 
6:  94,  1824;  also  see  Tulasne  {Compt.  Refid.  Acad.  Paris 
15:617,1855). 

syn.  Syzgites  Ehrenberg  {Sylvae  Myc.  Berol,  p.  25.  1818). 
Mycelium  not  forming  stolons,  profusely  developed,  occasion- 
ally septate;  sporangiophores  erect,  abundantly  septate,  branch- 
ing at  the  apex  repeatedly  in  a  dichotomous  fashion;  each  branch 


248 


THE  LOWER  FUNGI— PHYCOMYCETES 


terminated  by  a  more  or  less  globose  sporangium ;  sporangial  wall 
neither  cutinized  nor  incrusted.  very  thin  and  soon  disintegrat- 
ing; columella  large,  hemispherical;  sporangiospores  spherical, 
smooth,  dark  brown;  zygospores  developed  on  specialized  erect, 
dichotomously  branched,  aerial  hyphae,  termed  zygophores; 
copulating  branches  lateral  on  the  zygophore;  the  zygospore 
formed  between  their  tips  as  in  Mucor;  species  homothaUic 
(Fig.  85). 


Fig.  85. — Sporodinia  grandis  Link,  (a)  Sporangiophore  and  sporangia,  (fe) 
Zygophore  showing  conjugating  gametangia.  (c)  Gametangia  and  suspensors. 
{d)  Mature  zygospore,  (a,  after  Lendner  1908;  b,  after  de  Bary  1864;  c,  d,  after 
Keene  1914.) 

Link  based  his  description  of  Sporodinia  on  the  sporangial 
stage  alone.  The  zygophore  and  zygospore  were  described  earlier 
by  Ehrenberg  who  founded  the  genus  Syzgites  on  them.  Tulasne 
emended  the  generic  description  of  Sporodinia  to  include  both 
stages,  and  Brefeld  later,  by  germinating  the  zygospores,  proved 
that  the  two  stages  do  in  fact  arise  from  the  same  mycelium. 

The  species  ;S.  grandis  Link,  type  of  the  genus,  is  apparently 
the  only  known  species,  it  having  been  included  in  the  genus 
under  a  considerable  number  of  specific  names  by  various 
students. 

8.  Phycomyces  Kunze  and  Schmidt  {Mycol.  Hefte,  2 :  113,  1823). 
Mycehum  wide-spreading  in  and  on  the  substratum,  richly 
branched;  stolons  absent;  sporangiophores  simple,  stiffly  erect, 
possessing  a  pronounced  metallic  iridescence,  often  exceptionally 
tall,  reaching  a  length  in  some  cases  of  ten  or  twelve  inches, 
though  usually  shorter;  sporangia  terminal,  large,  globose,  with 
a  pyriform  apically  broadened  columella;  sporangial  wall  not 


MU  COR  ALES  249 

cutinized,  somewhat  incrusted  with  crystals  of  calcium  oxalate, 
soon  disintegrating;  sporangiospores  smooth,  yellowish,  ellip- 
soidal; zygospores  formed  on  the  mycelium;  copulating  branches 
shaped  like  tongs  and  forming  the  zygospore  between  their  tips; 
suspensors  provided  with  dichotomously  branched,  dark  brown, 
rigid  outgrowths,  which  radiate  in  various  directions  and  have 
the  aspect  of  antlers  (Fig.  86),  not  enclosing  the  zygospore  as  in 
Ahsidia. 


Fig.  8G. — Phycomyces  riitens  (Agardh)  Kunze.  (a)  Early  stage  in  conjugation 
showing  outgrowths  arising  from  one  of  the  suspensors.  (6)  Same  somewhat 
later,  (c)  Mature  zygospore;  the  outgrowths  from  the  suspensors  rigid  and 
dichotomously  branched,  (o,  after  Blakeslee,  1904;  b,  after  Keene  1919;  c, 
after  van  Tieghem  and  le  Monnicr  1873.) 

The  best  known  species  is  P.  nitens  (Agardh)  Kunze  & 
Schmidt.  At  least  five  other  species  have  been  recognized:  P. 
splendens  Fries,  P.  microsporus  van  Tieghem,  P.  pirottianus 
Morini,  P.  spinulosus  Morini,  and  P.  hlakesleeanus  Burgeff . 

9.  Zygorhynchus  Vuillemin  (1903  a:  116). 

Sporangial  stage  as  in  Mucor;  zygospore  formed  in  a  charac- 
teristic manner  from  wholly  dissimilar  gametangia  (Fig.  87); 
all  species  homothallic;  genus  merged  with  Mucor  by  Lendner 
(1908  6:72). 

The  genus  contains  relatively  few  species:  Z.  heterogamus 
Vuillemin  (1903  a:  117);  Z.  moelleri  Vuillemin  (1903  a:  117), 
Z.  vuilleminii  Namyslowski  (1910  h:  152),  Z.  dangeardi  Moreau 
(1912  a:  67),  Z.  hernaldi  Moreau  (1913  c\  256),  Z.  japonicus 
Kominami  (1914:  3). 

The  details  of  zygospore  formation  are  discussed  by  Gruber 
(1912:  126),  Atkinson  (1912:  151),  and  Blakeslee  (1913:  241). 
The  terminal  portion  of  an  erect  hypha  is  delimited  by  a  septum 
from  the  part  below.  A  lateral  branch  then  pushes  out  just 
beneath  the  septum,  grows  upward,  and  recurves  to  meet  the  side 


250 


THE  LOWER  FUNGI— PHYCOMYCETES 


of  the  main  hypha  above  the  septum.  At  the  point  of  contact 
the  main  hypha  pushes  out  and  cuts  off  a  small  gametangium. 
The  much  enlarged  tip  of  the  lateral  branch  cuts  off  the  other. 
The  zygospore  formed  by  their  union  is  thus  always  homothallic 
in  origin.  The  termination  of  the  main  hypha  is  often  turned 
to  one  side,  and  projecting  beyond  the  zygospore  as  a  slender 
prolongation  gives  the  zygophoric  apparatus  a  characteristic 
aspect. 


Fig.    87.^ — Zyoorhynchus    heterorjamiis    Vuillemin.      (a-g)    Successive    stages    in 
conjugation  terminating  in  formation  of  zygospore.      {After  Blakeslee  1913.) 

10.  Mucor  Micheli,  in  Nova  Plantarum  Genera,  p.  215,  pi.  95, 1729; 

also  see  Link  in  Linnaeus  Species  Plantarum  (4  edit.),  6:  80, 

1824. 

syn.  Hydrophora  Tode  {Fung.  Meckl.,  2:  5,  1791). 
Mycelium  developed  profusely  both  in  and  on  the  substratum, 
lacking  definite  rhizoids  and  stolons;  sporangiophores  not  fascic- 
ulate as  in  Rhizopus,  arising  singly  from  the  mycelium,  erect, 
simple  or  somewhat  branched  in  a  monopodial  or  sympodial 
manner;  all  the  branches  terminated  by  sporangia;  sporangia 
large,  globose,  many-spored;  sporangial  wall  evanescent  in  most 
species,  not  cutinized,  more  or  less  incrusted  with  crystals  of 
calcium  oxalate;  columella  always  present,  various  in  shape; 
sporangiospores  globose  to  ellipsoidal,  with  a  thin,  smooth  wall; 
zygospores  borne  on  the  mycelium;  suspensors  lacking  out- 
growths; copulating  branches  lying  end  to  end,  forming  a  straight 


MUCORALES  251 

line,  not  having  the  tongs-Hke  aspect  seen  in  certain  other  genera; 
terminal  or  intercalary,  smooth,  hyaline  chlamydospores  found 
in  some  species. 

The  genus  is  the  largest  in  the  Mucorales,  over  one  hundred  and 
fifty  species  being  described  by  Saccardo  (Sylloge  Fungorum) 
for  the  world,  and  over  fifty  by  Lendner  (1908  b)  for  Switzerland. 
The  genus  is  a  difficult  one  for  the  taxonomist.  Notes  of  interest 
on  American  species  are  given  by  Povah  (1917). 

The  genera  Parasitella  Bainier  (1903:  153),  Chlamydomucor 
Brefeld  (1889:  223;  also  see  Calyptromyces  Karst.  in  Sumstine 
1910:  145),  and  Glomerula  Bainier  (1903:  154)  are  here  embraced 
in  Mucor  (see  Lendner  1908  6:  69,  71,  77). 

Pilobolaceae 

!  Sporangium  discoid  to  lenticular,  multispored,  in  most  species 
provided  with  a  prominent  sub-sporangial  vesicle  and  at  maturity 
shot  way;  lower  portion  of  sporangial  wall  thin  and  light-colored; 
upper  part  heavily  cutinized  and  black;  sporangiola  and  conidia 
lacking;  zygospore  not  enclosed  in  a  definite  hyphal  envelope, 
formed  at  the  point  of  union  of  conjugating  branches  which 
have  the  aspect  of  closed  tongs. 

Key  to  Genera  of  Pilobolaceae 

I.  Sporangiophore  provided  with  a  large  subsporangial  vesicle;  sporangium, 
accompanied  by  columella,  forcibly  discharged  from  the  sporangio- 
phore at  maturity. 

1.  Pilobolus,  p.  251 
II.  Sporangiophore  lacking  a  subsporangial  vesicle;  sporangium  not  shot 
away. 

2.  Pilaira,  p.  253 

1.  Pilobolus  Tode  (Schrift.  Naturf.  Freimde  Berlin,  5:  46,  1784). 

syn.  Hydrogera  Web.  &  Wigg.  {Prim.  Fl.  Holstat.,  p.  110, 

1780);  see  Sumstine  (1910:  136). 

Sporangiophore  erect,  unbranched,  apically  enlarged  to  form 

a  prominent,  clavate,  subsporangial  vesicle  (Fig.  88),  frequently 

also  swollen  at  its  point  of  origin  from  the  mycelium,  usually 

separated  from  the  mycelium  by  a  septum  and  anchored  to  the 

substratum  by  rhizoids;  sporangium  solitary,  apical,  discoid  to 

lenticular,  many-spored;  provided  with  a  central  columella  of 

much  smaller  diameter  than  the  subsporangial  swelling,  the  upper 

half  of  the  membrane  thickened  and  black,  the  lower  half  thin 


252 


THE  LOWER  FUNGI— PHYCOMYCETES 


and  light  colored;  the  mature  sporangium  discharged  with 
violence  from  the  end  of  the  sporangiophore,  commonly  projected 
for  several  feet,  the  columella  being  carried  away  with  it;  zygo- 
spore formed  at  the  point  of  union  of  conjugating  branches  which 
lie  in  such  a  position  as  to  give  the  appearance  of  a  pair  of  tongs. 
The  genus  contains  a  dozen  or  more  species.  It  is  particularly 
interesting  on  account  of  the  phenomenon  of  sporangial  discharge 
which  anticipates  conditions  in  the  following  order,  where  such 
a  discharge  commonly  occurs.  An  entertaining  discussion  of 
the  mechanism  which  accomplishes  discharge  is  given  by  Buller 


Fig.  88. — Pilobolus  crystallinus  (Wiggers)  Tode.  (a)  Sporangiophore,  sub- 
sporangial  vesicle  and  sporangium,  (b-d)  Stages  in  zygospore  formation. 
(After  Zopf  1888.) 


(1921).  He  finds  that  the  neck  of  the  subsporangial  vesicle 
ruptures  just  beneath  the  sporangium,  and  that  sudden  contrac- 
tion of  the  sporangiophore  results  in  the  squirting  out  of  a  jet  of 
cell  sap  on  which  the  sporangium  is  carried  through  the  air.  His 
experiments  have  demonstrated  also  that  the  vesicle  functions  as 
an  ocellus  (simple  eye),  and  directs  the  tip  of  the  sporangiophore 
toward  the  light  in  order  that  the  sporangium  may  be  discharged 
out  of  the  crevices  of  the  substratum  into  the  lighted  open. 
These  fungi  are  found  in  nature  on  dung  of  herbivorous  animals, 
and  the  spores  germinate  only  after  passing  through  the  alimen- 
tary canal.  The  surface  of  the  sporangial  wall  is  adhesive.  The 
sporangium  falling  on  the  grass  or  other  herbage,  adheres,  is  later 
eaten  by  the  browsing  animal,  and  enabled  to  complete  its  life 


MUCORALES  253 

cycle.  It  is  essential,  therefore,  that  the  sporangium  be  dis- 
charged toward  the  Hght  rather  than  into  the  crevices  of  the 
substratum.  The  subsporangial  vesicle  functions  as  a  lens  in 
much  the  same  way  as  does  a  flask  filled  with  water.  If  the  rays 
of  the  sun  strike  on  one  side  of  the  vesicle  they  are  refracted 
through  it  and  converge  on  the  opposite  side  forming  a  spot  of 
light.  The  protoplasm  at  that  point  receiving  thus  a  heliotropic 
stimulus,  growth  and  elongation  occur  on  that  side  of  the  sporan- 
giophore.  In  consequence  the  sporangium  is  turned  toward  the 
light  until  the  rays  strike  it  head  on.  A  condition  of  physio- 
logical equilibrium  is  then  reached  and  the  turning  movement 
ends. 

2.  Pilaira  van  Tieghem  (1875:  51). 

Sporangiophore  erect,  unbranched,  lacking  a  subsporangial 
vesicle;  sporangium  terminal,  not  shot  away,  when  young  globose; 
the  membrane  in  the  upper  hemisphere  black  and  thickened  as  in 
Pilobolus,  below  thin,  hyaline,  at  maturity  greatly  distended,  and 
finally  disappearing;  columella  flat  to  globose,  not  falling  away; 
zygospore  formed  as  in  Pilobolus,  the  conjugating  branches  erect 
and  tending  to  twine  about  each  other. 

At  least  four  species,  all  of  them  from  dung,  have  been  described 
in  this  genus.  The  possibility  that  they  were  based  on  abnormal 
material  of  Pilobolus,  leads  the  writer  to  regard  the  genus  as 
somewhat  doubtful. 

Thamnidiaceae 

Sporangia  and  sporangiola  formed  together,  usually  on  the 
same  sporangiophore;  sporangium  large,  multispored,  thin- 
walled,  and  provided  with  a  columella;  sporangiolum  much 
smaller,  lacking  a  columella,  provided  with  a  thicker  persistent 
wall,  and  faUing  away  at  maturity;  zygospore  not  enclosed  in  a 
hyphal  envelope. 

Key  to  Genera  of  Thamnidiaceae 

I.  Spores  in  the  sporangium  differing  in  size  and  shape  from  those  in  the 
sporangiola;  sporangiolum  clasped  at  the  base  by  several  sharp- 
pointed  claw-like  branches. 

1.  Dicranophora,  p.  254 
II.  Spores  in  sporangium  like  those  in  sporangiola;  branch  bearing  sporan- 
giolum lacking  terminal  claw-like  projections. 

2.  Thamnidium,  p.  25(5 


254 


THE  LOWER  FUNGI— PHYCOMYCETES 


1.  Dicranophora  Schroter  (Jahresb.  Schles.  Gesell.  Vaterl.  Culiur, 
64:  184,  1886). 

Mycelium  imbedded  in  or  creeping  over  the  substratum,  giving 
rise  to  erect,  sparingly  septate  sporangiophores  bearing  sporangia 
and  sporangiola  (Fig.  89);  sporangiophore  simple  or  branched, 
when  simple  terminated  by  a  single  large  many-spored  spo- 
rangium; several  such  sporangia  sometimes  formed  on  a  single 
sporangiophore  as  the  result  of  cymose  branching ;  sporangiophores 
usually  provided  with  lateral  branches,  which  divide  repeatedly 


Fig.  89. — Dicranophora  fulva  Schroter.  (a)  Sporangiola.  (h)  Spore  from 
sporangiolum.  (c)  Sporangiophore  bearing  one  sporangium  and  several  spo- 
rangiola.     (d)  Sporangium.      (After  Schroter  1893.) 


in  a  dichotomous  fashion,  the  ultimate  branchlets  being  ter- 
minated by  small  few-spored  sporangiola;  large  sporangium 
provided  with  a  central,  conical  columella,  and  containing  many 
small  ellipsoidal  spores  unusually  variable  in  size;  sporangiolum 
containing  only  one  or  two  large  reniform  spores  and  lacking  a 
columella;  zygospores  globose,  naked,  formed  from  very  unequal 
gametangia. 

When  the  sporangiolum  falls  away  the  tip  of  the  sporangio- 
phore is  seen  to  be  provided  with  two  or  three  incurved  claw-like 
projections.  These  have  been  erroneously  regarded  by  various 
workers  as  constituting  a  columella.  Their  true  nature  is  eluci- 
dated by  Vuillemin  (1907:  33). 


MU  COR  ALES 


255 


The  genus  was  based  on  the  single  species,  D.  fulva  Schroter, 
found  on  PaxiUus  in   Baden.     Another  collected   by  Thaxter 


Fig.  90.- — (a,  h)  Thamnidium  simplex  Brefeld,  showing  terminal  sporangium 
and  lateral  sporangiola.  (c,  d)  Th.  fresenii  Schroter,  showing  terminal  sporan- 
gium, sporangiola,  and  sterile  spines,  (e)  Th.  elegans  Link  showing  sporangiola. 
{After  Brefeld  1881,  1891.) 

on  Boletus  in  Maine  is  discussed  by  Blakeslee  (1904:  300)  but  is 
not  named.  The  genus  is  of  unusual  interest  on  account  of  the 
dimorphism  of  spores  in  the  two  sorts  of  sporangia. 


256  THE  LOWER  FUNGI— PHYCOMYCETES 

2.  Thamnidium  Link  (Berl.  Mag.  Naturf.  Freunde,  3:  31,  1809). 

syn.  Ilelicostylum  Corda  p,  p.  (Icon.  Fung.,  5:  18,  55,  1842). 

Bulbothamnidium  Klein  p.  p.  (1870:  557). 

Chaetostylum  van  Tieghem  &  le  Monnier  p.  p.  (1873: 

328). 

Sporangiophore  erect,  consisting  of  a  cylindrical  central  axis, 

usually  terminated  by  a  single,  large,  many-spored  sporangium, 

and    lateral    branches    bearing    numerous,    small,    few-spored 

sporangiola   (Fig.   90);   lateral   branches  usually  several  times 

divided;  the  ultimate  branchlets  straight  or  circinate,  terminating 

in    sporangiola,    or    tapering    into    sterile   spines;    sporangium 

provided  with  a  prominent  columella;  sporangiolum  lacking  a 

columella,  containing  one  to  twenty  or  more  (usually  about  four) 

spores;  spores  alike  in  both  sorts  of  sporangia;  zygospores  as 

far  as  known  formed  as  in  Mucor  from  approximately  equal 

gametangia. 

Individual  sporangiophores,  bearing  only  sporangiola,  and 
others,  bearing  only  the  terminal  sporangium,  are  not  infrequently 
encountered.     Three  subgenera  are  recognized  here. 

Subgenus  Euthamnidium  Schroter  (1893:  127). 

Lateral  branches  of  the  sporangiophore  typically  dichoto- 
mously  branched,  the  ultimate  branchlets  not  circinate  and 
usually  all  bearing  sporangiola.  About  a  half  dozen  species  are 
included  here,  of  which  the  best  known  is  Th.  elegans  Link. 

Subgenus  Chaetostylum  (van  Tieghem  &  le  Monnier)  Schroter. 
syn.  Bulbothamnidium  Klein  (1870:  557). 
Lateral  branches  of  the  sporangiophore  verticillately  branched, 
the  central  axis  of  each  successive  division  swollen  at  the  point 
of  origin  of  the  whorl  of  branches,  and  prolonged  beyond  them 
into  a  sterile  spine.  Two  or  three  species  are  placed  here, 
including  Th.  fresenii  (van  Tiegh.  &  le  Monn.)  Schroter,  the 
type  of  this  group.     (See  Sumstine,  1910:  143). 

Subgenus  Helicostylum  (Corda)  Schroter. 

Lateral  branches  of  the  sporangiophore  monopodially  or 
cymosely  branched,  the  ultimate  branches  circinate;  in  some  cases 
the  central  axis  terminating  in  a  spine  as  in  the  preceding  sub- 
genus. The  species  Th.  amoenum  (Preuss)  Schroter  [Ilelicosty- 
lum elegans  Corda]  and  about  a  half  dozen  other  species  fall  here. 


MU  COR  ALES  257 

In  recognizing  the  above  subgenera  the  treatment  of  Schroter 
(1893:  127)  is  followed.  The  groups  were  originally  described 
as  separate  genera,  and  are  given  generic  rank  by  Fischer  (1892: 
246).  They  are  clearly  very  closely  related,  and  intermediate 
species  and  intergrading  conditions  occur  (Brefeld  1881:  58; 
Bainier  1906 :  210).  For  descriptions  of  American  species  consult 
Sumstine  (1910),  Pound  (1894),  and  Povah  (1915).  The  striking 
beauty  of  the  sporangiophore  in  the  genus  renders  it  a  favorable 
subject  for  class  use. 

The  genus  Actinomncor  Schostak.  (1898:  155),  placed  by 
Lendner  near  Thamnidium,  is  known  only  from  the  original 
description.     It  is  here  regarded  as  a  doubtful  form. 

Chaetocladiaceae 

Sporangia  and  sporangiola  lacking,  replaced  by  unicellular 
conidia,  which  cover  sub-terminal  enlargements  of  branches  of 
the  conidiophore;  zygospore  not  enclosed  in  a  hyphal  envelope. 

A  single  genus.  1.  Chaetocladium  (Fig.  91). 

1.  Chaetocladium  Fresenius  (1863:  97). 

Mycelium  parasitic  on  other  members  of  the  Mucorales,  wide- 
spreading,  profusely  branched;  point  of  attachment  to  host  hypha 
marked  by  a  dense  cluster  of  peculiar  vesicular  outgrowths 
(Burgeff,  1920) ;  fertile  hyphae  repeatedly  branched;  the  branches 
tapering  to  long,  sterile,  sharp-pointed  tips,  many  of  which  are 
provided  with  small  subterminal  swellings  covered  with  sterig- 
mata  bearing  conidia;  conidia  globose,  unicellular;  zygospores 
globose,  formed  between  the  ends  of  the  copulating  gametangia 
as  in  Rhizopus. 

The  genus  contains  two  species,  C.  jonesii  (Berk.  &  Broome) 
Fresenius  (1863:  97)  [C.  fresenianum  Brefeld,  1881:  55]  based  on 
Botrytis  jonesii  Berk.  &  Broome  (1854:  462),  and  C.  hrefeldii 
van  Tieghem  &  le  Monnier  (1873:  342)  based  on  a  form  which 
Brefeld  (1872:  29)  had  discussed  under  the  name  C.  jonesii.  The 
two  species  are  very  similar,  the  conidia  of  the  first  being  spiny 
at  maturity  and  measuring  six  to  eight  microns  in  diameter, 
while  those  of  the  second  are  smooth  and  smaller  (two  to  four 
microns). 

The  conidia  of  Chaetocladium  are  frequently  termed  mono- 
sporous  sporangia  or  sporangiola.     This  terminology  is  based 


258 


THE  LOWER  FUNGI— PHYCOMYCETES 


on  the  work  of  van  Tieghem  and  le  Monnier  (1873:  pZ.  23,  jig.  63), 
who  figure  germination  stages  in  C.  jonesii.  They  show  the 
rupture  of  the  spiny  wall  (sporangia!  wall)  and  the  escape  of  a 
smooth-walled  spore.  Brefeld  (1881:  pi.  2,  fig.  1)  made  the 
same  observation.  Preceding  rupture  the  two  walls  are  in  close 
contact  and  indistinguishable.     The  homology  of  the  conidium 


Fig.  91. —  (a-c)  Chaetocladium  brefeldii  van  TicKhem  &  le  Monnier.  (d) 
Ch.  jonesii  Fresenius.  (a)  Portion  of  branching  thallus  showing  conidia,  sterile 
branchlets,  and  a  zygospore.  (6)  Germinating  conidium  producing  threads 
which  are  attacking  a  hypha  of  Mucor  sp.  (c)  A  cluster  of  short  branches 
surrounding  the  host  hypha  in  connection  with  haustorium  formation,  (d) 
Germinating  conidium.      (After  Brrfcld  1872,  1891.) 

of  this  genus  with  the  sporangium  of  other  members  of  the  order 
would  have  been  clear,  of  course,  even  in  the  absence  of  a 
visable  double-walled  condition. 


Choanephoraceae 

Sporangium  present  in  some  forms,  absent  in  others;  either 
sporangiola  or  conidia  present  in  all  cases,  and  covering  terminal 
capitate  enlargements  of  branches  of  the  sporangiophore  or 
conidiophore. 


MU  COR  ALES  259 

Key  to  Genera  of  Choanephoraceae 

I.  Sporangium  present,  accompanied  by  either  sporangiola  or  conidia. 

.1.    Sporangiola   present,    conidia   absent;  sporangiospores  longitud- 
inally striate. 

1.  Blakeslea,  p.  259 

B.  Sporangiola  absent;  conidia  present;  sporangiospores  not  striate; 
conidia  striate. 

2.  Choanephora,  p.  261 
II.  Sporangium  and  sporangiola  absent;  conidia  present  and  echinulate,  not 

striate 

3.  Cunninghamella,  p.  263 

1    Blakeslea  Thaxter  (1914:  353). 

Conidia  absent;  sporangia  of  two  types  (Fig.  92),  larger 
solitary  ones  possessing  a  columella,  and  smaller  ones  termed 
sporangiola  which  lack  a  columella  and  occur  in  considerable 
numbers  over  the  surface  of  large,  spherical  sporangioliferous 
heads;  the  two  types  showing,  however,  numerous  intergrad- 
ing  variations;  larger  sporangia  extremely  variable  in  size, 
sometimes  not  larger  than  the  sporangiola;  the  columella  often 
obsolete;  sporangioliferous  heads  sometimes  sohtary  at  the  ends 
of  erect  unbranched  sporangiophores,  but  usually  in  groups  of 
ten  or  more  and  terminating  branchlets  of  the  subdichotomously 
branched  end  of  the  sporangiophore;  sporangiolum  typically 
three-spored,  rarely  four-  or  six-spored,  attached  to  the  sporangio- 
liferous head  by  a  small  spherical  vesicle,  when  mature  falling 
away  carrying  the  vesicle  with  it;  spores  variable  in  size  but  in 
general  alike  in  all  types  of  sporangia,  longitudinally  striate, 
provided  at  each  end  with  a  cluster  of  delicate  radiating  append- 
ages like  those  of  the  sporangiospores  of  Choanephora;  chlamydo- 
spores  variable;  zygospores  where  known  formed  between  the 
tips  of  twining  branches. 

The  genus  contains  a  single  species,  B.  trispora  Thaxter,  first 
isolated  as  a  contamination  from  a  Botrytis  culture  which  in 
turn  had  been  obtained  from  flowers  of  cowpea.  It  seems  to 
occur  as  a  weak  parasite  on  various  plants  (Jochems,  1927).  It 
has  been  shown  by  Weber  and  Wolf  (1927)  to  be  heterothaUic. 
It  is  very  closely  related  to  Choanephora,  differing  chiefly  in  that 
the  conidia  of  that  genus  are  here  replaced  by  sporangiola.  The 
spores  combine  the  characters  of  the  sporangiospores  and  conidia 
of  Choanephora,  possessing  the  appendages  of  the  one  and  the 
striations  of  the  other.     Thaxter  (1914:  357)  in  a  very  interesting 


260 


THE  LOWER  FUNGI— PHYCOMYCETES 


discussion  homologized  the  conidia  of  Choanephora  with  the 
sporangiola  of  Blakeslea,  and  suggests  that  the  conidia  are  to 
be   regarded    as    monosporous    sporangiola.     Although    he    was 


Fig.  92. — Blakeslea  trispora  Thaxter.  (a)  Typical  many-spored  sporangium. 
(6,  c)  Selected  individuals  illustrating  the  transition  from  sporangium  to  spo- 
ra'ngiolum.  (d)  Typical  sporangiola  borne  over  globose  heads  at  the  apex  of  a 
fertile  hypha.  (e)  Group  of  such  globose  heads  denuded  of  sporangiola.  (/) 
One  head  with  five  sporangiola  attached,  {g)  A  single  sporangiospore.  (After 
Thaxter  1914.) 


unable  to  separate  mechanically  an  outer  thin  sporangial  wall 
from  the  conidia  of  C hoariephora  he  figures  somewhat  abnormal 
conidia  of  C.  cucurbitarum  in  which  its  existence  is  indicated.  In 
any  case  homology  of  conidia  and  sporangia  is  very  evident  in 
these  genera. 


MU  COR  ALES 


261 


2.  Choanephora  Currey  (1873:  578). 

syn.  Cunninghamia  Currey  (1873:  334). 
Both  sporangia  and  conidia  present  and  not  infrequently 
arising  from  the  same  myceHum;  sporangium  terminal  and 
usually  pendent  on  the  recurved  end  of  an  erect  unbranched 
sporangiophore,  provided  with  a  definite  columella  which  tends 
to  be  globose,  and  usually  containing  a  large  number  of  spores, 
though  diminutive  few-spored  sporangia  sometimes  occur; 
sporangiospores    usually    ovoid    to    fusiform,    but    occasionally 


Fig.    93." — Choanephora  cucurhitarum    (Berk.    &    Rav.)    Thaxter.      (a)    Young 
conidiophore  with  spherical  heads  on  which  conidia  are  just  beginning  to  form. 

(b)  Same  at  later  stage ;  the  heads  covered  with  conidia  borne  on  short  sterigmata. 

(c)  Single  head  enlarged,  (d)  Single  "conidium,"  here  shown  to  be  in  fact  a 
mono-spored  sporangiolum.  (e)  Conidium  of  more  usual  aspect;  the  outer 
wall  not  evident.  (/)  Sporangium.  ((?)  Sporangiospores;  the  lower  atypical, 
(a-e,  after  Thaxter  1903,  1914;  (f-g)  after  Wolf  1917.) 

varying  to  inequilateral  or  triangular,  not  striate  like  the  conidia, 
provided  at  both  ends,  and  in  spores  of  odd  shape  sometimes  also 
at  the  side,  with  a  cluster  of  very  fine,  radiating  appendages  as 
in  the  related  genus  Blakeslea;  conidiophore  an  erect  hypha 
terminated  in  a  capitate  vesicle  from  which  a  few  short  branches 
emerge;  these  branches,  usually  without  branching  again,  enlarg- 
ing at  their  tips  to  form  secondary  vesicles,  which  at  maturity 
are  covered  with  short  sterigmata  bearing  conidia;  the  conidio- 
phore rarely  unbranched  and  bearing  the  conidia  on  the  primary 
enlargement  somewhat  as  in  the  genus  Rhopalomyces  (Thaxter 
1891:  pi.  3);  conidia  resembling  the  sporangiospores  in  shape 
but  non-ciliate,  longitudinally  striate,  and  provided  at  the  base 


262  THE  LOWER  FUNGI— PHYCOMYCETES 

with  a  short  hyahne  appendage  (Thaxter,  1914:  ^gr.  18h);  inter- 
calary chlamydospores  with  more  or  less  thickened  walls  borne 
on  the  mycehum;  zygospores  observed  in  various  described 
species  (Fig.  93). 

The  genus  Choanephora  is  of  unusual  interest,  since  in  it 
sporangia  and  conidia  occur  together.  It  is  most  closely  related 
to  the  genus  Blakeslea  in  which  the  conidia  are  replaced  by 
sporangiola.  An  interesting  undescribed  species  is  mentioned 
by  Thaxter  (1914:  358),  which  grew  in  culture  over  a  period  of 
years  without  producing  conidia,  though  sporangia  bearing  the 
typical  ciliated  spores  of  this  group  were  always  present.  The 
following  species  have  been  described: 

C.  infundihuUJera  (Currcy)  Sacc.  {Syll  Fung.,  9:  339,  1891). 
syn.  Cunninghamia  infundibulifera  Currey  (1873:  334). 
Choanephora  cunning hamiana  Currey  (1873:  578). 
First  reported  from  material  collected  in  India  by  Cunningham  on  faded 
flowers  of  Hibiscus;  also  collected  by  Thaxter  (1914:  360)  from  flowers  of 
the  same  host  in  the  West  Indies  and  South  America.     The  secondary 
heads  of  the  conidiophores  are  persistent,  and  become  cupulate  after  the 
conidia  have  fallen. 

C.  simsoni  Cunningham  (1895:  169). 

Collected  in  India  on  Ipomoea  and  Zinnia. 
C.  cucurbitarimi  (Berk.  &  Rav.)  Thaxter  (1903:  102). 

syn.  Rhopalomyces  cucurbitarum  Berk.  &  Rav.  {Grevillea,  3:  11,  1875); 
see  Thaxter  (1891:  20). 

C.  americana  Moller  (1901:  18). 
Reported  on  fading  flowers  of  Hibiscus,  Cucumis,  Gossypium,  Capsicum 
etc.  (Dastur,  1920;  Wolf,  1917;  Moller,  1901;  Thaxter,  1903;  1914). 
It  is  parasitic  on  summer  squash  (Wolf,  1917).  An  undescribed  species 
closely  related  to  C.  cucurbitarum,  but  differing  in  possessing  smooth  conidia 
of  a  lighter  color,  was  collected  on  flowers  of  Cucurbitaceae  in  South  America 
by  Thaxter  (1914:  361). 

C.  persicaria  Eddy  (1925:  207). 

A  species,  closely  related  to  the  preceding,  and  found  recently  causing  a  rot 
of  peaches. 

C.  conjuncta  Couch  (1925). 
A  dioecious  species. 

Saito  and  Naganishi  described  in  1915  under  the  name,  Cun- 
ninghamella  mandshurica,  a  species  whose  affinities  seem  to  be 
quite  as  much  with  Choanephora  as  with  Cunninghamella.  Only 
conidia  are  known,  and  these  are  longitudinally  striate  and 
identical  in  aspect  with  those  of  Choanephora.  The  conidiophore 
is  of  a  somewhat  intermediate  type  of  branching,  there  being  no 


MUCORALES 


263 


appreciable  enlargement  of  the  primary  stalk  at  the  point  of 
origin  of  the  conidia-bearing  branches. 

Gandrup  (1923)  mentions  a  new  species,  Choanephora  dichot- 
oma,  but  does  not  describe  it. 

3.  Cunninghamella  Matruchot   (Saccardo  Syll.  Fung.,   6:  508, 

1905;  nom.  nud.  Ann.  Mycol.,  1:  46,  1903). 

syn.  Adinocephalum  Saito  (Bot.  Mag.  Tokyo,  19:  1,  1904). 
Sporangia  never  observed  in  the  genus,  though  perhaps 
occasionally  developed  under  special  conditions  of  environment 
(Thaxter,  1914:  358);  asexual  reproduction,  as  far  as  known, 
taking  place  exclusively  by  means  of  conidia  (Fig.  94);  conidio- 
phores  arising  from  the  vegetative  hyphae,  erect,  more  or  less 
branched,  sometimes  septate;  each 
branch  terminated  in  a  capitate 
vesicle  covered  with  sterigmata  bear- 
ing small,  spiny,  unicellular,  globose 
to  oval  or  pyriform,  deciduous  con- 
idia; the  type  of  branching  differing 
in  the  various  species;  in  C.  elegans 
a  main  stalk  bearing  a  subterminal 
whorl  of  branches  each  of  which  is 
apically  swollen;  in  C.  echimdata  the 
branching  cymose  to  indefinite;  glo- 
bose chlamydospores  intercalary  in 
the  mycelium;  the  known  species 
heterothallic ;  gametangia  approxi- 
mately equal;  zygospore  rough  but 
not  appendaged. 

The  type  species  of  the  genus  was 
originally  described  by  Thaxter  (1891 : 
17)  as  Oedocephalum  echinulatuni. 
Its  inclusion  in  this  hyphomycetous 
genus  was  questioned  by  Matruchot 
(1903:46)  inasmuch  as  its  hyphae  are    conidiophore.    {After    Thaxter 

,  „  1891.) 

characteristically  coenocytic,   and  in 

an  interesting  experiment  he  demonstrated  that  it  will  serve 
as  a  host  for  the  species  of  Piptocephalis  which  parasitize 
Mucorales  exclusively.  He  established  the  genus  Cunning- 
hamella for  its  inclusion  and  renamed  the  species  C.  africana. 
Though  he  failed  to  give  a  generic  description,  this  was  later 


Fig.  9  4. — Cunninghamella 
echinulata  Thaxter.  Showing 
echinulate  conidia  covering 
capitate    terminations    of    the 


264  THE  LOWER  FUNGI— FHYCOMYCETES 

provided  by  Saccardo  (Syll.  Fung.,  6:  508,  1905)  and  attributed 
to  him.  Blakeslee  (1905:  161)  further  justified  the  inckision 
of  the  species  in  the  Mucorales  by  discovering  its  zygospores. 
Thaxter  (1903:  98)  pointed  out  that  the  species  should  bear  the 
name  C.  echinulata  Thaxter.  The  following  additional  species 
have  been  described. 

C.  elegans  Lcndner  [Bid.  flerbier  Boissier  (2  ser.),  5:  250,  1907;  also 
Mucorinees  de  la  Suisse  p.  159,  1908].  The  genus  Actinocephalum  Saito, 
cited  above  as  a  synonym  of  C unninghamella,  was  based  on  a  single  species, 
A.  japonic mti,  which  is  clearly  very  close  to  C.  elegans. 

C.  bertholletiae  Stadel  (1911). 

C.  hlakesleeana  Lendner  (1928). 

C.   mandshurica  Saito  &  Naganishi.     Discussed  above  under  Choanephora. 

C.  albida  (Sacc.)  Matruchot  (1903:  56).  This  species,  based  on  Oedo- 
cephalum  alhiduvi  Sacc.  (Michelia,  2  :  288,  and  Fungi  Italici,  fig.  805),  and  the 
following  based  on  Gonatobolrys  microspora  Rivolta  were  tentatively  incor- 
porated in  Cumdnghamella  by  Matruchot  but  were  not  recognized  by 
Saccardo.     They  may  be  listed  as  doubtful. 

C.  microspora  (Rivolta)  Matruchot  (1903:  56). 

Another  species  is  mentioned  but  not  named  by  Blakeslee, 
Cartledge,  and  Welch  (1921). 

For  a  discussion  of  zygospore  formation  in  the  genus  consult 
their  paper  and  that  of  Burger  (1919). 

The  genera  Sigmoideotmjces  Thaxter  (1891:  22)  and  Thatnno- 
cephalis  Blakeslee  (1905:  165),  known  only  in  their  conidial 
stages,  may  be  listed  as  doubtful  members  of  the  order,  but  in 
the  absence  of  zygospores  cannot  be  certainly  included.  If 
incorporated  they  would  fall  somewhere  in  the  general  vicinity 
of  C unninghamella. 

Mortierellaceae 

Multispored  sporangium  present  in  some  forms,  lacking  in 
others,  when  present  lacking  a  columella;  sporangiola  and  conidia 
formed  in  some  genera,  when  present  isolated,  not  covering  an 
enlargement  on  the  sporangiophore  or  conidiophore;  zygospore 
where  known  enveloped  in  a  thick  layer  of  interwoven  hyphae. 

Key  to  Genera  of  Mortierellaceae 

I.  Sporangium  present,  sometimes  accompaiiitHl  by  conidia. 

A.  Sporangiophore    :irising    directly     from     the    ordinary    mycelial 
liyphae. 

1.   Sporangiophore  erect,  usually  tapering  to  a  delicate,  hair-like 
tip  lieneath  the  sporangium,  more  or  less  swollen  toward 


I 


MUCORALES  265 

the  hasp;  conidia  unicellular,  slohose,  orhinulato,  bonio 
apically  on  simple  or  ))ranchcd  conidiophores;  zygospore 
enveloped  at  maturity  in  a  thick  layer  of  closely  woven 
hyphae. 

1.  Mortierella,  p.  265 

2.  Sporangiophore  procumbent,  of  uniform  diameter  through- 
out, sympodially  branched. 

2.  Herpocladium,  p.  268 

B.  Sporangiophores  arising  from  a  liighly  specialized,  stout,  creeping 
fertile  hypha,  and  successively  produced  as  buds  behind  its 
advancing  tip. 

3.  Dissophora,  p.  268 

II.  Sporangium  absent,  replaced  by  mono-  or  bispored  sporangiola  which 
are  borne  terminally  and  sometimes  also  laterally  on  short  branches 
which  radiate  from  fertile  intercalary  segments  of  the  mycelium. 

4.  Haplosporangium,  p.  268 

1.  Mortierella  Coemans  (1863:  536). 

Mycelium  procumbent,  within  the  upper  layer  of  the  medium 
or  forming  a  tightly  appressed  weft  over  its  surface,  not  typically 
aerial ;  sporangiophores  erect,  simple,  or  variously  and  character- 
istically branched,  usually  tapering  to  a  delicate  hair-like  tip 
just  below  the  sporangium,  and  more  or  less  swollen  or  ventricose 
downwards;  sporangia  globose,  lacking  a  columella,  provided  with 
a  delicate  wall  which  disappears  soon  after  reaching  maturity, 
leaving  only  a  remnant  at  the  pointed  apex  of  the  sporangiophore ; 
conidia  (by  several  writers  here  termed  stylospores)  unicellular, 
globose,  echinulate,  occurring  at  the  tips  of  simple  or  branched 
aerial  conidiophores  in  various  species,  and  recalling  the  mono- 
spored  sporangia  of  Haplosporangium  decipiens;  zygospores 
enveloped  at  maturity  in  a  thick  layer  of  closely  woven  hyphae, 
which  arise  immediately  below  the  gametangia  and  tend  to 
obscure  the  conjugation  process  (Fig.  95). 

The  species  of  the  genus,  about  thirty  in  number,  are  for  the 
most  part  saprophytes  on  dung,  humus,  fruit  bodies  of  higher 
fungi,  etc.  A  few  are  facultative  parasites.  They  are  known 
chiefly  from  Europe,  the  genus  having  received  little  attention 
in  America  (Kauffman,  1920).  The  best  taxonomic  treatment 
of  the  group  is  that  of  Dauphin  (1908). 

Thaxter  (1922:  291)  has  brought  together  under  the  pro- 
visional name  Endogoneae  several  as  yet  imperfectly  understood 
genera  which  show  in  certain  respects  indication  of  relationship 
with  Mortierella.  The  genera  included  are  Endogone  Link, 
{Glomm     Tulasne),     Sphaerocreas     Sacc.    &     Ellis,     Sclerocytis 


266 


THE  LOWER  FVNGI—PHYCOMYCETES 


Berk.  &  Br.  (Xenomyces  Cesati,  Ackermannia  Pat.),  and  Glaz- 
iella  Berk.  {Endogonella  v.  Hohnel.)  The  genus  Endogone  (see 
Bucholtz,  1912:  147)  is  the  largest  and  most  interesting  member 
of  the  group  (Fig.  96).  In  certain  of  its  species  thick- walled 
zygospores  arc  produced  in  compact  groups,  the  whole  mass 
usually  being  enclosed  in  a  hyphal  envelope.  A  definite  fruit 
body  thus  results  which  recalls  on  the  one  hand  the  zygosporic 


Fig.  95.- — (a)  Morticrella  candelabrum  v.  Tiegham  &  le  Monnier,  showing 
branching  sporangiophore.  (b)  M.  fusispora  v.  Tieghem.  "Stylospore"  (coni- 
dium).  (c-e)  M.  nigreacens  v.  Tieghem,  showing  successive  stages  in  zygospore 
formation.      {After  v.  Tieghem  and  le  Monnier  1873,  1876.) 

envelope  of  Mortierella  and  on  the  other  the  more  definite  fruit 
body  of  the  Ascomycetes.  In  other  species  of  the  genus  the 
interior  of  the  fruit  body  is  filled  with  azygospores  (chlamydo- 
spores),  and  in  still  others  with  sporangia.  In  one  known  species 
zygospores  and  chlamydospores  occur  together,  but  neither  of 
these  spore  forms  has  been  found  in  any  of  the  sporangia-pro- 
ducing species.  The  sporangia  resemble  those  of  Mortierella. 
The  zygospore  is  formed  in  a  bud  put  out  by  the  fusion  cell  which 
results  from  the  copulation  of  the  gametangia,  and  appears  to 
surmount     them.     Thus,     though     resembling     Mortierella    in 


MU  COR  ALES 


267 


possessing  an  envelope,  it  shows  an  essential  relationship  with 
species  of  the  Piptocephalaceae.  The  zygospores  and  chlamydo- 
spores  have  never  been  seen  to  germinate,  but  sporangial  ger- 
mination has  been  observed  (Walker,  1923:  245).  The  genus  has 
been  considerably  misunderstood,  the  term  ascus  having  been 
apphed  to  the  sporangium  as  well  as  to  the  zygospore  and 
chlamydospore  by  various  authors.  Atkinson  (1918:  1)  regarded 
the  genus  as  constituting  an  interesting  type  between  the  Zygo- 
mycetes and  the  Protoascomycetes,  and  states  that  it  affords 


Fig.  96. — Endoyone  upp.  (a)  Zygospore;  its  origin  from  gametangia,  and 
enveloping  hyphae  of  sporocarp  (fruit  body)  shown,  (b-f)  Stages  in  zygospore 
formation,  (g)  Portion  of  sporocarp  in  section  showing  peridium  and  spores, 
some  of  the  latter  immature.      {After  Thaxter  1922.) 


strong  evidence  of  the  Phycomycete  ancestry  of  the  Ascomycetes. 
The  genera  Sphaerocreas,  Sclerocystis,  and  Glaziella,  known  only 
in  the  chlamydospore  condition,  resemble  the  chlamydospore- 
producing  species  of  Endogone  sufficiently  to  indicate  a  relation- 
ship between  the  various  genera.  They  differ  chiefly  in  minor 
structural  features  of  the  fruit  body.  Whether  these  four 
genera  should  be  regarded  as  constituting  a  separate  family 
of  the  Mucorales  related  to  and  somewhat  higher  than  the 
Mortierellaceae  is  perhaps  open  to  question,  but  in  the  present 
state  of  knowledge  it  seems  very  likely  that  the  group  should 
be  incorporated  in  the  Mucorales. 


268  THE  LOWER  FUNGI— PHYCOMYCETES 

2.  Herpocladium  Schroter  (1886:  213). 

syn.  Ilerpodadiella  Schroter  (1893:  130). 

Mycelial  characters  unknown;  sporangiophore  of  equal  diam- 
eter throughout,  sympodially  branched,  winding  about  over  the 
substratum  for  a  considerable  distance,  not  erect;  sporangia 
terminating  the  branches,  globose,  lacking  a  columella  and  with 
a  transitory  wall  as  in  Mortierella;  zygospores  unknown. 

A  doubtful  monotypic  genus  based  on  a  little  known  species, 
//.  circinans  Schroter.  This  genus  and  Mortierella  compose  the 
family  Mortierellaceae  of  Schroter.  They  are  similar  in  spo- 
rangial  characters  but  seem  to  have  little  else  in  common  and 
may  prove  on  further  study  to  be  unrelated. 

The  name  Herpocladium  was  changed  by  Schroter  to  Ilerpo- 
dadiella, on  account  of  the  existence  elsewhere  of  a  subgenus 
bearing  the  former  name. 

3.  Dissophora  Thaxter  (1914:  361). 

A  monotypic  genus,  based  on  D.  decumbens  Thaxter  (Fig.  97) ; 
sporangia  and  sporangiophores  as  in  Mortierella;  fertile  hypha 
unlike  those  of  other  genera  of  the  order,  at  first  erect,  then  falling 
over  and  creeping  over  the  substratum,  stout;  abruptly  differ- 
entiated from  the  slender  vegetative  hyphae,  producing  spo- 
rangiophores which  arise  as  buds  successively  produced  behind 
its  advancing  tip;  fertile  hyphae  and  sporangiophores  septate; 
zygospores  unknown. 

4.  Haplosporangium  Thaxter  (1914:  362). 

Resembling  Dissophora  in  the  possession  of  highly  specialized 
structures  from  which  the  sporangiophores  arise,  but  the.se  struc- 
tures consisting  of  prostrate,  intercalary,  septate  segments  of 
the  mycehum;  sporangiophores  borne  without  regularity  on  all 
sides  of  the  fertile  segment  and  radiating  from  it,  short,  stout, 
tapering  to  hair-like  tips  bearing  the  sporangiola,  sometimes 
branching  slightly  and  bearing  lateral  sporangiola  also;  spo- 
rangiola very  minute,  containing  only  one  or  two  spores;  columella 
lacking;  zygospores  unknown  (Fig.  98). 

In  general  aspect  the  fungi  included  here  resemble  certain 
Hyphomycetes  such  as  Hyalopus  or  Cephalosporium,  and  may  be 
easily  mistaken  for  them.  The  genus  includes  only  the  two 
species  on  which  it  was  erected.  In  one  of  these,  //.  hisporale 
Thaxter,  the  sporangiolum  usually  contains  two  spores,  though 


MUCORALES 


269 


sometimes  only  one.     In  the  second  species,  //.  decipiens  Thaxter, 
one-spored  sporangiola  only  have  been  observed.     In  the  latter 


Fig.  97.- — Dissophora  decumhens  Thaxter.  (a)  Terminal  portion  of  fertile 
hypha  showing  origin  of  sporangiophores  behind  the  elongating  apex.  (6) 
Portion  of  fertile  hypha  bearing  mature  sporangiophores.  (c)  Mature  sporan- 
gium.     {After  Thaxter  1914.) 


Fig.  98.- — (o,  b)  Haploaporanyium  decipiens  Thaxter,  showing  monosporic 
sporangiola.  (c-e)  H.  bisporale  Thaxter  with  bisporic  sporangiola.  {After 
Thaxter  1914.) 


case  the  wall  of  the  sporangiolum  is  roughened  while  that  of  the 
enclosed  spore  is  smooth. 


270  THE  LOWER  FUNGI— PHYCOMYCETES 

Thaxter  regards  the  genus  as  closely  related  to  Mortierella. 
Torrey  (1921)  regards  the  1-spored  sporangiola  of  Haplosporan- 
gium  as  equivalent  to  the  conidia  ("stylospores")  of  Mortierella. 
He  then  arranges  a  phylogenetic  line  in  which  H.  bisporale  ("with 
sporangiola  and  stylospores")  lies  between  H.  decipiens  ("with 
only  stylospores")  on  the  one  hand,  and  Mortierella  ("with  spo- 
rangia and  stylospores")  on  the  other. 

Piptocephalaceae 

Sporangium  narrowly  cylindrical  or  rod-like,  relatively  few- 
spored;  sporangiospores  standing  in  a  single  row,  at  maturity 
having  the  aspect  of  a  chain  of  conidia  due  to  the  dissolution  of 
the  sporangial  wall;  zygospore  usually  formed  in  a  bud  put  out 
by  the  fusion  cell  resulting  from  the  copulation  of  the  game- 
tangia,  not  enveloped  in  a  layer  of  hyphae. 

Key  to  Genera  of  Piptocephalaceae 

I.  Fertile  sporangiferous  hypha  branched. 

A.  Branching  dichotomous  or  pseudodichotomous  in  tj'pe. 

1.  Some  of  the  branches  prolonged  into  sterile  prongs;  sporan- 

giferous heads  not  deciduous. 

1.  Dispira,  p.  270 

2.  All  the  branches  terminating  in  sporangiferous  heads;  the 

latter  deciduous. 

2.  Piptocephalis,  p.  272 

B.  Branching  cymose  to  indefinite,  not  dichotomous,  sporangiferous 

heads  not  deciduous. 

3.  Syncephalastrum,  p.  273 
II.   Fertile  sporangiferous  hypha  not  branched  below  the  terminal  enlarge- 
ment; provided  with  spur-like  rhizoids  at  the  point  of  attachment 
with  the  substratum. 

4.  Syncephalis,  p.  273 

I.  Dispira  van  Tieghem  (1875:  160,^1^.  173-177). 

Mycelium  parasitic  on  other  Mucorales;  sporangiophores  erect, 
repeatedly  branched  in  a  dichotomous  or  pseudodichotomous 
fashion;  each  successive  branch  delimited  by  a  septum  at  its  base; 
some  of  the  terminal  branches  tapering  into  curved,  sterile, 
sharp-pointed  tips;  the  others  swollen  to  form  spherical  heads 
over  which  numerous  sterigmata  arise  bearing  cylindrical  spo- 
rangia; each  sterigma  consisting  of  a  single  cell  with  a  transverse 
median  constriction  or  of  two  superimposed  cells,  the  terminal 
one  of  which  buds  from  the  lower;  sporangium  containing  a 


MU  COR  ALES 


271 


single  row  of  spores  (six  in  D.  cornula  van  Tieg.,  two  in  D. 
americana  Thaxter)  which  at  maturity  have  the  aspect  of  a  chain 
of  conidia  ckie  to  the  dissolution  of  the  sporangial  wall; 
zygospores  formed  in  an  anomalous  manner  and  always  in  close 
connection  with  the  host  hypha;  at  maturity  partly  enclosed  by 
finger-like  processes  which  arise  from  one  of  the  gametangia 
(Fig.  99). 

The  points  of  dissimilarity  between  the  two  above  named 
species,  as  indicated  by  the  original  descriptions,  are  enumerated 
by  Thaxter   (1895:  513).     More  recently  Bainier   (1906:  213) 


Fig.  99. — Diapira  americana  Thaxter.  (a)  Sporangiophore  with  spherical 
sporangium-bearing  heads  and  sterile  sharp-pointed  tips,  {h)  Optical  section 
of  a  single  such  head  showing  the  peculiar  budding  sterigmata  terminated  by 
sporangia,  (c)  Sterigma  bearing  two  sporangia,  each  containing  two  spores. 
{d)  Sporangiophore  of  Mucor  attacked  by  hyphae  of  Dispira;  the  latter  septate 
near  host  hypha  to  form  pairs  of  gametangia.  (e)  Gametangia  and  zygospores 
in  various  stages  of  development.  (/)  Single  mature  zygospore  surrounded 
in  part  by  a  rosette  of  finger-like  processes  arising  from  one  of  the  gametangia. 
(After  Thaxter  1895.) 

has  redescribed  D.  cornuta  and  states  that  the  two  species  are 
identical.  A  third  species,  D.  circmata  Elliott  (1926)  has  been 
described  rather  inadequately  from  the  asexual  stage  only. 

The  sexual  process  as  described  by  Thaxter  for  D.  americana, 
may  be  briefly  reviewed.  From  the  slender  creeping  vegetative 
hyphae  of  the  parasite  short  lateral  branches  are  put  out  which 
come  in  contact  with  the  host  hypha  and  attach  themselves  to  it 
as  suckers.  Each  sucker  then  becomes  septate  into  two  cells 
which  then  function  as  gametangia  in  zygospore  formation.  The 
enveloping  finger-like  processes  always  arise  from  that  game- 
tangium  which  joins  the  host. 

Although  in  Dispira  the  chains  of  spores  developed  at  the 
tips  of  the  fertile  hyphae  have  not  been  demonstrated  clearly 


272  THE  LOWER  FUNGI— PHYCOMYCETES 

to  be  ondogenou.s  in  chanicter,  they  are  here  so  regarded  from 
analogy  with  those  of  the  other  genera  incorporated  in  the  family. 
Several  other  genera,  known  only  in  the  asexual  stage,  appar- 
ently belong  near  Dispira.  One  of  these,  Dimargaris  van 
Tieghem  (1875:  154,  figs.  165-172),  a  monotypic  genus  based  on 
D.  cristalligena,  possesses  fertile  hyphae  so  strikingly  similar  to 
those  of  Dispira  americana  that  discovery  of  intermediate  species 
would  necessitate  the  merging  of  the  two  genera.  The  other 
genera  are  Kickxella  Coemans  (1862:  155)  [Coemansiella 
Saccardo,  SyllogeFnngorum,  2:  815],  il/ar^ewseZ/a  Coemans  (1863: 
536),  Spinalis  Vuillemin  (1904  h:  26),  Saitomyces  Ricker  {Jour. 
Mycol.,  12:  61,  1906),  and  Coemansia  van  Tieghem  &  le  Monnier 
(1873:392). 

2.  Piptocephalis  de  Bary  (1866:  356). 

IVIycelium  parasitic  on  other  Mucorales,  running  over  the  host 
hyphae  and  attached  to  them  at  intervals  b}'  swollen  suckers 
from  which  delicate,  filamentous  haustoria  penetrate  the  host 
cell;  fertile  hyphae  erect,  cylindrical,  septate,  repeatedly  dichot- 
omously  branched;  ultimate  branches  terminally  more  or  less 
swollen  to  form  deciduous  capitate  enlargements  over  whose 
surface  sterigmata  project  bearing  cylindrical  rod-like  sporangia; 
sporangia  at  maturity  forming  simultaneously  a  single  row  of 
spores  which  appear,  after  the  dissolution  of  the  sporangial 
wall,  as  a  row  of  conidia;  in  one  species,  P.  monospora  Mangin 
(1899:  376),  the  sporangium  containing  only  a  single  spore,  in 
another,  P.  microcephala  van  Tieghem  (1875:  148),  only  two; 
zygospore  globose,  rough,  formed  by  the  enlargement  of  a  bud 
which  develops  from  the  point  of  union  of  two  clavate  game- 
tangia  which  come  in  contact  at  their  apices  after  the  fashion  of 
a  pair  of  tongs  (Fig.  100). 

About  a  dozen  species  have  been  described,  the  majority  by 
van  Tieghem  (1875:  137).  No  recent  monograph  of  the  genus 
has  appeared,  the  best  general  treatment  being  that  of  Fischer 
(1892:  287). 

An  unusual  interpretation  of  the  homologies  of  the  asexual 
stage  in  this  genus  and  the  others  of  the  family  is  given  by 
Gaumann  (1926:  103).  He  regards  the  capitate  enlargement  at 
the  apex  of  the  fertile  hypha  as  the  sporangium,  and  terms  the 
cylindrical  branches  in  which  the  spores  are  borne  extrasporangial 
partial  sporangia.     His  point  of  view  is  the  same  with  respect 


MU  COR  ALES 


273 


to  Blakeslea  which  he  regards  as  a  connecting  form  in  a  phylo- 
genetic  series  embracing  Choanephora  and  Cunninghamella  on 
the  one  hand  and  Piptocephalis,  Syncephalis,  and  Syncephalastrum 
on  the  other. 


Fig.  100.- — Piptocephalis  frcscniana  de  Bary  {a,  h)  Zygospore  formation. 
(c-/)  Steps  in  the  process  which  results  in  the  formation  of  chains  of  sporangio- 
spores.  ((?)  Mycelium  attached  to  host  hypha  and  sending  rhizoids  into  it. 
{After  Brefeld  1872.) 

3.  Syncephalastrum  Schroter  (1886:  217). 

Mycehum  wide-spreading,  abundantly  branched;  sporangio- 
phore  erect,  lacking  basal  rhizoids,  repeatedly  branched,  each 
branch  apically  dilated  to  form  a  globose  head  bearing  rod-shaped 
sporangia  on  sterigmata;  sporangiospores  formed  simultaneously 
and  assuming  the  aspect  of  chains  of  conidia  as  in  related  genera; 
zygospores  unknown  (Fig.  101). 

About  six  or  seven  species  are  known.  Although  the  members 
of  the  genus  are  typically  saprophytic,  a  species  has  been  recently 
described  by  Vuillemin  (1922:  986)  as  parasitic  on  Rhizopus. 

4.  Syncephalis  van  Tieghem  &  le  Monnier  (1873:  372). 
Mycelium    parasitic    on    other    Mucorales    or    saprophytic, 

attached  to  the  host  hypha  by  suckers  and  sending  in  deHcate 


274 


THE  LOWER  FUNGI— PHYCOMYCETES 


thread-like  haustoria  as  in  Piptocephalis;  fertile  hyphae  erect, 
straight  or  apically  uncinate,  provided  at  the  base  with  prom- 
inent rhizoids,  apically  dilated  to  form  a  clavate  to  globose 
enlargement,  which  in  some  species  bears  rod-like  sporangia 
directly  on  sterigmata,  but  in  other  forms  more  or  less  elongate 
branches  which  are  provided  at  the  tips  with  sterigmata  bearing 
the  sporangia;  number  of  spores  in  a  sporangium  more  or  less 


Fig.  101.- — (a-d)  Syncephalis  wynneae  Thaxter.  (e,  /)  Synccphalis  reflcxa 
V.  Tieghem.  (y,  h,  m,  n)  Syncephalastrum  racemosum  Cohn.  a.  Fertile  hypha 
with  spur-like  rhizoids  at  base  and  spores  still  in  situ  at  apex,  (h)  Spores  freed 
from  sporangia  adhering  in  a  viscous  spherical  mass,  (c)  Enlarged  apex  of 
fertile  hypha  from  which  radiate  branches  terminated  by  clusters  of  tubular 
sporangia,  (d)  One  such  sporangium  with  its  pair  of  spores  nearly  mature. 
(e,  /)  Sporangia  before  and  after  spore  formation,  (g)  Normal  sporangium 
containing  single  row  of  mature  spores,  (h)  Sporangium  containing  one  lateral 
spore,  (w)  Spores  escaping  through  base  of  a  detached  sporangium,  (n) 
Crushed  sporangium.     {After  Thaxter  1897.) 


definite  in  a  given  species,  in  some  species  only  two  or  three; 
spores  at  maturity  assuming  the  aspect  of  a  chain  of  conidia; 
under  moist  conditions  all  the  spores  on  a  head  held  together  as 
a  spherical  mass  in  a  droplet  of  water;  zygospores  formed  some- 
what as  in  Piptocephalis,  conjugating  branches  more  or  less  coiled 
about  each  other  (Fig.  101), 

The  genus  contains  about  twenty-five  species.  The  most 
extensive  taxonomic  treatments  are  those  of  van  Tieghem  (1875: 
114-137)  and  Fischer  (1892:  295).  An  interesting  discussion 
of  the  genus  is  given  by  Thaxter  (1897:  1). 


MUCORALES  275 


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CHAPTER  X 
ENTOMOPHTHORALES 

Mycelium  is  less  profusely  developed  in  this  order  than  in 
the  Mucorales,  and  is  more  characteristically  septate.  Though 
in  a  few  species  it  persists  to  maturity  as  a  filamentous  branching 
thallus,  there  is  the  tendency  in  the  majority  of  forms  for  the 
hyphae  to  be  limited  in  development  and  to  fall  apart  early  at 
the  septa  into  the  component  cells.  These  hyphal  segments 
are  then  termed  hyphal  bodies.  They  increase  in  number 
rapidly  by  fission  and  budding.  The  cells  of  the  thallus  are 
usually  plurinucleate,  but  in  the  genus  Bcusidiobolus  are  typically 
uninucleate. 

The  majority  of  species  are  parasitic  on  insects,  and  relatively 
few  of  these  have  ever  been  obtained  in  culture  on  artificial 
media.  Consequently,  obligate  parasitism  has  been  assumed 
to  be  predominant  in  the  group.  In  recent  years  some  degree 
of  success  has  attended  attempts  to  get  these  forms  in  culture, 
and  it  now  seems  probable  that  many  of  them  will  be  found  to 
develop  saprophytically  when  favorable  media  are  provided 
(Sawyer,  1929).  Although  the  group  is  chiefly  entomogenous 
a  few  species  are  parasitic  on  plants,  and  several  forms  are  true 
saprophytes  wholly  lacking  in  parasitic  tendencies. 

In  asexual  reproduction  conidia  are  abjointed  at  the  tips 
of  simple  or  indefinitely  branched  clavate  conidiophores,  and, 
except  in  Massospora,  are  forcibly  discharged,  the  phenomenon 
being  strikingly  similar  to  that  exhibited  in  Pilobolus  of  the 
preceding  order,  where  a  multispored  sporangium  is  shot  away. 
The  conidium  is  in  all  cases  unicellular,  and  is  assumed  to  be 
the  homologue  of  the  sporangium  present  in  preceding  groups. 
In  Basidiobolus,  in  the  case  of  one  of  the  two  species  comprising 
the  genus,  it  has  been  shown  recently  that  the  "conidium, "  after 
being  ejected,  functions  as  a  sporangium  by  the  production 
of  endogenous  spores.  In  all  other  cases,  as  far  as  known, 
the  conidium  germinates  by  a  tube,  which  grows  directly  into 
mycelium  or  cuts  off  a  secondary  conidium   which  is  in  turn 

281 


282  THE  LOWER  FUNGI— PIIYCOMYCETES 

discharged.  The  almost  total  suppression  of  sporangiospore 
formation,  coupled  with  the  presence  of  the  phenomenon  of 
discharge,  indicates  that  the  asexual  stage  in  this  order  has 
reached  a  higher  point  in  development  than  is  seen  elsewhere  in 
the  Phycomycetes.  The  conidiophore  arises  as  an  outgrowth 
from  a  cell  of  the  filamentous  mycelium  or  from  a  hyphal  body 
and,  except  in  Massospora,  pushes  through  the  host  tissue  or 
substratum  to  the  surface,  where  it  forms  its  conidia  in  the  air. 
The  conidiophores  stand  finally  in  tufts  or  in  a  definite  palisade 
layer  or  hymenium  which  may  cover  a  considerable  area.  In 
Massospora  the  conidia  reach  maturity  within  the  host  and  fall 
away  from  the  condiophores  instead  of  being  discharged. 

The  hyphal  bodies  sometimes  assume  thick  walls  and  function 
as  chlamydospores.  Definite  globose,  thick-walled  resting  spores 
(zygospores  or  azygospores)  are  formed  in  most  species.  Zygo- 
spores result  from  a  true  sexual  conjugation  of  a  pair  of  hyphal 
bodies  or  cells  of  the  filamentous  mycelium.  Azygospores  are 
formed  without  conjugation  from  one  such  cell.  These  resting 
spores  are  formed  either  within  one  of  the  fusing  cells  (Basidio- 
holus,  Conidioholus)  or  in  an  outgrowth  or  bud  from  one  of  the 
cells  or  from  the  canal  at  their  point  of  union  as  in  Piptocephalis  of 
the  preceding  order.  Little  is  known  concerning  germination  of 
the  resting  spore  in  the  group.  It  probably  puts  out  a  tube  which 
functions  as  a  conidiophore  or  grows  directly  into  mycelium. 

The  order  as  here  treated  consists  of  the  single  family  Ento- 
mophthoraceae,  including  five  genera.  The  genus  Basidioholus 
was  removed  from  this  family  by  Gaumann  (1926),  and  made 
the  basis  of  another  family  Basidiobolaceae.  Later  Gaumann 
and  Dodge  (1928)  incorporated  all  the  forms  in  the  single  family 
Entomophthoraceae  but  recognized  two  subfamilies,  Basidio- 
boleae  and  Entomophthoreae.  Lakon  (1926)  emphasizes  the 
desirability  of  retaining  Basidioholus  in  the  family  on  account 
of  intergrading  characters  in  various  forms.  The  writer  feels 
that  little  if  anything  is  to  be  gained  by  splitting  the  group. 

No  general  monograph  of  the  species  of  the  world  has  yet 
been  prepared.  The  paper  on  American  forms  by  Thaxter  (1888) 
is  the  most  extensive  discussion  of  the  group,  and  is  excellently 
illustrated. 

The  most  widely  distributed  and  generally  known  species  of 
the  order  is  Empusa  muscae,  parasitic  in  the  house  fly.  In  late 
summer  and  autumn  flies  attacked  by  this  fungus  may  be  seen, 


ENTOMOPHTHORALES  283 

held  fast  to  window  panes  by  the  rhizoids  of  the  parasite,  and 
are  easily  identified  by  the  whitish  halo  of  eonidia  which  lie  on 
the  glass  surrounding  them. 

Key  to  Genera  of  Entomophthoraceae 

I.   Mycelium  not  entomogenous  (i.e.,  not  living  in  insects). 

A.  Mycelium  profusely  developed,  not  intracellular. 

1.  The   asexual   reproductive   cell   finally   forming   endogenous 

spores,  hence  termed  a  sporangium;  apical  portion  of 
sporangiophore  immediately  below  the  sporangium  dif- 
ferentiated as  a  peculiar  conical  "basidium,"  which  is 
shot  away  with  the  sporangium;  saprophytes. 

1.  Basidiobolus,  p.  283 

2.  The  asexual  reproductive  cell  functioning  as  a  conidium;  a 

specialized  "basidium"  absent;  conidium  freed  from  the 
conidiophore  completely  as  in  Etnpusa;  parasites  or 
saprophytes. 

2.  Conidiobolus,  p.  286 

B.  Mycelium  only  slightly  developed,  intracellular,  parasitic  in  fern 

prothallia. 

3.  Completoria,  p.  288 
II.  Mycelium  entomogenous. 

A.  Conidia  borne  within  the  body  of  the  host,  and  freed  bj^  its  dis- 

integration, not  shot  away,  verrucose. 

4.  Massospora,  p.  289 

B.  Conidia  borne  on  the  surface  of  the  host,  smooth-walled,  discharged 

forcibly  from  the  conidiophore. 

5.  Empusa,  p.  292 

1.  Basidiobolus  Eidam  (1886:  194). 

As  founded  by  Eidam  the  genus  Basidiobolus  embraced  two 
species,  B.  ranarum  Eidam  and  B.  lacertae  Eidam,  the  first 
saprophytic  in  nature  on  the  excrement  of  frogs,  the  second  on 
that  of  lizards.  Later  another  species,  B.  myxophilus  R.  E.  Fries 
(1899),  was  isolated  from  fallen  pine  needles,  where  it  was  found 
associated  with  a  slimy  bacterial  exudation.  An  extensive 
discussion  of  the  morphology  and  taxonomy  of  the  genus  was 
given  by  Eidam,  and  soon  afterward  Thaxter  (1888)  published 
notes  on  American  material  of  B.  ranarum.  More  recent  studies 
(e.g.,  Levisohn,  1927)  indicate  that  the  two  species  of  Eidam  are 
identical.  If  this  point  of  view  is  accepted  the  organism  should 
bear  the  name  B.  ranarum.  The  species  has  been  studied 
cytologically  by  Eidam,  Fairchild  (1897),  Woycicki  (1904;  1927), 
OHve  (1907),  and  Levisohn.     In  it,  zygospore  formation  is  of  an 


284 


THE  LOWER  FUNGI— PHYCOMYCETES 


unusual  type,  and  interesting  in  connection  with  any  consider- 
ation of  the  phylogeny  of  the  order.  In  a  sense  the  genus  may 
be  said  to  be  intermediate  in  type  between  the  Oomycetes  and 
Zygomycetes. 


Fi<;.  102. — Bayidioholus  ranarum  Eidam.  (a)  Formation  of  beaks,  (h) 
Nuclei  in  beaks,  (c)  Beaks  septate.,  (d,  e)  Nuclear  division  in  beaks.  (/) 
Zygospores,      (j/,  h)  Conidial  formation,     {a-e,  after  Eidam  1880';  f,  h,  after  Thaxtcr 

1888.) 


In  B.  ranarum  (Fig.  102)  the  myceHum  develops  profusely  on 
the  excrement,  and  consists  of  branching  threads  which  in  nature 
retain  their  hyphal  form.  They  are  composed  normally  of  uninu- 
cleate cells,  though  in  age  or  under  conditions  of  unsatisfactory 
nutrition  they  may  become  multinucleate.  The  fungus  grows 
well  in  culture  on  various  artificial  media,  but  in  culture  may 


ENTOMOPHTHORALES  285 

break  up  into  oidia,  which  are  regarded  as  comparable  to  the 
hyphal  bodies  commonly  developed  elsewhere  in  the  family. 

In  asexual  reproduction,  slender  erect  sporangiophores  are 
raised  above  the  substratum,  each  becoming  apically  inflated  to 
form  a  clavate  termination  recalling  the  subsporangial  vesicle 
of  Piloholus.  From  this  a  terminal  bud  is  put  out  which  enlarges 
into  a  pyriform  sporangium  ("conidium").  The  sporangium 
is  uninucleate,  and  finally  is  discharged  with  violence  from 
the  sporangiophore.  Preceding  discharge  a  portion  of  the  tip 
of  the  subsporangial  vesicle  is  differentiated  by  contraction  and 
the  assumption  of  a  thicker  wall  to  form  a  conical  structure, 
termed  the  "basidium,"  immediately  beneath  the  sporangium. 
This  "basidium"  is  carried  away  with  the  sporangium  when  dis- 
charge occurs,  rupture  of  the  apex  of  the  subsporangial  vesicle 
being  transverse.  Later  the  two  fall  apart.  At  the  time  of 
discharge  sporangiospores  have  not  yet  been  formed. 

Until  very  recently  the  phase  of  the  life  cycle  of  B.  ranarum 
which  precedes  the  appearance  of  the  mycelium  in  the  excrement 
was  wholly  unknown.  In  an  able  investigation  Levisohn  (1927) 
has  now  shown  that  the  sporangia,  after  being  shot  away  from 
the  sporangiophore,  are  eaten  by  beetles,  and  that  these  in  turn 
are  devoured  by  frogs.  In  the  alimentary  tract  of  the  frog  the 
sporangium  undergoes  further  development.  Its  nucleus  divides 
several  times,  and  thin-walled  non-motile  sporangiospores  are 
cut  out.  The  number  is  often  eight.  These  spores  escape 
by  the  disintegration  of  the  sporangial  wall,  and  lie  free  for 
a  time  in  the  body  of  the  frog,  multiplying  there  by  fission.  Only 
after  reaching  the  outer  air  are  they  capable  of  germination  to 
form  mycelium.  In  culture  under  optimum  conditions  the 
sporangium  germinates  by  forming  endogenous  spores,  but  more 
commonly  it  functions  as  a  conidium  and  sends  out  germ  tubes 
directly. 

In  age,  the  mycelium  forms  zygospores.  Conjugation  takes 
place  between  adjacent  cells  of  the  same  hypha.  Since  the  cells 
are  uninucleate  it  is  not  unlikely  that  their  nuclei  are  sisters. 
This  close  relationship  may  explain  the  rather  peculiar  and 
apparently  unnecessary  phenomenon  which  follows.  At  the 
point  where  the  zygospore  is  to  be  formed  a  beak-like  protrusion 
is  pushed  out  on  each  side  of  a  transverse  septum.  These  beaks 
grow  in  lateral  contact  until  a  considerable  length  is  attained. 
In  each  case  the  nucleus  of  the  parent  cell  migrates  out  into 


286  THE  LOWER  FUNGI— PHYCOMYCETES 

the  beak  and  divides  there  by  mitosis.  One  of  the  daughter 
nuclei  in  each  beak  then  passes  back  into  the  parent  cell,  the 
beaks  are  cut  off  by  septa,  and  the  nuclei  remaining  in  the  beaks 
disintegrate.  One  of  the  parent  cells  then  enlarges  until  it 
becomes  many  times  the  size  of  the  other,  and  the  septum 
between  the  cells  in  part  disappears  leaving  a  large  pore.  The 
nucleus  of  the  smaller  cell  accompanied  by  the  cytoplasm  passes 
through  the  pore,  and  in  the  larger  cell  the  two  nuclei  soon  lie 
together  and  seem  about  to  fuse.  In  some  cases  they  may  do 
so,  but  in  others  they  seem  to  undergo  a  final  division,  after 
which  one  daughter  nucleus  in  each  case  disintegrates  and  the 
remaining  pair  fuse.  The  combined  cytoplasm  of  the  two  cells 
finally  contracts  about  the  fusion  nucleus,  forming  a  resting 
spore  which  at  maturity  is  thick-walled  and  lies  free  in  the 
larger  cell.  In  several  respects  this  process  of  sexual  spore 
formation  recalls  that  of  the  Oomycetes,  and  the  spore  might 
easily  be  regarded  as  an  oospore.  However,  it  is  termed  a 
zygospore  in  all  the  literature,  and  the  characters  of  the  asexual 
stage  indicate  clearly  that  the  fungus  belongs  to  the  Zygomycetes. 

The  life  history  of  the  other  species,  B.  myxophilus  is  very 
imperfectly  known. 

The  genus  Ichthyophones  Plehn  and  Mulsow  containing  several 
species  isolated  from  the  intestinal  tract  and  excrement  of  fish 
is  very  closely  related  to  Basidiobolus,  if  not  in  fact  actually 
identical  with  it.  This  is  strongly  indicated  by  figures  published 
recently  by  Leger  (1927)  for  /.  intestinalis  Leger  &  Hesse. 
The  presence  of  globose  uninucleate  cells  in  the  alimentary 
canal  of  the  fish  affords  a  point  of  striking  similarity  between 
the  two  genera,  and  may  indicate  a  comparable  life  cycle. 
2.  Conidiobolus  Brefeld  (1884:  37;  also  see  Schroter  1889:  224). 

In  this  genus  the  mycelium  when  young  is  profusely  devel- 
oped, consisting  of  richly  branching,  many-septate  threads. 
Later  irregularly  swollen  or  lobulated  portions  are  put  out, 
and  these,  shortly  before  conidiophore  formation,  break  apart 
at  the  septa  to  form  irregular  hyphal  bodies.  The  conidiophores 
are  unbranched.  They  arise  from  the  hyphal  bodies,  and  cut 
off  apically  large  solitary  conidia  which  are  discharged  violently 
as  in  Empusa. 

The  genus  was  founded  by  Brefeld  on  C.  utriculosus  Brefeld 
and  a  smaller-spored  form,  C.  minor  Brefeld,  both  occurring  on 
the  fruit  body  of  Auriadaria  as  parasites  or  facultative  sapro- 


EX  TO  MOP  11 THOKA  LES 


287 


phytes.  Another  species  studied  in  recent  years  in  America  by 
Gilbert  (1919:  263)  and  Martin  (1925  6:  311),  and  described  by 
the  latter  writer  as  C.  villosus  INIartin,  was  isolated  from  fern 
prothallia  and  from  rotting  wood  bearing  a  species  of  Hypochnus. 
It  grows  readily  on  artificial  media. 

Sexual  spores  are  known  only  in  C.  utriculosus.     Here  a  pair 
of  projections  arising  from  two  hyphal  bodies  enlarge  terminally. 


Fig.    103. — Conidioholus    villosus    Martin,      (a-rf)    Stages    in    germination  of 

conidium    and    formation    of    secondary    conidium.      (e,   /)    Transformation  of 

conidium  into   an   appendaged   resting  spore,      {g)    Resting  spore   shrunken  to 
oval  form,  {h)  Germination  of  resting  spore.      {After  Martin  1925.) 


These  apical  swellings,  which  are  very  unequal  in  size,  come  in 
contact  and  conjugate,  the  intervening  walls  being  broken  down. 
The  contents  of  the  two  cells  merge,  and  a  large,  thick-walled 
spore  is  formed  in  one  of  the  cells.  Brefeld  regarded  the  process 
as  distinctly  oomycetous  in  nature,  but  Thaxter  feels  that  the 
spore  is  clearly  a  zygospore.  In  C.  villosus  (Fig.  103)  the  direct 
transformation  of  mature  conidia  into  characteristically  append- 
aged resting  spores  is  described  by  Martin. 


288  THE  LOWER  FUNGI— PHYCOMYCETES 

The  genus  Delacroixia  Constantin  (1897),  known  only  in  the 
conidial  phase,  is  clearly  very  closely  related  to  Conidioholus. 
It  contains  the  single  species,  D.  coronata  Constantin,  found 
growing  as  a  saprophyte  on  the  gills  of  mushrooms  and  on  orchid 
seed.  Gallaud  (1905)  has  studied  the  form  in  culture  in  nutrient 
solutions  and  on  various  soUd  media.  Until  its  resting  spores 
are  discovered  its  position  will  remain  somewhat  in  doubt. 

3.  Completoria  Lohde  (1874). 

The  genus  Completoria  contains  a  single  species,  C.  complens 
Lohde,  parasitic  on  prothallia  of  various  ferns.  It  has  been 
studied  extensively  by  Leitgeb  (1881)  in  Europe  and  by  Atkinson 
(1894)  in  America. 

The  vegetative  portion  of  the  fungus  consists  of  a  more  or 
less  compact  botryose  cluster  of  short,  oval,  or  somewhat  curved 
hyphal  branches  originating  from  a  common  center  and  present- 
ing on  the  surface  a  convoluted  appearance  (Fig.  104).  This 
vegetative  body  is  confined  at  first  to  a  single  host  cell,  and  is 
often  small  and  inconspicuous,  being  composed  of  only  a  few 
branches  closely  recurved  upon  the  parent  hyphae.  At  times  it 
is  larger,  completely  filling  even  a  large  host  cell.  At  maturity 
it  usually  spreads  to  neighboring  cells,  certain  peripheral  branches 
merely  putting  out  slender  threads  which  pierce  the  intervening 
walls.  Such  a  thread  on  reaching  the  center  of  the  new  cell 
cavity  enlarges  at  its  tip  to  form  an  oval  body  into  which  the 
protoplasm  of  the  parent  cell  flows.  This  oval  enlargement  then 
puts  out  short  protuberances  which  become  enlarged  at  a  short 
distance  from  their  point  of  origin,  undergo  branching,  and  soon 
give  the  botryose  appearance  of  the  parent  thallus. 

Under  certain  conditions  the  fungus  produces  resting  spores. 
They  are  formed  in  the  interior  of  the  thallus,  ten  or  more  often 
being  found  in  a  compact  group  surrounded  by  the  smaller, 
terminal,  then  empty,  peripheral  branches.  The  resting  spore 
is  globose  to  oval,  and  at  maturity  is  provided  with  a  smooth, 
three-layered  wall.  Its  sexual  nature  has  not  been  demonstrated. 
Asexual  reproduction  by  means  of  aerial  conidia  sometimes 
occurs.  The  conidia  in  their  shape  and  method  of  formation 
resemble  those  of  other  members  of  the  order,  and  at  maturity 
are  forcibly  ejected.  Inclusion  of  the  genus  in  the  Entomoph- 
thorales  rests  chiefly  on  a  consideration  of  the  conidial  stage. 
I'he  resting  spore,   though  tentatively  termed  an  oospore  by 


ENTOMOPHTHORALES 


289 


Atkinson  has  been  regarded  by  others  as  a  chlamydospore  or 
azygospore. 


Fig.  104. — Completoria  complens  Lohde.  (a)  Botryose  cluster  of  cells  com- 
prising the  thallus,  germinating  in  water  to  form  long  tubes,  (b)  Host  cell 
containing  the  thallus  of  the  parasite,  two  peripheral  colls  of  which  have  developed 
tubes  and  penetrated  adjacent  host  cells,  (c)  Two  young  thalli  still  showing 
attachment  to  penetration  tubes  which  entered  from  other  host  cells,  (d) 
Several  cells  of  thallus  forming  resting  spores;  one  developing  a  conidium. 
(e,  /)  Resting  spores  surrounded  by  empty  peripheral  cells,  (g)  Resting  spores 
and  a  single  fully  formed  conidium.  {h}  Germinating  conidium.  {After 
Atkinson  1895.) 

4.  Massospora  Peck  (1879:  44). 

The  genus  was  founded  on  a  single  species,  M.  cicadina  Peck, 
parasitic  on  the  seventeen-year  cicada,    Tibicina  septendecim. 


290 


THE  LOWER  FUNGI— PHYCOMYCETE^ 


It  was  regarded  by  Peck  as  a  relative  of  Protomyces,  but  Thaxter 
(1888)  and  Forbes  (1888)  working  independently  transferred 
it  to  the  Entomophthoraceae.  Their  knowledge  of  the  fungus 
was  very  imperfect,  and  its  real  nature  has  been  elucidated  only 
recently  by  Speare  (1921).  Though  clearly  a  member  of  the 
Entomophthoraceae  it  differs  from  the  other  genera  in  several 
outstanding  respects. 

The  vegetative  growth  of  the  fungus  is  confined  to  the  softer 
tissues  in  the  posterior  segments  of  the  body  of  the  host.  These 
segments,  as  a  result  of  their  complete  destruction,  disintegrate 


Fig.  105. — Masso/spora  cicadina  Peck,  (o)  Group  of  coiiidiophores.  (h) 
Conidial  formation,  (c)  Conidium.  {d)  Resting  spores  formed  as  buds  from 
hyphal  bodies,      (e)  Mature  resting  spore.      {After  Speare  1921.) 


progressively  forward  until  as  much  as  half  of  the  body  of  the 
insect  has  fallen  away  (Fig.  106).  Meanwhile  the  host  remains 
alive  for  a  considerable  period,  and  may  fly  and  crawl  about 
among  its  fellows.  This  process  of  sloughing  off  of  the  body  of 
the  insect  is  unknown  in  other  genera  of  the  Entomophthoraceae 
and  is  here  concerned  in  spore  dispersal.  In  Massospora  the 
conidia  are  neither  borne  over  the  surface  of  the  host  nor  ejected 
forcibly  from  the  tips  of  the  conidiophores.  They  are  formed 
within  the  body  of  the  insect  (see  Amer.  Jour.  Bot.,  16  :  394,  1929) 
and,  though  delimited  on  the  conidiophore  in  the  manner  usual 
in  this  group,  are  held  in  the  approximate  position  in  which 
produced,  finally  cohering  with  one  another  to  form  a  powdery 
mass  of  spores.     They  are  exposed  by  the  disintegration  of  the 


ENTOMOPHTHORALES 


291 


intersegmental  abdominal  membranes  of  the  host,  and  falling 
away  gradually,  are  disseminated  by  the  wind.  The  conidia, 
unlike  those  of  other  genera,  are  markedly  verrucose  instead  of 
smooth  (Fig.  105).  The  early  stages  of  mycelial  development 
have  not  yet  been  satisfactorily  observed,  but  in  later  phases 
hyphal  bodies  are  present,  and  give  rise  to  conidiophores  and 


Fig.  106. — iMassospora  cicadina  Peck  on  periodical  cicada  {Tihicina  septen- 
decim  L.).  (a)  Portions  of  the  anterior  four  abdominal  segments  dissected  away 
to  expose  the  mass  of  resting  spores  within,  (b)  The  abdomen  with  the  attached 
mass  of  conidia  after  considerable  natural  sloughing  off  has  occurred.  (After 
Spear  e  1921.) 


resting  spores.  The  latter  are  spherical,  slightly  brownish,  and 
have  beautifully  reticulated  walls.  Each  resting  spore  arises  as 
a  bud  from  a  hyphal  body  and  is  apparently  asexually  produced. 
In  the  present  state  of  knowledge  these  spores  are  to  be  regarded 
as  azygospores,  but  a  more  critical  study  of  their  method  of 
formation  is  desirable.  No  data  are  available  bearing  on  the 
question  of  how  the  fungus  passes  the  long  period  during  which 
the  host  remains  under  ground. 


292  THE  LOWER  FUNGI— PHYCOMYCETES 

Three  other  species  have  been  referred  in  the  hterature  to 
this  genus.  One,  M.  richteri  Bresadola  &  Staritz  (Staritz, 
1892),  was  subsequently  transferred  to  Empusa  (Bubak,  1906: 
105).  The  remaining  two,  M.  cleoni  Wize  (1905:  716)  and 
M.  starilzii  Bresadola  (1892:  133)  are  so  imperfectly  known  that 
their  inclusion  here  must  be  regarded  as  merely  tentative. 
5.  Empusa  Cohn  (1855:  301). 

syn.  Entomophthora  Fresenius  (1856:  882). 
Lamia  Nowakowski  p.p.  (1884:  153). 
Tarichium  Cohn  p.p.  (1875:  58). 

The  members  of  this  genus  are  all  entomogenous,  and  were  long 
thought  to  be  obligate  in  their  parasitism.  In  recent  years 
several  species  have  been  induced  to  grow  saprophytically  on 
artificial  culture  media  (Sheldon,  1903;  Speare,  1912;  Sawyer, 
1929)  and  it  is  probable  that  others  will  be  obtained  in  culture 
when  the  proper  conditions  are  provided. 

In  nature,  infection  of  the  host  results  when  a  germ  tube 
from  the  conidium  penetrates  the  outer  covering  of  the  insect 
and  enters  the  body  cavity.  In  the  host  the  infection  thread 
usually  does  not  develop  a  profusely  branching  mycehum. 
Instead  it  forms  short  thick  segments  which  break  apart  from 
one  another,  and  undergo  a  process  of  division  and  budding. 
These  segments  are  termed  hyphal  bodies.  The  process  is  con- 
tinued until  the  body  cavity  is  almost  wholly  filled  with  them. 
Meanwhile,  powerful  enzymes  are  excreted  which  quickly  dissolve 
the  various  internal  structures  of  the  host  until  practically 
nothing  remains  but  the  chitinous  outer  coat.  Under  unfavor- 
able environmental  conditions  the  hyphal  bodies  may  assume 
heavier  walls,  and  enter  a  period  of  rest  as  chlamydospores.  On 
the  return  of  favorable  conditions  they  germinate  quickly  and 
proceed  at  once  to  the  formation  of  conidiophores.  In  the  more 
normal  development  chlamydospores  are  lacking  and  the  conidio- 
phores arise  from  the  thin-walled  hyphal  bodies.  They  penetrate 
the  outer  covering  of  the  host  and  form  conidia  in  the  air.  In 
some  species  the  primary  hypha,  without  branching,  abjoints 
terminally  a  single  conidium.  In  others  considerable  branching 
may  occur,  each  ultimate  branch  becoming  a  conidiophore.  In 
either  case  the  conidium  is  formed  as  a  bud  at  the  apex  of 
the  clavate  termination  of  the  conidiophore.  It  enlarges  as  the 
protoplasm  of  the  conidiophore  passes  into  it,  and  when  the 
mature  shape  and  size  have  been  attained  it  is  cut  off  from  the 


EN  TO  MOPH  THORALES 


293 


conidiophore  by  a  transverse  septum.     This  conidium  is  clearly 
the  homologue  of  the  sporangium  of  the  Mucorales,  and  the 


Fig.  107.' — Empusa  spp.  (a-d)  Primary  conidia  of  four  different  species  showing 
variation  in  shape,  (e,  /)  Primary  "conidium"  after  period  in  water  showing 
spore  floating  free  within  sporangial  wall;  the  conidium,  therefore,  a  monosporic 
sporangium,  (g)  Primary  conidium  at  left  and  secondary  at  right  showing 
different  form  in  same  species,  (h)  Layer  of  unbranched  conidiophores  (k) 
One  of  these  ready  to  discharge  the  conidium.  (m)  Branched  conidiophores  of 
another  species,  (n,  o)  Primary  conidia  germinating  and  forming  secondary 
conidia.  (p)  Rhizoids  of  two  different  species,  serving  to  attach  host  to  sub- 
stratum, (r)  Germination  of  a  hyphal  body,  (s)  Primary  conidia  germinating 
by  capillary  tubes  to  form  secondary  conidia.      (After  Thaxtcr  1888.) 


septum  is  essentially  the  same  as  the  columella  in  that  group.     In 
fact  as  emphasized  by  Thaxter  (1888:  143,  yig.  321)  the  cell  may 


294  THE  LOWER  FUNGI— PHYCOMYCETES 

be  regarded  as  a  one-sporcd  sporangium,  for  after  it  is  cut  off  a 
second  spore  wall  is  formed  about  the  protoplast.  Although 
the  two  walls,  that  of  the  sporangium  and  that  of  the  sporangio- 
spore,  are  normally  in  close  apposition  they  sometimes  become  so 
widely  separated  through  the  absorption  of  water  that  the  spore 
may  be  seen  floating  in  the  sporangium  (Fig.  107). 

As  the  conidium  approaches  its  mature  size  its  contents  and 
those  of  the  conidiophore  absorb  water  rapidly.  The  osmotic 
force  exerted  is  greater  in  the  conidiophore,  and  the  septum  is 
pushed  into  the  conidium  as  a  definite  columella.  Later  the 
contents  of  the  conidium  becoming  more  dense,  exert  the  greater 
pressure,  and  the  columella  is  forced  back  into  the  conidiophore, 
its  former  position  thus  being  reversed.  Finally  the  pressure 
exerted  is  so  strong  that  the  outer  of  the  two  walls  enclosing  the 
conidium  ruptures  transversely  in  a  circle  about  its  base,  and 
the  conidium  is  discharged  violently  into  the  air  and  carried  a 
considerable  distance.  The  conidia  of  different  species  vary 
greatly  in  size,  and  range  in  shape  from  spherical  to  ellipsoidal. 
The  wall  is  always  smooth  (never  verrucose  as  in  Massospora), 
and  is  covered  with  an  adhesive  material  which  serves  to  fasten 
the  conidium  to  the  object  on  which  it  falls.  Should  it  fail  to 
strike  an  insect  host  it  may  put  out  a  germ  tube,  and,  on  this, 
form  a  secondary  conidium  which  is  in  turn  discharged.  This 
process  may  be  repeated  until  the  vitality  of  the  protoplasm  is 
exhausted  or  a  susceptible  host  encountered.  Other  more 
abnormal  variations,  in  which  secondary  conidia  bud  directly 
from  the  primary  or  in  which  thicker-walled  resting  conidia  are 
formed,  occur  under  unfavorable  conditions. 

In  most  species  the  conidiophores  emerge  in  great  numbers 
from  the  host  through  the  less  resistant  portions  of  its  surface 
and  form  tufts  or  definite  palisade  layers  evident  to  the  unaided 
eye  as  felt-like  masses,  powdery  with  conidia.  The  color 
is  usually  white,  but  may  vary  to  some  shade  of  gray  or  green. 
Occasionally  sterile  hyphae  protrude  beyond  the  layer  of  conidio- 
phores. These  have  been  termed  paraphyses  by  some  authors 
and  by  others  cystidia.  As  the  host  sickens  and  dies  hyphae 
are  sometimes  pushed  out  from  its  body  to  anchor  it  firmly  to  the 
substratum.  These  are  termed  rhizoids.  They  occur  chiefly  in 
species  having  branched  conidiophores. 

True  zygospores  resulting  from  a  sexual  conjugation  are 
formed  in  some  species,  but  in  others  the  resting  spore  is  devel- 


ENTOMOPHTHORALES 


295 


oped  asexually  (Fig.  108).  The  spore  formed  in  the  latter  case  is 
morphologically  equivalent  to  the  zygospore,  and  is  termed  the 
azygospore.  The  true  zygospore  is  formed  when  two  hyphal 
bodies  or  two  mycelial  cells  conjugate.  The  young  zygospore 
arises  as  an  outgrowth  from  one  of  the  conjugating  cells,  or  may 


Fig.  108. — Empusa  spp.  (a-c)  Zygospore  formation  between  cells  of  hyphae 
in  three  different  species,  (d)  Three  stages  in  zygospore  formation,  (e)  Echinu- 
late  zygospore  typical  of  one  species,  (y,  h)  Terminal  and  intercalary  azygo- 
spores.  (m)  Successive  steps  in  conjugation  of  hyphal  bodies  to  form  zygospores. 
(After  Thaxtcr  1888.) 


bud  out  from  their  point  of  union  as  in  Piptocephalis.  At 
maturity  it  is  usually  large  and  spherical,  and  may  be  character- 
istically roughened.  The  fusing  cells  are  plurinucleate.  Though 
fusion  of  the  nuclei  in  pairs  at  the  time  of  zygospore  germination 
was  suspected  by  Riddle  (1906:  184),  it  has  not  yet  been  demon- 
strated. In  azygospore  formation  a  bud  is  put  out  from  a  hyphal 
body  or  mycelial  cell,  and  enlarges  to  form  a  spore  similar  to  the 


296  THE  LOWER  FUNGI— PHYCOMYCETES 

zygospore.  The  details  of  zygospore  and  azygospore  formation 
are  given  by  Riddle  (1906)  and  Thaxter  (1888). 

The  genus  Empusa  was  founded  by  Cohn  (1855)  on  the  house 
fly  parasite,  E.  muscae.  The  name  Empusa  had  been  applied 
earlier,  however,  to  a  genus  of  orchids,  and  Fresenius  (1856:  882) 
recognizing  this  fact  proposed  Entomophihora  to  replace  Empusa 
for  the  fungus  genus.  Later  both  names  were  used  together  in 
the  Entomophthoraceae  by  Nowakowski  (1884)  and  Brefeld 
(1877)  for  two  distinct  generic  concepts.  Nowakowski  separated 
the  known  entomogenous  species  into  three  genera,  Empusa, 
Entomophthora,  and  Lamia.  His  treatment  was  followed  by 
others,  including  Schroter  (1893)  who  uses  it  in  Engler  und 
Prantl's  Die  Natiirliche  Pflanzenfamilien.  In  this  arrangement 
Entomophthora  is  characterized  by  branched  conidiophores,  the 
presence  of  rhizoids  and  cystidia,  and  the  production,  in  at  least 
some  species,  of  true  sexually  formed  zygospores.  Empusa,  as 
limited,  lacks  rhizoids  and  cystidia,  has  unbranched  conidio- 
phores, and  forms  azygospores  instead  of  zygospores.  Lamia  is 
said  to  be  intermediate,  differing  from  Empusa  chiefly  in  the 
possession  of  cystidia. 

Thaxter  (1888)  who  gave  us  the  first  really  critical  account 
of  the  group  states  that  these  characters  are  inconstant,  and 
that  border  line  species  make  the  maintenance  of  this  separation 
impossible.  He  unites  all  the  species  in  a  single  genus  under 
the  name  Em,pusa. 

Some  years  after  the  appearance  of  Thaxter's  paper  Cavara 
(1899)  studied  cytologically  two  species,  Empusa  muscae  and 
Entomophthora  delpiniana,  and  found  that  while  in  the  former  the 
conidia  are  typically  multinucleate,  they  are  uninucleate  in  the 
latter.  Riddle  (1906)  then  investigated  seven  other  species,  and 
found  that  the  conidia  of  the  species  which  had  been  referred  to 
Empusa  are  regularly  multinucleate  while  those  of  the  species 
placed  in  Entomophthora  are  uninucleate.  Olive  (1906:  202) 
obtained  similar,  though  less  definite,  results  in  five  additional 
species.  He  showed  that  the  branching  habit  of  the  conidiophore 
is  correlated  with  the  uninucleate  condition  of  the  conidia. 
In  forms  such  as  Empusa  muscae  all  the  nuclei  in  the  vegetative 
cell  from  which  the  conidiophore  arises  flow  out  into  the  conidium. 
In  species  like  Entomophthora  sciarae,  on  the  other  hand,  the 
coenocytic  conidiophore  is  divided  by  septa  into  uninucleate 
cells.     Each  cell  then  pushes  out  laterally  and  elongates  until 


ENTOMOPHT  MORALES  297 

the  surface  of  the  host  is  reached  and  penetrated.  A  branching 
conidiophore  thus  results,  each  branch  of  which  abjoints  termi- 
nally a  single  uninucleate  conidium. 

These  observations  indicate  that  the  earlier  usage  of  Nowa- 
kowski  in  applying  the  names  Empusa  and  Eyitomophthora  to 
species  with  unbranched  and  branched  conidiophores  respectively 
was  probably  in  the  main  phylogenetically  sound,  and  it  is  not 
unlikely  that  later  students  will  return  to  it.  However,  the 
monograph  of  Thaxter  has  long  been  the  standard  treatment  of 
the  group,  and  the  writer  prefers  to  follow  it  in  incorporating 
all  the  species  in  the  single  genus  Empusa.  Departure  from  this 
nomenclature  at  present  would  be  premature,  and  result  in  chang- 
ing various  well  known  names.  In  any  case  additional  species 
must  be  investigated  cytologically  before  the  nuclear  condition 
of  the  conidium  can  be  said  to  have  unquestioned  taxonomic 
value. 

Thaxter's  use  of  the  generic  name  Empusa  in  preference  to 
Entomophthora  will  be  questioned  by  some  students  in  the  light 
of  present  rules  of  nomenclature.  Although  Empusa  is  the  older, 
its  earlier  use  in  the  orchids  holds  the  possibility  of  confusion 
in  the  event  of  its  future  resurrection  there.  It  has  not  seemed 
necessary  in  view  of  this  somewhat  unstable  situation  to  use  the 
family  name  Empusaceae  or  the  ordinal  name  Empusales. 

The  genus  Empusa,  as  here  treated,  is  by  far  the  largest 
genus  of  the  family.  Only  four  species  were  known  to  occur  in 
the  United  States  before  Thaxter's  monograph  appeared.  He 
described  a  total  of  twenty-six.  At  present  approximately  forty 
species  are  known. 

The  genus  Tarichium  Cohn  (1875:  58)  was  based  on  the  resting 
spore  condition  of  an  unknown  species  of  Empusa.  There  is  no 
reason,  therefore,  for  recognizing  it  as  a  distinct  genus. 

The  fungus  described  by  Krassilstschik  in  1886  as  Tarichium 
uvella,  and  in  1888  redescribed  by  Sorokin  as  Sorosporella  agro- 
tidis,  has  been  referred  by  various  authors  to  the  Entomoph- 
thoraceae.  Recently  it  has  been  shown  by  Speare  (1920:  399) 
to  belong  instead  to  the  verticilliaceous  hyphomycetes. 

The  green  muscardine  fungus,  Metarrhizium  anisopliae 
(Metsch.)  Sorokin,  which  has  been  incorporated  by  some  students 
in  the  Entomophthoraceae  near  Empusa  is  here  excluded  from  the 
family.  It  apparently  (Stevenson,  1918)  belongs  near  Peni- 
cillium.     It  is  an  important  parasite  of  many  insects,  some  of 


298  THE  LOWER  FUNGI—PHYCOMYCETES 

which  are  of  considerable  economic  importance,  and  the  literature 
dealing  with  it  is  very  extensive.  The  following  papers  bear  on 
the  question  of  its  taxonomic  position:  Friederichs  (1920:335), 
Speare  (1912:  pi.  5,  fig.  a),  Rorer  (1913:  88,  pi.  7). 

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Urniejejndsci  zu  Krakau,  8:  153-183,  pi.  5,  1884. 
Olive,  E.  W.,  Cj^tological  studies  on  the  Entomophthoreae.     Botan.  Gaz., 

41:  192-208,  229-261,  pi.  I4-I6,  1906. 
-,  Cell  and  nuclear  division  in  Basidiobolus.    Ann.  Mycol.,  6 :  404-418, 

pi.  10,  1907. 
Peck,  Chas.,  Massospora  gen.  nov.     Thirty-first  Report,  N .  Y.  State  Museum 

Nat.  Hist.,  p.  44,  1879. 
Pettit,  R.  H.,  Studies  in  artificial  cultures  of  entomogenous  fungi.     Neio 

York  {Cornell)  Agr.  Exp.  Sta.  Bui.  97:  339-378,  pi.  1-11,  1895. 


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Riddle,  L.  W.,  On  the  cytology  of  the  Entomophthoraceae.     Proc.  Amer. 

Acad..  Arts.  &  Sci.,  42:  177-197,  pi.  1-3,  1906. 
RoRER,  J.  B.,  The  use  of  the  green  muscardine  in  the  control  of  some  sugar 

cane  pests.     Phytopathology,  3:  88,  pi.  7,  1913. 
Sawyer,   W.  H.,   Observations  on  some  entomogenous  members  of  the 

Entomophthoraceae   in   artificial  culture.     Amer.  Jour.   Botany,    16: 

87-121,  pi.  9-12,  1929. 
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Schlesien  S^:  814  pp.,  1889. 
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Prantl),  V:  134-141,  ^g^.  121-127,  1893. 
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tory Methods,  6:  2212-2221,  1903. 
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Work  Exp.  Sta.  Hawaiian  Sugar  Planters'  Assoc.  Bui.  12:  1912. 
,  Further  studies  of  Sorosporella  uvella,  a  fungous  parasite  of  noctuid 

larvae.     Jour.  Agr.  Res.,  18 :  399-440,  pi.  51-56,  1920. 
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cicada.     Mycologia,  13:  72-82,  pi.  5,  6,  1921. 
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Stevenson,  J.  H.,  The  green  muscardine  fungus  in  Porto   Rico.     Jour. 

Dept.  Agric.  Porto  Rico,  2:  19-32,  pi.  1,  1918. 
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Soc.  Nat.  Hist.,  4:  133-201,  pi.  14-21,  1888. 
VuiLLEMiN,  P.,  Developpement  des  azygospores  chez  les  Entomphthorees. 

Compt.  Rend.  Acad.  Sd.  Paris,  130:  522-524,  1900.     (Also  in  Compt. 

Rend.  Assoc.  Franc.  Avanc.  Sci.  Congres  de  Paris,  pp.  670-683,  pi.  6, 

1900.) 
Winter,    G.,    Zwei   neue    Entomophthoreen    Formen.     Bot.   Centralb.,    5: 

62-64,  1881. 
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russelkafers  (Cleonus  punctiventris  Germ.)  mit  besonderer  Beriicksichti- 

gung   neuer    Arten.     Bui.   Inter.  Acad.  Sci.  Cracovie,  1904:  713-727, 

1905. 
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bolus  Ranarum  Eidam.     Flora,  93:  87-97,  pi.  4,  1904. 
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Flora,  122:  159-166,  pi.  1,  2,  1927. 


CHAPTER  XI 

PHYCOMYCETOUS  AFFINITIES  OF  THE 
HEMIASCOMYCETES 

In  the  foregoing  treatment  of  the  Phycomycetes  it  has  been 
emphasized  (p.  21)  that  there  are  two  well  known  opposing 
theories  as  to  the  origin  of  the  fungi.  One  of  these  treats  the 
group  as  an  aggregation  of  relatively  unrelated  parts,  which 
have  degenerated  along  different  lines  from  widely  separated 
subdivisions  of  the  algae.  The  other  maintains  that  the  fungi 
are  monophyletic,  and  have  arisen  from  non-chlorophyll  bearing 
organisms  lying  below  the  level  of  the  lowest  of  the  present  day 
Phycomycetes. 

Advocates  of  the  former  theory  regard  the  Phycomycetes  and 
Ascomycetes  as  only  remotely  related,  and  believe  the  simplest 
of  the  Ascomycetes  to  be  degenerate  forms  which  have  been 
derived  in  relatively  recent  times  from  more  complex  Asco- 
mycetes. Adherents  of  the  other  theory  maintain  that  the 
higher  fungi  have  had  a  phycomycetous  ancestry,  and  regard 
the  simplest  of  the  Ascomycetes  as  primitive  and  clearly  related 
to  certain  of  the  higher  Phycomycetes.  In  order  that  this 
latter  point  of  view  might  be  adequately  presented  for  the  con- 
sideration of  the  student  interested  in  phylogeny  it  has  been 
necessary  to  incorporate  in  the  book  the  material  composing  this 
final  chapter.  This  inclusion  has  been  desirable  from  the 
standpoint  of  taxonomy  also,  since  some  of  the  forms  treated  by 
various  authors  as  simple  Ascomycetes  are  at  best  doubtful 
members  of  that  group,  and  may  be  regarded  by  other  writers  as 
belonging  to  the  Phycomycetes. 

The  essential  features  of  the  Ascomycetes  have  been  enumer- 
ated above  (p.  16)  in  the  introductory  chapter,  and  require 
little  elaboration  here.  It  should  be  recalled  that  the  group 
is  distinguished  by  the  ascus,  a  sac-Hke  cell  forming  endogenous 
spores  called  ascospores,  usually  in  small  and  definite  number 
(typically  eight,  less  frequently  some  other  multiple  of  two). 
It  should  be  remembered  too  that  the  ascus  and  sporangium 

301 


302  THE  LOWER  FUNGI— PHYCOMYCETES 

are  not  homologous  structures.  The  ascus  is  essentially  sexual 
in  character.  In  the  young  condition  it  is  binucleate.  The 
nuclei  fuse,  and  the  fusion  nucleus,  thus  formed,  undergoes 
three  mitoses  resulting  in  eight  nuclei.  At  the  close  of  the  last 
mitosis  the  astral  rays  cut  out  the  ascospores  in  the  interior 
of  the  cytoplasm,  the  process  being  one  of  free-oell  formation 
and  thus  differing  wholly  from  that  of  progressive  cytoplasmic 
cleavage  by  means  of  which  sporangiospores  are  formed.  In 
some  Ascomycetes  additional  mitoses  occur  and  the  mature 
ascus  is  polysporic.  The  number  of  ascospores,  even  in  such 
cases,  may  be  definite,  and  is  never  wholly  indefinite  in  the  com- 
plete sense  in  which  this  is  true  of  sporangiospores.  The  cyto- 
plasm not  incorporated  in  the  ascospores  is  termed  epiplasm, 
and  functions  in  many  species  in  maintaining  turgor  and  in 
effecting  spore  discharge.  Epiplasm  is  wholly  lacking  in  the 
sporangium,  though  in  a  few  forms  a  mucilaginous  secretion  lies 
between  the  spores  and  gives  a  similar  aspect. 

Though  the  ascus,  strictly  speaking,  is  not  homologous  with 
any  structure  in  the  Phycomycetes,  and,  in  its  typical  form  in 
the  higher  Ascomycetes,  is  clearly  a  new  development,  it  gives 
evidence  of  having  been  derived  from  the  sexual  apparatus 
of  the  Phycomycetes  rather  than  from  the  sporangium.  The 
sporangium  may  be  conceived  to  have  given  rise  to  the  conidium 
in  the  Ascomycetes  and  Basidiomycetes  as  well  as  in  the  higher 
Phycomycetes.  The  Ascomycetes  include  a  very  large  number 
of  fungi,  and  in  certain  features  of  morphology  are  extremely 
various.  In  the  standard  classification  presented  by  Schroter 
(1894)  the  group  is  split  into  the  three  primary  subdivisions, 
Hemiascomycetes,  Ptotoascomycetes  and  Euascomycetes. 

The  group  Euascomycetes  is  much  the  largest  of  the  three,  and 
includes  all  the  highly  developed  forms.  In  practically  all  of  its 
members,  asci  are  aggregated  in  definite  fashion  in  a  more  or  less 
conspicuous  fruit  body  termed  the  ascocarp.  In  one  of  the  major 
subdivisions  of  the  Euascomycetes,  known  as  the  Piscomycetes, 
the  ascocarp  is  a  typically  open,  cup-shaped  or  saucer-shaped 
body  lined  with  a  palisade  layer  of  asci,  and  receives  the  special 
name  apothecium.  In  another  large  group,  the  Pyrenomycetes, 
it  is  a  typically  closed,  spherical  or  flask-shaped  structure 
enclosing  the  asci,  and  is  termed  the  perithecium. 

The  Protoascomycetcs  as  treated  by  Schroter  include  the 
Saccharomycetaceae (yeasts),  Endomycetaceae,  Exoascaceae  (leaf 


PHYCOMYCETOUS  AFFINITIES  303 

curl  fungi),  and  Ascocorticiaceae.  These  forms  correspond  with 
the  Euascomycetes  in  that  the  ascus  contains  usually  a  small 
and  definite  number  of  spores,  but  they  differ  from  them  in 
that  a  definite  ascocarp  is  lacking.  The  asci  are  scattered 
without  order  over  a  mould-like  mycelium  or  exist  as  wholly 
isolated  cells. 

The  Hemiascomycetes  in  Schroter's  classification  embrace  a 
relatively  small  number  of  species,  regarded  by  him  as  the 
most  primitive  of  the  known  Ascomycetes.  In  the  group,  as 
characterized  by  him,  a  fruit  body  is  lacking  and  the  ascus 
contains  a  large  and  indefinite  number  of  spores.  He  recognized 
for  these  forms  three  families,  Ascoideaceae,  Protomycetaceae, 
and  Monascaceae.  An  additional  family,  Thelebolaceae,  had 
meanwhile  been  erected  by  Brefeld  (1891).  These  families  in 
fact  do  not  constitute  natural  groups,  and  subsequent  investiga- 
tion has  shown  that  the  genera  included  in  them  represent  for 
the  most  part  miscellaneous  collections  of  unrelated,  doubtful, 
or  misunderstood  fungi. 

The  family  Thelebolaceae  was  founded  by  Brefeld  (1891) 
on  the  single  genus  Theleobolus  Tode  (1790:  41),  and  was  incor- 
porated by  him  and  by  Lindau  (1894;  1905)  in  the  Hemiasco- 
mycetes. The  genus  name  has  been  spelled  by  other  authors 
Theleholus  and  Telebolus.  No  other  genus  has  been  added  to 
the  family,  and  it  is  now  recognized  as  closely  related  to  Rhj- 
parohhis  of  the  Ascobolaceae,  a  family  of  the  Discomycetes.  It 
is  so  treated  by  Saccardo  (1928)  and  Rehm  (1896).  Two 
species,  Thel.  stercoreus  Tode  and  Thel  zukalii  Heimerl.  have 
been  studied  cytologically  by  Ramlow  (1906;  1914).  Although 
the  mature  ascus  is  multinucleate  and  multispored  it  is  enclosed 
in  a  definite  fruit  body  and  arises  from  a  binucleate  cell  of  a 
coiled  archicarp  such  as  occur  in  other  genera  of  the  Ascobolaceae. 
One  to  several  asci  are  formed  in  the  fruit  body.  The  genus 
contains  several  species  in  addition  to  the  two  studied  by  Ramlow. 
The  family  Monascaceae  as  presented  by  Schroter  includes 
three  genera,  Monascus  van  Tieghem,  Ilelicosporangium  H. 
Karsten,  and  Papulaspora  Preuss.  Through  the  subsequent 
incorporation  of  all  of  these  in  other  groups  the  family  has  auto- 
matically disappeared.  In  Monascus  a  definite  ascocarp  is 
formed  resembhng  that  of  the  Aspergillaceae,  and  the  genus  is 
clearly  a  member  of  that  group.  The  early  deliquescence  of 
the  ascus  walls,  and  the  consequent  freeing  of  many  spores  into 


304  THE  LOWER  FUNGI— PHYCOMYCETES 

the  central  cavity  of  the  fruit  body  led  van  Tieghem  to  regard  the 
latter  as  a  multispored  ascus.  The  papers  of  Barker  (1903), 
Ikeno  (1903),  and  OHvc  (1905)  have  clarified  the  situation. 
The  position  of  the  Aspergillaceae  in  the  classification  is  dis- 
cussed below.  The  genera  Helicosporanghim  and  Papulaspora 
have  been  studied  in  recent  years  by  Hotson  (1912).  He  merges 
them  under  the  latter  name,  and  regards  the  group  as  a  form 
genus  characterized  by  peculiar  vegetative  structures  called 
bulbils  which  are  evidently  merely  sclerotia  of  loose  structure. 
The  genus  must  be  included  in  the  group  of  sterile  fungi  with 
such  genera  as  Ozonium,  Sclerotium,  and  Rhizoctonia.  Its 
species  have  been  shown  to  have  fruiting  stages  representative  of 
various  groups  of  the  fungi.  Complete  misinterpretation  of  the 
nature  of  the  bulbil  led  to  the  inclusion  of  these  forms  in  the 
Hemiascomycetes. 

The  family  Protomycetaceae,  as  treated  by  Schroter,  includes 
two  genera  Protomijces  Unger  (1833)  and  Endogone  Link  (1809). 
These  are  not  in  fact  closely  related.  Endogone  has  been  dis- 
cussed in  a  preceding  chapter  as  a  member  of  the  Mucorales. 
As  now  understood  the  Protomycetaceae  include  three  genera, 
Protomyces,  Protomycopsis,  and  Taphridium.  These  constitute 
a  coherent  group  of  definitely  related  forms.  The  species  are  all 
parasitic  in  higher  plants.  The  mycelium  consists  of  delicate, 
intercellular,  septate,  branching  hyphae,  which  bear  large, 
globose  to  ellipsoidal,  thick-walled,  unicellular  chlamydospores 
as  terminal  or  intercalary  enlargements.  The  chlamydospore 
after  a  period  of  rest  germinates  by  the  rupture  of  the  thick 
exospore  and  the  extrusion  of  the  thin  endospore  as  a  globose 
or  cylindrical  sac.  The  contents  of  the  chlamydospore,  before 
or  after  passing  into  the  sac,  are  broken  up  into  a  large 
number  of  small  unicellular  spores.  These  are  disseminated  by 
the  violent  apical  rupture  of  the  sac,  and  after  their  escape  may 
undergo  copulation  in  pairs.  In  germination  they  produce  the 
endophytic  mycelium  directly,  or  in  nutrient  solutions  bud  like 
yeasts.  The  chlamydospore  is  multinucleate  in  young  stages 
and  is  probably  so  from  the  first,  the  nuclei  being  scattered 
without  order  throughout  the  cytoplasm.  In  Protomyces  and 
Protomycopsis  they  pass  over  thus  with  the  cytoplasm  into  the  sac- 
like extruded  endospore  (Fig.  109).  Vacuoles  then  appear,  and 
when  the  sac  is  fully  formed  the  cytoplasm  and  nuclei  constitute 
a  thin  peripheral  layer  surrounding  a  single  large  central  vacuole. 


PH  YCOM  YCETO  US  A  FFIXI  TIES 


805 


This  layer  at  maturity  is  split  by  cleavage  planes  to  form  many 
small,  prismatic,  uninucleate  segments  lining  the  wall.  These 
may  well  be  termed  spore  mother  cells,  for  the  nucleus  in  each 
divides  twice  to  give  four,  and  four  uninucleate  spores  round  up 
in  each.  Finally  these  spore  tetrads  break  apart  and  the  spores 
recede  from  the  periphery  of  the  sac  to  become  aggregated  in  a 
ball  near  its  tip.  They  are  then  ready  for  discharge.  In 
Taphridium  essentially  the  same  condition  exists,  except  that  the 
spores  are  formed  at  the  periphery  of  the  chlamydospore  before 


Fit;.  109. — (a)  Protomyccs  pachydcrmus  Thi'iai.  ( ■hhiniydosporc  with  extruded 
sac-like  endospore  in  section  at  stage  when  spore-mother  cells  line  the  sac. 
(6)  P.  kriegerianus  Biiren.  Later  stage;  the  spores  aggregated  in  the  apical 
region  of  the  extruded  sac.      (After  Biiren  1915,  1922.) 


the  extrusion  of  its  endospore  to  form  the  sac.  The  two  nuclear 
divisions  concerned  in  the  formation  of  the  spore  tetrads 
perhaps  accomplish  reduction  but  the  point  is  as  yet  in  doubt. 
It  is  not  certain,  moreover,  that  nuclear  fusion  occurs  in  the 
copulating  spores. 

The  genus  Protomyces  linger  (1833)  is  the  largest  of  the  three 
composing  the  family.  Biiren  (1915;  1922)  gives  a  thorough 
taxonomic  treatment  of  its  species  for  Switzerland.  The  type 
species,  P.  macrosponis  linger,  is  confined  to  the  Umbelliferae, 
but  is  composed  of  at  least  seven  distinct  biologic  races.  Ten  or 
more  species  occur  on  Compositae.  Cytological  conditions  in 
the  genus  have  been  studied  chiefly  in  P.  macrusporuH  and  P. 
pachydermits.  The  cells  of  the  mycelium  are  multinucleate. 
The  papers  of  Biiren  (1913;  1914  a,  h;  1915;  1922),  Popta  (1899), 


306  THE  LOWER  FUNGI— PHYCOMYCETES  • 

and  Juel  (1902  h;  1921)  constitute  the  literature  on  the  cytology 
of  the  forms.  Ramsbottom  (1915;  1916)  has  contributed 
valuable  comments  on  these.  In  Protomyces  the  endogenous 
spores  are  delimited  within  the  endospore  after  its  extrusion, 
the  chlamydospores  are  intercalary  with  a  smooth  membrane,  and 
the  endogenous  spores  copulate  regularly  in  pairs. 

In  the  genus  Protomycopsis  Magnus  (1905)  the  endogenous 
spores  are  formed  within  the  extruded  endospore  as  in 
Protomyces,  but  they  do  not  copulate.  The  chlamydospore  is, 
moreover,  terminal  and  provided  with  a  warty  exospore.  The 
genus  includes  at  least  eight  or  ten  species  (Biiren,  1915;  1922), 
the  type  being  Protomyco'psis  leucanthemi  Magnus  on  Chrysanthe- 
tnum  leucanthemum. 

In  the  genus  Taphridium  Lagerheim  &  Juel  (Juel,  1902  h) 
the  endogenous  spores  are  delimited  in  a  peripheral  layer  within 
the  chlamydospore  before  the  extrusion  of  its  endospore. 
The  genus,  as  known  at  present,  embraces  three  species, 
T.  umhelliferanun  (Rostrup)  Lag.  &  Juel  on  Umbelliferae,  T. 
rhaetica  (Volkart)  Maire  on  Crepis  spp.,  and  T.  algeriense  Juel  on 
Ferula  communis.  The  first  named  is  the  type  of  Taphridium, 
the  second  the  type  of  Volkartia  Maire  (1907:145).  Due  to 
ignorance  of  life  cycles  and  to  varying  conceptions  of  generic 
limits  the  nomenclatorial  situation  here  has  become  much 
confused.  In  the  light  of  present  knowledge  the  merging  of 
Taphridium  and  Volkartia  seems  necessary.  In  at  least  one 
species  the  spores  have  been  described  as  fusing  in  pairs  after 
their  escape. 

The  position  of  the  family  Protomycetaceae  in  the  natural 
system  is  in  doubt,  any  disposition  of  it  being  to  an  extent 
dependent  upon  the  interpretation  given  to  the  structures  and 
phenomena  just  described.  Unless  the  extruded  endospore  be 
regarded  as  a  many-spored  ascus  there  would  seem  to  be  no  reason 
for  incorporating  these  forms  in  the  Ascomycetes.  The  earlier 
view  of  de  Bary  that  these  fungi  are  intermediate  between  the 
chytrids  (Chytridiales)  and  smuts  (Ustilaginales)  is  at  least 
suggestive.  Biiren  (1915),  in  his  earlier  work,  regarded  the  spore 
mother  cells  as  comparable  to  asci  and  termed  the  whole  sac  a 
synascus.  He  was  inclined  toward  this  point  of  view  by  his 
assumption  that  nuclear  fusion  occurs  in  the  young  chlamydo- 
spore. His  later  observations  (Biiren,  1922)  led  him  to  reverse 
his  opinion,  some  evidence  of  nuclear  fusion  in  the  copulating 


PHYCOMYCETOUS  AFFINITIES  307 

spores  having  been  obtained.  Juel  (1921)  attempts  to  homolo- 
gize  the  chlamydospore  in  this  group  with  the  fertile  cells  of 
the  ascogenous  layer  in  the  Exoascaceae.  Gaumann  (1926) 
and  Gaumann  and  Dodge  (1928),  following  this  conception, 
embrace  the  two  families  in  the  single  order  Exoascales.  To  the 
author  there  seems  to  be  no  justification  for  this  point  of  view, 
inasmuch  as  the  spore  sac  of  Taphrina  and  Exoascus  is  clearly 
an  ascus  of  a  high  type.  As  treated  here  the  Protomycetaceae 
are  regarded  as  of  unknown  relationship.  They  may  represent 
an  isolated  hne  of  development  with  a  phycomycetous  ancestry, 
but  there  is  no  sure  basis  for  their  inclusion  in  the  Ascomycetes. 
Until  their  nuclear  history  is  better  understood  it  would  be  futile 
to  attempt  to  treat  the  group  more  definitely. 

Of  the  famihes  included  by  Schroter  in  the  Hemiascomycetes 
the  Ascoideaceae  alone  remain  for  consideration.  Two  genera 
Dipodascus  Lagerheim  (1892)  and  Ascoidea  Brefeld  (1891)  were 
incorporated  in  the  family  by  Schroter,  two  others,  Oscarhrefeldia 
Holtermann  (1898:  6)  and  Conidiascus  Holtermann  (1898:  23), 
were  added  by  Lindau.  There  is  insufficient  evidence  to  show 
that  any  two  of  these  four  genera  are  in  fact  closely  related. 

The  genus  Dipodascus  was  based  on  a  single  species  and  is 
still  monotypic.  This  species,  D.  alhidus  Lagerheim,  was  first 
discovered  by  its  author  in  Ecuador  growing  in  a  shme  flux  from 
one  of  the  Bromeliaceae.  He  obtained  it  in  pure  culture,  and 
studied  it  in  the  living  state.  Nine  years  later  it  was  found 
again  by  Juel  (1902  a)  in  Sweden,  where  it  occurred  in  a  similar 
exudation  from  a  wounded  birch.  Apparently  only  these  two 
widely  isolated  collections  have  been  made.  Subcultures  from 
Juel's  material  were  widely  distributed,  and  the  fungus  was 
studied  in  many  institutions.  The  writer  carried  it  in  culture 
through  many  transfers  over  a  period  of  years,  but  it  has  now 
died  out,  and  is  apparently  no  longer  available  in  culture  else- 
where. Probably  it  is  not  uncommon  in  nature,  but  if  reisolated 
it  should  again  be  made  widely  available. 

The  fungus  forms  a  white  mat  of  profusely  branching,  septate 
hyphae,  composed  of  multinucleate  cells.  At  the  tips  of  some 
branches  oval,  unicellular,  multinucleate,  hyaline  oidia  are 
formed.  A  definite  sexual  process  occurs,  numerous  gametangia 
being  formed  over  the  mycelium.  The  gametangia  arise  in 
pairs  as  short  lateral  outgrowths  from  adjacent  cells  of  the  same 
hypha,  or  are  cut  off  as  terminal  cells  on  different  hyphae.     In 


308  THE  LOWER  FUNGI— PHYCOMYCETES 

either  case  they  are  multinucleate  from  the  first  and  are  morpho- 
logically indistinguishable.  They  come  in  contact  near  their 
tips  and  fuse,  a  wide  opening  resulting.  The  female  cell  (ascogo- 
nium)  then  pushes  out  at  its  apex,  and  elongates  to  form  a  long 
fiexuous  tube  which  tapers  to  a  slender  termination.  The  male 
cell  (antheridium)  does  not  increase  in  size,  but  retains  its 
identity,  so  that  the  elongated  ascogonium  seems  at  maturity 
to  have  a  forked  base.  The  nuclei  of  the  antheridium  mingle 
with  those  of  the  ascogonium,  and  one  of  the  male  nuclei  fuses 
with  one  of  the  female  to  form  a  single  large  fusion  nucleus. 
This  fusion  is  figured  by  both  Juel  (1902  a;  1921)  and  Dangeard 
(1907).  Following  fusion,  repeated  nuclear  divison  results  finally 
in  a  large  number  of  small  nuclei.  These  are  distinguished  with 
difficulty  from  the  supernumerary  sexual  nuclei.  The  latter 
tend  to  sink  toward  the  bottom  of  the  cell,  while  the  progeny 
of  the  fusion  nucleus  retain  their  position  in  its  upper  end  and 
become  the  centers  of  uninucleate  spores.  The  spores  are  accom- 
panied by  intersporal  substance,  and  are  said  by  Juel  to  be  cut 
out  as  in  higher  Ascomycetes  by  free  cell  formation.  They  are 
termed  ascospores,  and  the  elongated  ascogonium  which  bears 
them  is  then  called  the  ascus.  It  ruptures  apically  at  maturity 
and  the  spores  are  extruded  in  a  mass  through  a  definite  pore. 
They  are  globose  to  ellipsoidal,  hyaUne,  and  smooth. 

The  inclusion  of  Dipodascus  in  the  Ascomycetes  seems  to  be 
completely  justified  by  Juel's  observations  on  stained  material. 
Though  the  ascogonium  and  ascus  here  are  essentially  the 
same  structure,  and  though  ascogenous  hyphae  and  ascus  hooks, 
common  in  higher  Ascomycetes,  are  lacking,  two  features 
typical  of  the  ascus  of  the  Euascomycetes  are  present.  There  is 
a  fusion  of  a  single  pair  of  sexual  nuclei,  and  the  spores  are  thought 
to  be  delimited  by  the  astral  rays.  The  multispored  character 
of  the  ascus  emphasized  by  Schroter  is  of  little  significance, 
since  this  condition  exists  in  various  higher  forms  also.  In  an 
interesting  discussion  of  the  phjdogeny  of  the  Ascomycetes 
Atkinson  (1915)  presents  arguments  supporting  the  hypothesis 
that  that  group  arose  from  phycomycetous  ancestors  through 
forms  such  as  Dipodascus.  From  this  point  of  view  D.  alhidus  is 
the  most  primitive  of  all  the  known  Ascomycetes,  and  may  be 
regarded  as  perhaps  showing  relationship  with  species  of  the 
genus  Endogone  which  is  placed  by  various  authors  in  the  Muco- 
rales  (p.  265).     The  complete  life  cycle  in  the  last  named  genus  is 


PHYCOMYCETOUS  AFFINITIES  309 

unfortunately  not  yet  known.  In  the  Ascomycetes  genera  such 
as  Eremascus,  Endomyces,  and  Zijgosaccharomyces  afford  forms 
intermediate  in  type  between  Dipodascus  and  the  Euascomycetes. 
In  these  genera  also,  the  cell  formed  by  the  fusing  gametangia 
functions  as  the  ascus,  but  the  ascospores  are  of  small  and 
definite  number.  In  the  multinucleate  character  of  its  gametangia 
Dipodascus  stands  alone  among  these  lower  forms.  Its  nearest 
known  relative  is  perhaps  Endomyces  magnusii  of  the  Endomycet- 
aceae.  In  that  species  the  ascus  results  from  the  fusion  of 
uninucleate  cells  and  only  four  ascospores  are  formed,  but  the 
cells  of  the  mycehum  and  the  oidia  are  multinucleate.  In  the 
other  species  of  Endomijces  all  the  cells  are  uninucleate.  In  some 
higher  forms  (e.g.,  Sphaerotheca)  the  mature  ascogonium  is 
septate  and  one  of  its  cells  becomes  the  ascus. 

Though  Dipodascus  is  clearly  ascomycetous,  the  three  other 
genera,  Ascoidea,  Conidiascus,  and  Oscarhrefeldia,  included 
with  it  in  the  Ascoideaceae  by  Schroter  and  Lindau,  are  of  doubt- 
ful affinity. 

In  Ascoidea  the  mycelium  is  abundantly  septate,  repeatedly 
branched,  and  saprophytic,  and  a  spore  sac  containing  many 
spores  as  in  Dipodascus  is  formed.  The  genus  has  been  inade- 
quately investigated,  and  accounts  based  on  cytological  studies 
are  contradictory  (Popta,  1899;Lohwag,  1926;  Varitchak,  1928; 
Walker,  1929).  Apparently  a  fusion  of  sexual  nuclei  does  not 
occur,  and  the  spores  seem  not  to  be  delimited  by  the  astral 
rays.  The  spore  sac  is  ovate  to  clavate-cylindrical,  is  formed 
terminally,  and  dehisces  by  an  apical  pore.  After  the  escape 
of  the  spores  it  proliferates  repeatedly  as  does  the  sporangium 
in  Saprolegnia.  In  the  light  of  present  knowledge  there  seems 
to  be  Httle  justification  for  regarding  this  sac  as  an  ascus.  How- 
ever, in  a  discussion  of  the  origin  of  the  Ascomycetes  Atkinson 
(1915)  takes  the  position  that  Ascoidea  may  be  related  to  Dipo- 
dascus, and  that  the  spore  sac  may  be  merely  the  result  of  the 
apogamous  development  of  one  gametangium  in  the  absence 
of  the  other.  Perhaps  from  that  point  of  view  the  term  ascus 
could  be  logically  applied.  Under  certain  conditions  cells 
morphologically  equivalent  to  the  spore  sacs  function  as  conidia, 
falling  off  and  germinating  by  germ  tube.  The  first  conidium 
formed  is  terminal  on  the  hypha,  but  further  apical  growth  of 
the  hypha  pushes  it  aside  and  causes  it  to  have  a  lateral  position. 
Successive    formation    of    conidia  in  this  fashion  results  in  a 


310 


THE  LOWER  FUNGI— PHYCOMYCETES 


terminal  cluster.  The  spore  sac  and  the  conidium  are  clearly- 
one  fundamental  structure  undergoing  two  types  of  germination. 
Even  in  proliferation  a  conidium  may  form  within  the  old  sac 
after  the  escape  of  the  spores. 

The  genus  was  founded  on  a  single  species,  A.  ruhescens 
Brefeld  (1891)  isolated  from  a  slime  flux  of  beech  in  Germany. 
A  single  other  species,  A.  saprolegnoides  Holtermann  (1898)  was 
described  from  Java  where  it  was  found  forming  a  brownish 
encrusting  mat  on  various  trees.     In  the  first  species  the  spores 


Fig.  110.- — Ascoidea  ruhtticens  Brofeld.  (n,  l>,  d)  Spore-sacs  proliferating:. 
Spores  freed  in  an  oily  matrix,  (c)  Hat-shaped  spores.  (From  unpublished 
drawings  by  Leva  B.  Walker). 


are  hat-shaped  and  lie  in  the  sac  with  the  flattened  sides  together. 
They  are  extruded  in  a  long  coiling  thread-like  mass.  The 
second  species  as  described  differs  chiefly  in  having  globose  to 
oval  spores,  not  in  pairs,  which  when  extruded  do  not  form  a 
thread.  In  A.  ruhescens  the  empty  walls  of  several  spore  sacs 
commonly  are  found  nesting  one  within  the  other.  In  A.  sap- 
rolegnoides,  elongation  of  the  thread  is  said  to  result  usually 
in  the  formation  of  each  successive  sac  beyond  the  limits  of  its 
predecessor.  In  spite  of  these  described  differences  it  is  possible 
that  the  two  species  are  the  same.  The  hat-shape  of  the  spore 
is  not  always  observed  with  ease  in  ^.  ruhescens,  and  may  actually 
occur  in  Holtermann 's  species. 


PH YCOM  YCETO  US  A FFINI TIES  3 1 1 

The  genus  Oscarbrefeldia  is  monotypic,  having  been  based  on 
0.  pelliicida  Holtcrmann  (1898),  isolated  in  Java  from  a  slime 
flux  of  trees.  The  mycelium  is  septate  and  bears  ellipsoidal 
conidia  similar  to  those  of  Ascoidea.  Frequently  also,  cells 
indistinguishable  from  the  conidia  in  shape  and  position  form 
definite  oval  endogenous  spores.  Though  Holtermann  states 
that  the  spore  number  varies  from  one  to  seventy,  his  figures 
show  it  to  be  frequently  eight.  The  spore  sacs  are  sometimes 
formed  in  chains.  Proliferation  does  not  occur.  As  figured 
the  spores  are  seen  surrounded  by  epiplasm,  but  stained  prepa- 
rations were  not  made,  and  no  evidence  that  nuclear  fusion 
or  free-cell  formation  occurs  in  these  cells  is  provided.  The 
author's  figures  and  statements  are  confusing  and  unconvincing, 


Fig.  111. — Pericystis  alvei  Betts.      (a)   Copulation  of  gametangia  to  form  a  sac. 
(6)  Mature  sac  containing  spores.      {After  Claussen  1921). 

and  we  are  left  in  doubt  as  to  the  real  nature  of  the  form  studied. 
No  adequate  proof  of  its  relationship  with  Dipodascus  or  Ascoidea 
is  given.     The  genus  is  at  best  of  doubtful  position. 

The  genus  Conidiascus  is  of  similar  status.  It  also  is  mono- 
typic, having  been  based  on  C.  paradoxus  Holtermann  (1898:  23), 
found  in  Java  in  a  slimy  exudation  from  Ficus.  The  mycelium 
forms  a  mat  of  septate,  branching  hyphae  at  whose  tips  oval 
conidia  cluster  as  in  Ascoidea.  In  cultures  of  distilled  water 
the  contents  of  a  few  conidia  were  observed  to  round  up  to  form 
three  to  five  globose  spore-like  bodies.  In  such  cases  the  terms 
sporangium  and  ascus  are  used  indiscriminately  by  Holtermann. 
He  figures  the  escape  of  the  spores  through  a  simple  pore  at  the 
end  of  the  cell.  No  evidence  of  nuclear  fusion  or  free-cell 
formation  is  given.     Though  the  species  may  yet  be  shown  to 


312 


THE  LOWER  FUNGI— PHYCOMYCETES 


be  related  to  Endomyces  its  ascomycetous  character  is  still  in 
doubt. 

In  recent  years  another  genus  has  been  described  which 
seems  to  fall  near  Dipodascus.  It  has  been  studied  by  Betts 
(1912)  and  Claussen  (1921)  and  bears  the  name  Pericystis  Betts. 
It  is  based  on  a  single  species  P.  alvei  Betts  occurring  in  hives 
of  bees,  where  it  causes  a  well  known  trouble  termed  chalk  brood. 
The  fungus  is  heterothallic,  and  a  multispored  globose  sac  is 
formed  by  the  copulation  of  a  pair  of  gametangia  much  as  in 
Dipodascus.  The  nuclear  history  is  not  known,  but  in  general 
aspect  the  fungus  seems  to  be  intermediate  in  type  between 
Dipodascus,  Endogone,  and  Eremascus  (Eidam,  1883).  Its  cyto- 
logical  study  should  prove  very  interesting. 


Fig.  112.- — Dipodasctis  albidus  Lagerheim.  (a)  Young  progametangia.  (b) 
Fusion  of  gametangia.  (c)  Female  gametangium  showing  fusion  nucleus. 
(d)  Young  ascus.  (e)  Mature  ascus  containing  spores,  (6,  after  Lagerheim; 
c,  after  Juel;  others  from  material.) 

All  the  members  of  the  Hemiascomycetes,  as  that  group  was 
conceived  by  Schroter,  have  now  been  discussed.  The  ascomyce- 
tous character  of  several  of  these  is  much  in  doubt,  but  until 
further  investigation  is  carried  on  none  of  them  may  be  placed 
with  complete  assurance  in  the  Phycomycetes.  Only  a  few  may 
be  regarded  as  constituting  connecting  forms  between  the  two 
groups.     Of  these  Dipodascus  albidus  is  the  most  unquestioned. 

Recently  Gaumann  (1926)  has  presented  a  scheme  of  classi- 
fication in  which  the  Ascomycetes  are  split  into  the  two  major 
subdivisions  Hemiascomycetes  and  Euascomycetes.  In  his 
grouping  the  Hemiascomycetes  include  two  orders,  the  Endomy- 
cetales,  embracing  the  Dipodascaceae,  Endomycetaceae,  and 
Saccharomycetaceae,  and  the  Exoascales,  incorporating  the 
Protomycetaceae    and    the    Exoascaceae.     Immediately    above 


PHYCOMYCETOUS  AFFINITIES  313 

these  in  his  scheme  lie  the  Gymnoascaceae  and  other  similar 
forms  of  the  Euascomycetes. 

In  another  recent  classification,  that  of  Gwynne-Vaughan 
(1922),  the  Ascomycetes  are  subdivided  into  Plectomycetes, 
Discomycetes,  and  Pyrenomycetes.  The  first  named  group 
includes  the  Plectascales,  Erysiphales,  and  Exoascales.  The 
Plectascales  are  in  turn  subdivided  into  Endomycetaceae  (includ- 
ing Dipodascus),  Saccharomycetaceae,  Gymnoascaceae,  and 
Aspergillaceae. 

The  general  naiure  of  those  separations  indicates  clearly  the 
trend  of  modern  thought  with  respect  to  the  interrelationships  of 
the  Ascomycetes.  It  should  be  remembered,  however,  that  not 
all  authorities  regard  the  simple  forms  as  primitive.  Some  read 
the  evidence  in  reverse  order,  and  derive  the  simple  forms  through 
degeneration  from  the  more  complex.  The  student  interested  in 
studying  the  possible  relationships  between  the  Phycomycetes 
and  Ascomycetes  must  in  any  case  focus  his  attention  on  these 
forms  with  apparently  intermediate  types  of  morphology. 

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Unger,  F.,  Die  Exantheme  der  Pflanzen.     p.  341,  Wien,  1833. 

Varitchak,  B.,  L'evolution  nuclcaire  chez  Ascoidea  rubescens  Brefeld. 
Comp.  Rend.  Acad.  Sd.  Paris,  186:  96-98,  1928. 

Walker,  Leva  B.,  Some  observations  on  Ascoidea  rubescens.  Unpubl, 
paper  read  before  Botanical  Society  of  America,  Des  Moines,  Iowa, 
Dec.  30,  1929. 


INDEX 


Generic  and  specific  names  are  shown  in  italicx.^   Boldface  numerals  indicate 
pages  bearing  illustrations 


Aboospore,  36,  155 
Absidia,  243,  244 

caernlea,  237 

glauca,  244 

spinosa,  237,  239 
Acerviili,  16 
Achyla,  149,  150,  157,  167,  168 

bisexualis,  153 

colorata,  155 

paradoxa,  167 

polyandra,  155 
Achlyella,  89,  94 

flahaultii,  94 
Achlyogeton,  118,  119 

entophytum,  119 

rostralum,  119 
Achlyoid,  164 
Ackermannia,  266 
Acrasieae,  2,  5,  9,  11 
Acrasis,  11 
Actinocephalum,  263 

japonicum,  264 
Adinomucor,  257 
Adelphotaxy,  149 
Aethalium,  8 

Aggregation  plasmodium,  10 
Akarycyte,  51 
Albuginaceae,  186 
AZfow^o,  188,  192 

bliti,  188,  192 

Candida,  188,  192 

ipomoeae-panduranae,  188,  192 

lepigoni,  191 
minor,  192 
portulacae,  188,  192 
tragopogniri.s,  188,  192 


Algae,  2 

blue-green,  2,  3 

brown,  2 

fission,  2,  3 

green,  2 

red,  2,  21 
Algal  fungi,  21 
Allomyces,  133,  135,  209 

arbuscula,  134,  136 

javanicus,  29,  132,  136 
Alternation  of  generations,  17 
Amoebochytrium,  100,  101 

rhizidioides,  101 
Amoeboid,  6 

gametes,  44 

zygote,  29 
Amphigynous,  203 
Ancylistaceae,  118,  128 
Ancylistales,  39,  117 
Ancylistes,  119,  124 

closterii,  124,  125 

pfeifferi,  125 
Androgynous,  153 
Anisogamic,  29 
Anisomyxa,  52,  63 

plautaginis,  63 
Antheridial  branch,  152 
Antheridium,  29,  186,  308 

pierced  by  oogonium,  203 
Antherozoids,  30,  138 
Apaudrous,  37,  147 
Aphanomyces,  149,  150,  158,  167 

euteiches,  169 

laevis,  155,  167 

parasiticus,  170 
phycophilus,  169 

raphani,  169 
stellatus,  169 
317 


318 


THE  LOWER  FUNGI— PHYCOMYCETES 


Aphanomycopsis,  170 

bacillariacearum,  170 
Aphragmium,  196 
Aplanes,  149,  150,  156,  158 

androgynus,  158,  159 

ircleaseanus,  158,  159 

iurfosus,  158 
Aplanetism,  150 
Aplaiiospores,  15,  24 
Apodachlya,  172,  173 

completa,  175 

pyrijera,  175 
Apodya,  173 
Apogamous,  147 
Apophysis,  220 
Apothecium,  16,  302 
Araiospora,  172,  177 

coronata,  177 

pidchra,  177,  178 

sjnnosa,  177 
Archicarp,  303 
Archimycetes,  38 
Ascocarp,  16,  302 
Ascocorticiaceae,  303 
Ascogonium,  308 
Ascoidea,  307,  309 

ruhesceiis,  310 

saprolegnoides,  310 
Ascoideaceae,  307 
Ascomycetes,  2,  16 

conidium  in,  16 

essential  features  of,  16,  301 
Ascospores,  16,  301 
Ascus,  16,  301 

hooks,  17 
Asexual  reproduction,  14,  24 
Aspergillaceae,  303,  313 
Astral  rays,  ascosporc 

delimitation  by,  16,  302 
Asterocystis,  72 
Asterophlydis,  89,  94 

sarcoptoides,  94 
Azygospores,  36,  155,  234,  282,  296 


B 


Bacillus  radicicola,  49 
Bacteria,  2,  3,  4 
Badridium  radicicola,  49 


Basidiobolaceae,  282 
Basidioboleae,  282 
Basidiobolus,  283 

lacertae,  283 

myxophilus,  283,  286 

ranarum,  283,  284 
Basidiomycetes,  2,  17 

conidium  in,  16 
Basidiophora,  208,  211,  214 

entospora,  214,  215 

kellermanii,  215 
Basidiospore,  17 
Basidium,  17 

in  Entomophthoraceae,  285 
Basipetal  succession,  131,  148,  187 
Bean-shaped  spores,  149 
Bicricium,  120 
Biochemical      differences      between 

strains,  240 
Biometrical  methods,  204 
Blakeslea,  259 

trispora,  259,  260 
Blastocladia,  134,  136,  209 

pringsheimii,  135 

strangulata,  136 
Blastocladiaceae,  133,  171,  172  180 
Blastocladiales,  40,  130 
Blepharospora,  208 

cambivora,  208 

terrestris,  208 
Botrytis  jonesii,  257 
Branching,  circinate,  244 

cymose,  151 

dichotomous,  135,  221,  256 

monopodial,  215 

sj'mpodial,  135 

umbellate,  177 

verticillate,  256 
Bremia,  212,  219 

lactucae,  219,  220 
Bremiella,  212,  220 
Brevilegnia,  149,  157,  162,  164 

bispora,  164 

diclina,  164 

linearis,  164 

subclavata,  164 

unisperma,  164 

unisperma  var.  delica,  164 

unisperma  var.  litoralis,  164 


INDEX 


319 


Brevilegnia,  unisperma  var.  montana, 

164 
Budding,  292 
Bulbils,  304 
Bulbothamnidium,  256 


Cactorum  group,  in  Phytophthora,  203 
Calcium  oxalate,  244 
Calyptralegnia,  149,  157,  161,  162 

achlyoides,  162 
Calyptromyces,  251 
Capillitium    of    Myxomycetes    and 

Gastromj'cetes  contrasted,  9 
Carbohydrates,  synthesis  of  by  green 

plants,  2 
Catcnaria,  101,  107 

anguillulae,  101,  103 

pygmaca,  101 
Cell  wall,  composition  of  in  fungi,  24 
134,  147 

non-cellulose,  134 

true  cellulose,  13,  147 
CeUuUn,  130,  171,  208 
Cellulose,  fungus,  composition  of,  13 

occurrence  of  true,  13,  147 
Central  body,  190 
Centric  oosphere,  153 
Cephalosporium,  268 
Ceratiomyxa,  2,  6,  8 
Chaetocladiaceae,  242,  257 
Chaetocladium,  257 

brefeldii,  257,  258 

Jresenianum,  257 

jonesii,  257,  258 
Chaetostylum,  256 
Chitin,  13 
Chlamydomonas,  13 
Chlamydomucor,  251 
Chlamydospores,  27 

in  Blastocladia,  132 

in  Entomophthorales,  282,  292 

in  Mucorales,  234 

in  Phytophthora,  202 

in  Protomycetaceae,  304 

in  Saprolegnia,  151 
Chlorophyceae,  2,  5 
Chlorophyll,  2,  21 
Chlorospora,  222 


Chlorospora,  vastatrix,  222 
Choanephora  259,  261 

americana,  262 

conjuncta,  262 

cucurbitarum,  260,  261,  262 

cunninghamiana,  262 

dichotoma,  263 

infundibulifera,  262 

persicaria,  262 

simsoin,  262 
Choanephoraceae,  242,  258 
Chrysochytrium,  85 
Chrysophlyctis,  73,  82 

endobiotica,  73,  82 
Chytridiales,  39,  43,  47 
Chytridium,  90,  96 

oi^,  96 
Chytrids,  43 
CUium,  6,  24,  51 
Circindla,  242,  244 

umbellata,  244 
Cladochytriaceae,  48,  100 
Cladochytrium,  101,  102 

cornutum,  103 

irregulare,  103 

polystomum,  103 

tenue,  103 
Clamp  connections,  17 
Classification,    basis    of    in    Phyco- 

mycetes,  37 
Clathrosorus,  65 

caynpanulae,  65 
Cleavage     planes,     sporangiospores 

formed  by,  234 
Club  root,  57 
Coemansia,  272 
Coemansiella,  272 
Coenocentrum,  154,  190,  241 
Coenocytic,  23 
Coenogametangium,  128 
Coenogamete,  23,  31,  142,  234 
Coenonia,  11 
Coenozygote,  235 
Columella,  234 
Companion  cell,  34,  66 
Completoria,  283,  288 

complens,  288,  289 
Compound  oosphere,  31,  191 
Conidiascus  paradoxus,  307,  311 


320 


THE  LOWER  FUNGI— PHYCOMYCETES 


Conidiobolus,  283,  286 

mitior,  286 

utriculosis,  286 

villosus,  287 
Conidiophore,  16,  26 
Conidium,  152,  185 

forcible  discharge  of,  281 

homologj^  of  with  sporangium,  20 

in  Ascomycetes,  16 

in  Blastocladia,  131 

in  Mucorales,  235 

in  Peronosporales,  185 

term  restricted,  26 
Conjugation  tube,  33,  35,  46 
Constrictions,  in  hyphae,  130,  171 
Copulation,  anisogamic,  29 

gametangial,  28 

heterogametangic,  28,  29 

heterogamic,  29 

isogametangic,  28 

isogamic,  28 

planogamic,  27 

tube,  117 
Coremia,  16 
Crozier  formation,  17 
Cruciform  division,  50 
Cultural  characters,  in  Phytophthora, 

204 
Cunninghamella,  259,  263 

africana,  263 

albida,  264 

bertholletiae,  264 

blakesleeana,  264 

echinulata,  263 

elegans,  264 

mandshitrica,  262  264 

microspora,  264 
Cunning hamia,  261 

inJundibuUJcra,  262 
Cup  fungi,  16 
C.yanophyccae,  2,  3,  5 
Cymose  branching,  151 
Cystidia,  294 
Cystopus,  188,  192 

(See  also  Albugo.) 
Cystospora,  66 

batata,  66 
Cystospore,  45,  149 
Cytoplasm,  cleavage  of,  302 


D 


Dangeardia,  90,  96 

mamillata,  96 
Delacroixia,  288 

coronata,  288 
Diblepharis,  140 
Dichotomous,  135 
Diclinous,  153 
Dicranophora,  253 

fulva,  237,  239,  254,  255 
Dictydiaethalium,  7 
Dictyosteliaceae,  11 
Dictyostelium,  11 
Dictyuchus,  149,  150,  157,  162,  163 

achlyoides,  162 

magnusii,  162 

monosporus,  153,  162 

polysporiis,  162 

sterile,  162 
Didymium,  7 

Dimargaris  cristalligena,  272 
Dimorphism,  of  spores,  255 
Dioecious,  153 
Diplanetic,  150 
Diplanetism,  150 
Diplophlyctis,  90,  98 

intestina,  98 
Diplophrys,  11 
Diplophysa,  67,  74,  76 
Dipodascaceae,  312 
Dipodascus  albidus,  307,  308,  312 
Discomycetes,  16 
Dispira,  270 

americana,  271 

circinata,  271 

cornuta,  271 
Dissophora  decumbens,  265,  268,  269 
Downy  mildews,  211 
Drepanconis,  222 

brasiliensis,  222 

E 

Eccentric  oosphere,  153 
Ectrogella,  71,  77 

bacillariacearum,  77 

pcrforans,  78 
Elaioplasts,  241 


INDEX 


321 


Emission  collar,  199 
Empusa,  283,  292,  293,  295 

rmiscae,  296 
Empusaceae,  297 
Empusales,  297 
Encystinent  of  spores,  140 
Endobiotic,  44 
Endogenously,  17 
Endogonaceae,  3S 
Endognne,  265,  267,  308 
Endogoneae,  265 
Endogonclla,  266 
Endomyces,  309 

niagnusii,  309 
Endomycetaceae,  302.  312 
Endophytic,  34,  44 
Endospore,  80,  304 
Endosporeae,  2 
Endozoic,  44 
Entomogenous,  296 
Entomophlhora,  292 

delphiniaiia,  296 

sdarae,  296 
Entomophthoraceae,  282,  283 
Entomophthorales,  41,  281 
Entomophthoreae,  282 
Entophlydis,  90,  98 

bulligera,  97 

confervae-gkmieratae,  97 

heliomorpha,  98 
Epibiotic,  44 
Epiphytic,  44 
Epiplasm,  16,  302 
Epi'spore,  markings,  188 
Epizoic,  44 
Eremascus,  309 
Erysibe  subterranea,  64 
Erysiphaceae,  211 
Erysiphales,  313 
Euascomycetes,  302,  312 
Eucarpic,  24 
Eumj'cetes,  2,  15 
Euolpidiopsis,  67 
Eusynchytrium,  80 
Euthallophyta,  2 
Euthamjiidium,  256 
Exit  papilla,  68,  131 
Exit  tube,  35,  44 
Exoascaceae,  302,  312 


Exoascales.  312,  313 
Exnascus,  307 
Exogenously,  17 
Exospore,  304 
Exosporeae,  2,  8 
Extramatrical,  44 

Extrasporangial    partial    sporangia, 
272 


Facultative  parasitism,  186 
Family  names,  endings  of,  39 
Fertilization,  30,  190 

tube,  31,  153 
Fingers  and  toes,  57 
Fission,  3 
Fission  algae,  3 
Fission  fungi,  2,  3 
Flagella,  6 
Florideae,  21 
Form  genus,  15 
Free-cell   formation,   in   ascus,   235, 

302 
Fruit  body,  14 

in  Ascomycetes,  302 

in  Endogoneae,  266 
Fulminaria,  96 
Fungi,  2,  12 

algal,  21 

characterization  of,  12 

classification  of,  14 

fission,  2  3 

higher,  15 

lower,  2 

origin  of,  22,  47,  301 
Fungi  Imperfecti,  2,  14 
Fungus  cellulose,  13 
Fusiform,  11 
Fusion  nucleus,  302 

G 

Gametangia,  28,  234,  235 
Gametes,  23,  27,  29,  45,  142 

in  Allomyces,  29 

in  Myxomycetes,  7 
Gametophytic,  37 
Gastromycetes,  17 

capillitium  of,  9 
Gemmae,  27,  152,  199 


322 


THE  LOWER  FUNGI— PHYCOMYCETES 


Geolegnia,  149,  157,  164 

inflata,  164 

septisporangia,  164 
Germ  sporangium,  234,  237 
Germ  tube,  13 
Glaziella,  266 
Glomerula,  251 
Glo77iits,  265 
Glycogen,  13 
Gonapodya,  133,  134,  139,  171 

polymorpha,  133,  134 

siliquaeformis,  133,  134 
Gonatahotrys  microspora,  264 
Gonoplasm,  32 
Giittulina,  11 
Guttulinaceae,  11 
Guttidinopsis,  11 
Gymnoascaceae,  313 

H 

Haplosporangium,  265,  268 

bisporale,  268,  269 

decipiens,  269 
Harpochytrium,  90,  96 

hedenii,  95 
Harposporium  anguillulae,  110 
Haustoria,  185 
Helicosporangium,  303 
Helicostylum,  256 

elegans,  256 
Hemiascomycetes,  303,  312 
Herpodadiella,  268 
Herpocladium,  265,  268 

circinans,  268 
Heterogametangic,  28,  29,  239 
Heterogamic  copulation,  29 

of  planogametes,  132 
Heterothallic,  36,  153,  236,  259 
Heterothallism,  in  Ancylistales,  117 

in  Saprolegniales,  162 

in  Zoophagus,  199 
Higher  fungi,  15 
Hilum,  of  swarmspore,  24 
Holdfast,  45 
Holocarpic,  24 

Homothallic,  36,  117,  153,  237 
Homothallism,  162 

in  Ancylistales,  117 

in  Saprolegniaccae,  162 


Hyalopus,  268 

Hybridization,  imperfect  in  Muco- 

rales,  237 
Hydrogcra,  251 
Hydrophora,  246,  250 
Hymenium,  17 
Hymenomycetes,  17 
Hyphae,  13 

constricted,  171 
Hyphal  bodies,  281,  292 
Hyphochytriaceae,  46 
Hyphochyirium,  107 

infestans,  107,  108 
Hyphophagus,  107 
Hypothallus,  9 


Ichthijophones,  286 

intestinalis,  286 
Imperfect  stage,  defined,  14 
Infection  tube,  117 
Infestans    group,    of    Phjtophthora, 

202,  203 
Intercalary    cell,    simulation    of,    in 

Albugo,  187 
Intercellular,  185 
Intracellular,  186 
Intramatrical,  44 
Irish  Famine,  205 
Isoachlya,  150,  157,  167 

eccentrica,  167 

monilifera,  167 

paradoxa,  167 

toruloides,  167,  168 

unispora,  167 
Isogametangic,  28,  239 
Isogametes,  in  Olpidium,  75 

in  Synchytrium,  82 
Isogamic,  28 
Isogamy,  27,  239 


Jaraia,  171 
salicis,  171 


K 


Karj^ogamy,  51 


INDEX 


323 


Kawakamia,  207 

carica,  207 

cyperi,  207 
Kickxclla,  272 
Krankheitsherde,  57,  60 


Lahyrinthida,  11 
Labyrinthuleae,  2,  5,  11 
Lagena,  128 

radicicola,  128 
Lagenidiaceae,  128 
Lagenidiopsis,  126 

reducta,  126 
Lagenidium,  119,  122,  195 

americanum,  123,  124 

closterii,  124 

ellipticum,  124 

enecans,  124 

entophytum,  124 

gracile,  124 

intermedium,  124 

marcheliayiuyn,  124 

pygmaeum,  124 

rabenhorstii,  124 

syncytiorum,  124 
Lamia,  292 

Late  blight  of  potatoes,  205 
Lalrostium,  91 

comprirnens,  91 
Leaf  curl  fungi,  303 
Legume  tubercle  organism,  49 
Leptolegnia,  150,  151,  158,  170 

caudata,  170 

ecccntrica,  171 

subterranea,  171 
Leptomitaceae,  148,  171 
Lepiomitus,  172 

ZadcMs,  146,  173,  174 
Leucochytrium,  85 
Lichenes,  2,  4 
Lichens,  2,  4 

basidiomycetous,  5 

discomycetous,  5 

pyrenomycetous,  5 

thallus  in,  4 
Lichtheimia,  245 


Ligniera,  50,  61 
alismatis,  61 
bellidis,  61 
isoetes,  61 
menthae,  61 
pilorum,  61 
radically,  61 
verrucosa,  61 

Lobosa,  51 

Lower  fungi,  1 


M 


Macrochytrium,  109 

botryoides,  109 
Manocyst,  203 
Martensella,  272 
Massospora,  283,  289 

cicadina,  289,  290,  291 

cleoni,  292 

richteri,  292 

stariizii,  292 
Media,  synthetic,  146 
Mesochytrium,  80 
Metarrhizium  anisopliae,  297 
Microcysts,  6 

in  Acrasieae,  10 

in  Myxomycetes,  6 
Micromyces,  80,  87 

mesocarpi,  87 

petersenii,  87 

spirogyrae,  87 

zygogoni,  87 
Micromycopsis,  88 

cristata,  88 

fischerii,  88 
Mildews,  downy,  211 

powdery,  211 
Mindeniella,  173,  180 

spinospora,  180 
Mitochy  Iridium,  110 
Mitochytrium,  127 

ramosum,  127 
Mitosis,  in  Myxomycetes,  9 

in  Plasmodiophoraceae,  51 

simultaneous,  126 
Miyabella,  86 
MolUardia,  50,  60 
Monad  in  eae,  12 


324 


THE  LOWER  FUNGI— PHYCOMYCETES 


Monascaceae,  303 
Moniliform,  164 
Monasais,  303 
Monoblepharidaooae,  139 
Moiioblepharidali's,  40,  138 
Monoblepharis,  30,  138,  139,  142 

brachyandra,  142,  143 

fascicidata,  142,  144 

insignis,  142,  144 

macrandra,  140,  142 

ovigera,  142 

polymorpha,  142,  143 

regignens,  142 

sphaerica,  142,  143 
Monoblepharopsis,  142 

ovigera,  142 

regignens,  142 
M onochytrium  stevcnsianutn,  45,  75 
Monoecious,  153 
Monophagus,  43 
Monophyletic,  37 
Monoplanetic,  131,  150 
Monoplanetism,  150 
Morels,  16 
Mortierella,  264 

candelabrum^  266 

fusispora,  266 

nigrescens,  266 
Mortierellaceae,  242,  264 
iWwcor,  243,  250 

hiemalis,  239 

mucedo,  236,  237,  238 

zygospore  germination  in,  238 

zygospore  production  in,  236 
Mucoraceae,  241,  242 
Mucorales,  41,  234,  241 
Mycelium,  13,  43 

intercellular,  185 

intracellular,  186 
Mycetozoa,  2,  6 
Mycocladus,  243,  245 

verticellatus,  245 
Mycoplasm  hypothesis,  222 
Mycorrhiza,  209 
Myrioblepharis,  141 

paradoxa,  141 
Myxamoeba,  6,  52 
Myxobacteriaceae,  10 
Myxogastres,  2,  8 


Myxomycetes,  2,  5,  6 

amoeboid  movement,  6 

gametes,  7 

myxamoebae,  6 

nuclear  division,  9 

Plasmodium,  7 

swarmspores,  6 
Myxothallophyta,  2,  5 
Myzocytium,  118,  120 

irregular  e,  122 

megastomum,  122 

proliferum,  120,  121 

vermicolum,  119,  121,  122 

N 

Naegelia,  175 
Naegeliella,  175 
Nematosporangium,  196 
Net  Plasmodium,  11 
Nowakoivskia,  91,  99 

hormothecae,  99 
Nowakowskiella,  100,  101 

eiegans,  101,  102 

ramosa,  101 
Nozemia,  203 
Nuclear  division,  9 

simultaneous,  126 
Nuclear  fusion,  51 

O 

Obeluiium,  88,  92 

mucronatum,  92 
Obligate  parasitism,  186 
Ocellus,  252 
Oedocephalum,  263 

albidum,  264 

echinidatum,  263 
Oidia,  16,  234,  285 
Oil,  storage  of  in  fungi,  13 
Olpidiaceae,  48,  71 
Olpidiaster,  71,  72 

radicis,  73 
Olpidium,  67,  71,  73 

brassicae,  73,  74 

endogonum,  73 

entnphytum,  73 

oedogoniarum,  73 


INDEX 


325 


Olpidium,  pendulum,  73 

uredinis,  73 

viciae,  45,  75 

zijgneviicolum,  73 
Oljridiopsis,  66,  67,  73 

aphanomycis,  67 

luxurians,  67 

minor,  67 

saprolegniac,  67 

vexans,  67,  68 
Oi7MdiM?n-like  thalli,  63,  120 
Ooch>'triaceae,  105 
Oogonial  branch,  152 
Oogonium,  29,  186 

basal  type  of,  203 
Ooraycetes,  characterized,  32,  40 
Oomycetous,  32 
Ooplasm,  31 
Oosphere,  30,  153,  186 

compound,  31,  191 
Oosporangium,  44 
Oospore,  30,  32,  44,  153,  186 
Ordinal  names,  endings  of,  39 
Oscarbrefeldia  pcllucida,  307,  311 
Ostenfeldiella,  66 

diplantherar,  66 


Papidaspora,  303 
Paragynous,  203 
Paraphyses,  294 
Parasitella,  251 
Parasites,  2 

facultative,  186 

obligate,  186,  281 
Parthenogenesis,  36,  123,  147,  154 
Parthenospores,  131 
Pedicel  cell,  207 
Perfect  stage,  defined,  14 
Perforated  septa,  135 
Pericystis  alvei,  311,  312 
Peridium,  in  Myxomycetes,  9 
Periplasm,  in  antheridium,  32 

in  oogonium,  31,  186 
Perithecium,  16,  302 
Peronoplasviopara,  211,  218 

canabina,  219 

celtidis,  218 


Peronopla^^mopara,  cubensis,  218 

humidi,  219 

portoricensis,  219 
Peronospora,  212,  221 

cadorum,  206 

celtidis,  218 

cubensis,  218 

cffusa,  221 

fagi,  206 

parasitica,  222 

sempervivum,  206 

spinaciae,  221 
Peronosporaceae,  186,  210,  211 
Peronosporales,  40,  185 
Phaeophyceae,  2 
Phlyctidium,  90,  98 

brevipes,  97,  98 
Phlyctochytrium,  89,  94 

equate,  94 

planicorne,  94 
Phycocyanin,  3 
Phycomyccs,  243,  248 

blakesleeanus,  249 

microsporus,  249 

?»7e?i.s,  237,  238,  249 

pirottianus,  249 

spimdosus,  249 

splendens,  249 
Phycomycetes,  2,  15,  21 

origin  of,  21 
Phyllobium.,  13,  110 
Phylogeny,  37,  47,  54 
Physiological  research  on  Saproleg- 

niales,  146 
Physoderma,  101,  103 

butomi,  103 

heleocharidis,  106 

maculare,  103,  106 

menyanthis,  106 

vagans,  106 

zeae-maydis,  104,  106 
Pkysorhizophidium,  98 
Phytomyxa,  49 

leguminosarum,  49 

lupini,  49 
Phytomyxinae,  49 
Phytomyxini,  49 
PMjtophthorn,  194,  199 

agaves,  206 


326 


THE  LOWER  FUNGI— PHYCOMYCETES 


Phytophthora,  allii,  206 

arecae,  203,  206 

cactorum,  201,  203,  206 

cambivora,  208 

capstci,  206 

carica,  206 

cinnamomi,  206 

citri,  206 

citrophthorn,  207 

colocasiac,  206 

cryptogea,  203,  206 

erythroseptica,  201,  203,  206 

/a6er?:,  206 

/a^i,  206 

^d,  206 

gonapodioides,  209 

hibernalis,  207 

hydrophila,  207 

infestans,  201,  203,  205 

jatrophac,  207 

lepirotiiae,  207 

meadii,  206 

melongenae,  207 

mexicana,  207 

nicotianac,  207 

omnivora,  206 

paeoniae,  207 

palmivora,  200,  206 

parasitica,  203,  206,  207 

parasitica  var.  r/ici,  206 

phaseoH,  201,  203,  205,  216 

pint,  207 

richardiae,  207 

syringae,  207 

ierrestria,  206,  208 

thalictri,  207 

theohromae,  207 
Phytophthora  type,  201 
Phytophthoraceae,  203 
Phytophthorales,  203 
Pilaira,  251,  253 
Pilobolaceae,  241,  251 
Pilobolus,  251 

crystallinus,  252 
Piptocephalaceae,  242,  270 
Piptocephalis,  270,  272 
freseniana,  273 

microcephala,  272 

monospora,  272 


PireWa,  242,  243 

cirdnans,  243 
Pits,  in  oospore  wall,  152 
Planogamic  copulation,  27,  84 

in  Sy/ichytrium,  45 
Planozygote,  28 
Plasmodiocarp,  8 
Plasmodiophora,  49,  55 

aZni,  59 

brassicae,  55,  56,  57,  58 

californica,  59 

elaeagni,  59 

ficus-repentis,  59 

halophilae,  59 

humuli,  59 

orchidis,  59 

tabaci,  59 

i/ieae,  59 

vascularum,  59 

viiis,  59 
Plasmodiophoraceae,  48,  65 
Plasmodium,  7,  53 

aggregation,  10 

baby,  53 

pseudo-,  10 

net-,  11 
Plasmopara,  211,  215 

auslralis,  217 

geranii,  218 

halstedii,  218 

megasperma,  220 

mwea,  218 

obducens,  218 

pygniaea,  215,  218 

ribicola,  218 

viburni,  218 

viticola,  215,  216 
Plasmophagus,  71,  79 

oedogoniorum,  79 
Plectascales,  313 
Plectomycetes,  313 
Plectospira,  158,  167 

gemmijera,  167 

myriandra,  167 
Pleocystidium.,  76 
Pleolpidmm,  71,  78 

apodyae,  79 

araiosporae,  79 

blastocladiae,  79 


INDEX 


327 


Pleolpidium,  cuadus,  79 

monoblepharidis,  79 
Pleotrachelus,  71,  78 

fulgens,  78 
Plus  and  minus  strains,  237 
Podochytrium,  88,  92 

davatum,  92,  93 
Polymorphi.sm,  in  fungi,  14 
Polyphagus,  43 
Polijphagus,  46,  91,  100 

euglenae,  100 
Polyphyletic,  46 
PolyrUna,  107,  110 

multiforrnis,  109,  110 
Polysphondylium,  11 
Powdery  mildews,  211 
Powdery  scab,  64 
Presporangium,  199 
Primary  nucleus,  in  Synchytrium,  86 
Primary  sporangium,  151 
Proabsidia,  245 
Progametangia,  235 
Progametes,  235 
Proliferation  of  sporangia,  151 

in  Ascoiden,  309 

in  Gonapodya,  131 

in  Myrioblepharis,  141 

in  Pythiomorpha,  208 

in  Saprolegnia,  151 
Prosorus,  44,  80 
Prosporangium,  44,  199 
Protascaceae,  128 
Protascus,  127 

subuliformis,  127 
Protista,  6 
Protoachlya,  150,  158,  167 

paradoxa,  167 
Protoascomycetes,  267,  302 
Protomitosis,  50 
Protomyces,  304   ■ 

kriegerianus,  305 

niacrosporus,  305 

pachydermus,  305 

tuberum  solani,  64 
Protomycetaceae,  304,  312 
Protoinycopsis,  304 

leucanthemi,  306 
Protozoa,  6,  12 
Pseudoabsidia,  245 


Pseudolpidiopsis,  67,  71,  73 

appendiculala,  77 

elliptica,  77 

fibrillosa,  77 

parasitica,  77 

schenkiana,  76,  77 

zopfii,  77 
Pseudoljndium,  66,  67,  73 

aphanomycis,  67 

fusifortne,  67 

pythii,  67 

saprolegniae,  67 
Pseuduperonospora,  218 
Pseudophores,  238 
Pseudoplasmodiiun,  10 
Pseudoplasmopara,  215 

justiciae,  215 
Pseudosepta,  134,  135 
Pseudospore,  in  Acrasieae,  10 

in  Labyrinthuleae,  12 
Pycnidia,  16 
Pycnochytrium,  80 
Pyrenomycetes,  16 
Pyriform,  24 
Pyrrhosorus,  71 

marinus,  71 
Pythiaceae,  186,  193,  194 
Pythiacystis  citrophthnra,  207 
Pyihiogeton,  194 

ramosum,  194 

transversum,  194,  195 

idriforrne,  194 
Pythiomorpha  gonapodioides,  208 

undulatum,  209 
Pythiomorphaceae,  208 
Pythiopsis,  150,  157,  165 

cymosa,  165 

humphreyana,  165 

intermedia,  150,  165 
Pythium,  165,  194 

afertUe,  198 

aphanidermalum,  198,  199 

arrhenomanes,  198 

artotrogiis,  196 

biif^eri,  198 

cystosiphon,  196 

debaryanum,  196,  197,  199 

dictyospermum,  198 

entophytum,  195 


328 


THE  LOWER  FUNGI— PHYCOMYCETES 


Pythium  ferax,  196 

gracile,  195,  198 

graminicolum,  198 

indigoferae,  198 

intermedium,  196,  197 

irregular  e,  198 

viamillatum,  198 

megalacanthum,  196 

monospermum,  195,  198 

proliferum,  195 

tenue,  198 

torulosum,  198,  199 

vltimum,  199 

undulatum,  209 

vexans,  196 
Pythium  type,  201 

R 

Receptive  papilla,  189,  203 

Receptive  spot,  189 

Reesia,  75 

Relationships,  phylogenetic,  of  Phy- 

comycetes,  21 
Reniform,  24,  149 
Resticularia,  126 

boodlei,  126 

nodosa,  126,  127 
Resting  sporangium,  28,  44,  151 
Resting  spore,  28,  44 
Reticidaria,  7 
Rhabdium,  96 
Rheosporangium       aphanidermatmn, 

198 
Rhipidium,  173,  180 

americatium,  179,  180 

europaeum,  180 

parthenosporum,  180 

thaxteri,  180 
Rhizidiaceae,  48,  88 
Rhizidiocydis,  1 10 

ananasi,  110 
Rhizidiomyces,  89,  93 

apophysatus,  93 

ichneumon,  94 
Rhizidium,  90,  96 

lignicola,  96 

mycophilum,  94,  96 

operculalum,  96 


Rhizohium  leguminosarum,  49 
Rhizochlosmatium,  89,  94 

globosum,  94 
Rhizoids,  45,  130,  146,  245,  294 
Rhizomorphs,  17 
Rhizomyxa,  52,  62,  126 

hypogaea,  62 
Rhizophidium,  88,  91,  103 

brevipes,  98 

globosum,  91,  92 

pollonis,  91 
Rhizophidium-Vike    thalli,     in     P/i/y- 

soderma,  103 
Rhizophlydis,  90,  99 

mastigotrichis,  99 
Rhizopus,  243,  245 

nigricans,  237,  245,  246 
Rhizosiphon,  98 
Rhodochytrium,  13,  109 
Rhodophyceae,  2 
Rhopalomyces,  261 

cucurbitarum,  262 
Rhysotheca,  215 
Rozella,  67,  68 

septigena,  68,  69 

simidans,  68 
Rusts,  white,  187 


S 


Saccharomycetaceae,    13,   302,   312, 

313 
iSaccomyces,  90,  98 

dangeardii,  98 
Saitomyces,  372 
Sammelzellen,  104 
Sappinia,  11 
Sappiniaceae,  11 
Saprolegnia,  150,  151,  157,  166,  167 

dioica,  155 

hypogyna,  159 

monilifera,  167 

monoica,  155 

siliquaeformis,  138 

thureti,  155 
Saprolegniaceae,  147,  148,  156 
Saprolegnialcs,  40,  146,  147 
Sapromyces,  172,  175 

androgynous,  176,  177 


INDEX 


329 


Sapromyces  reinschii,  177 
Saprophytes,  2 
Schinzia  leguminosarum,  49 
Schizomycetes,  2,  3 
Schizophyceac,  2,  3 
Sclerocystis,  265 
Sclerospora,  211,  212 

graminicola,  212,  213 

macrospora,  213 

philippinensis,  213 

spontanea,  213 
Solerotia,  7 

Segments  of  thallus,  135,  171 
Segregation  of  sex,  36,  238 
Septocarpus  conjnephorns,  92 
Septocladia,  135 

dichotoma,  136 
Sex,  biochemical  studies  in,  240 

segregation  of,  36,  238 
Sexual  reproduction  in  lower  fungi, 

14,  27,  240 
Sigmoideomyces,  264 
Siphonaria,  90,  95 

variabilis,  95 
Slime  moulds,  2,  6 
SUme  thallophytes,  2,  5 
Soil  fungi,  130,  146 
Sommerstorffia,  170 

spinosa,  170 
Soral  membrane,  52,  84 
Sorodiscus,  55,  63 

callitrichis,  63 
Sorolpidium,  52,  63 

feeiae,  63 
Sorophoreae,  11 
Sorosphaera,  49,  55,  60 

graminis,  61 

isoetes,  62 

junci,  61 

radicalis,  62 

veronicae,  60 

verrucosa,  62 
Sorosporella  agrotidis,  297 
Sorus,  24,  43 
Spermatozoids,  30,  138 
Sperms,  30,  138 
Spliaerita,  71,  72 

endogena,  72 

trachelomonadis,  72 


Sphaerocreas,  265 
Sphaerosporangium,  196 
Spinalis,  272 
Spinellus,  243,  246 

fusiger,  237 

macrocarpus,  247 
Spongospora,  50,  55,  64 

scabies,  64 

solani,  64 

subterranea,  64 
Sporangia!  discliarge,  252 
Sporangiola,  27,  234,  254,  256 
Sporangioliferous  heads,  259 
Sporangiophore,  25,  185 
Sporangiospores,  15,  24,  285 

encystment  of,  149 

formation  of,  25,  302 

germination  of,  t'/t  si7;/,  150 

thick-walled,  164 
Sporangium,  8,  15,  24,  43 

extrasporangial-partial,  272 

germ,  234,  237 

moniliform,  164 

primary,  151 

proUfe ration  of,  141 

resting,  151 

simultaneous  development  of,  186 

summer,  43 

successive  development  of,  200 

swarm,  43 

thin-walled,  43 

violent  discharge  of,  252 
Spore,  in  fungi,  13 

in  Myxomycetes,  9 
Spore  balls,  61 
Spore     formation,      contrasted      in 

sporangium  and  ascus,  25 
Sporodinia,  108,  243,  247 

grandis,  237,  238,  248 
Sporodochium,  16 
Sporomyxa,  65 

scauri,  65 
Sporophlyctis,  91,  100 

rostrata,  100 
Sporophytic,  37 
Sterigmata,  17 

Stigeosporium   marattiacearum,  209 
Stolons,  244 
StyloHpores,  265,  270 


330 


THE  LOWER  FUNGI— PHYCOMYCETES 


Suboentric  oosphore,  153 
Sub-sporangial  vesicle,  285 
Summer  sporangia,  43 
Supernumerary  nuclei,  31,  154,  191 
Suspensors,  235 
Swarm  cells,  28 
Swarmsporangia,  25,  43 
Swarmspores,  15,  24 
Symbiosis,  4 
Sympodial,  135 
Synascus,  306 
Synccpluilastrum,  270,  273 

racemosum,  274 
Syncephalis,  270,  273 

reflexa,  274 

wynneae,  274 
Synchj'triaceae,  48,  80 
Synchytrium,  80 

aecidioides,  85 

anemones,  85 

anomalum,  85 

asari,  87 

aureum,  85 

caricis,  87 

cellulare,  84 

cinnamomeum,  85 

decijnens,  86 

eridobioHcum,  45,  82,  83 

fulgens,  82 

holwayi,  85 

innominatum,  87 

mercurialis,  85 

myosotidis,  85 

nigrescens,  87 

puerariae,  85 

scirpi,  87 

stellariae,  84 

succisiae,  84 

taraxaci,  81 

vaccina,  87 
Syngametic,  239 
Syngamy,  239 
Synthetic  media,  146 
Systemic  infection,   in  Phylophthora 

infestans,  205 
Syzgites,  247 


Taphridium,  306 
algcriense,  306 
rhaetica,  306 
tanbcllifcrarum,  306 
Taphrina,  307 
Tarichium,  292,  297 

uvella,  297 
Telebolus,  303 
Teirachytrium,  107 
triceps,  107,  108 
Tetramyxa,  49,  55,  59 
parasitica,  59 
triglochinis,  60 
Thallophyta,  1,  2 

subdivisions  of,  2 
Thallophytes,  1 
Thallus,  1,  23 
in  lichens,  4 
in  lower  fungi,  23 
Thamnidiaceae,  242,  253 
Thamnidium,  253,  256 
amoenum,  256 
elegans,  255,  256 
fresenii,  255,  256 
simplex,  255 
Thamnocephalis,  264 
Thelebolaceae,  303 
Thelebolus,  303 
stercoreus,  303 
zukalii,  303 
Theleobolus,  303 
Thin-walled  sporangia,  43 
Thin-walled  vesicle,  80 
Thraustotheca,  149,  150,  156,  160 
achly  aides,  161,  162 
clavata,  160,  161 
primoachlya,  160 
unisperma,  161 
unisperma,  var.  litoralis,  162 
Tieghemella,  245 
Trachysphacra,  194,  203,  209 

fructigena,  209,  210 
Truffles,  16 
Tubercinia  scabies,  64 
Turbinate  enlargements,   in  Physo- 
dcrma,  104 


INDEX 


331 


U 

rmbellate,  177 
Uro-phlycHs,  101,  107 

alfalfae,  104,  107 

kriegeriana,  106 

leproides,  106 

major,  107 

pluriannulatus,  104,  105,  107 

piilposa,  103,  107 

Verticillate  l^ranching,  256 
\'esicle,  subsporangial,  251,  285 

thin-walled,  199,  200 
\'irescence,  213 
Volkartia,  306 

W 

Water  moulds,  physiology  of,  146 
"White  rusts,"  187 
Woronina,  67,  69,  70 

glomerata,  70 

polycystis,  70 
Woroninaceae,  48,  66 
]Voroni?iella,  80,  85 

aecidioides,  86 

psophocarpi,  85 

vulcanica,  85 


X 


Xenomyces,  266 


Yeasts,  16,  302 


Zonation,  in  oogonium.  191 
Zoophagiis  insidians,  199 
Zoosporangium,  25 
Zoospores,  15,  24 

multiciliate,  141 

repeated  emergence  of,  150 
Zygochytrium,  108 

aurant'iacum,  lOS,  109 
Zygomycetes,  33,  41 
Zygomycetous,  33 
Zygophores,  248 
Zygorhizidium,  46,  89,  93 

willei,  93 
Zygorhynchus,  237,  243,  249 

bernaldi,  249 

dangeardi,  249 

heterogamus,  239,  249,  260 

japonicus,  249 

moelleri,  239,  249 

vuilleminii,  249 
Zygosporangium,  44 
Zygospores,  28,  33,  44,  234,  282,  294 

formation  of,  235,  236,  249 

germination  of,  237,  238 

imperfect,  237 
Zygote,  27,  100 

amoeboid,  29 

biciliate,  132 

in  Myxomycetes,  7 

piano-,  28 


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