Pantone, D.J.

Womersley, C.

Horizon / Pleins textes

The  distribution of flower galls 
caused by Anguina  amsinckiae on  the weed, 
common fiddleneck, Amsinckia intermedia 
Dan James PANTONE and Christopher WOMERSLEY 
Graduate  Group  in Ecology  and the Department of Plant  Pathology, University of California,  Davis, Ca 95616, 
and  Department of Zoology, University of Hawaii  ut  Manou, Honolulu, Hi  96822, USA. 
SUMMARY 
The distribution of  flower  galls  caused  by Anguina  amsinckiae (Steiner & Scott, 1934) Thorne, 1961 on  the  host  plant Amsinckia 
intermedia Fischer & Meyer  (Borraginaceae)  is  described.  Galls  were  exclusively  associated  with  floral  tissues,  and  were  restricted 
to the five  uppermost  inflorescences  of  the  host  plants.  Approximately 93 O’o of total  galls  were  located in  the two uppermost 
inflorescences.  Within  a  given  inflorescence,  galls  were  restiicted  to  the six basal  flowers  with  approximately 82 O/O of the  galls  being 
distributed  between  the  most  basal  flower  and  the  flower  directly  above  it.  This  gall  distribution  suggests  that  nematode  attack 
occurs  during  the  host’s  early  flowering  stages,  and  that  the  pattern  observed  may  be  a  function  of  moisture  availability  to the 
nematode  during  infection.  Plant growth regulators  are  suggested  as  a  possible  means of  enhancing  the  onset  and  degree  of  galling. 
RESUME 
La répartition  des  galles  florales causées par Anguina  amsinckiae sur la plante Amsinckia  intermedia 
La répartition des galles florales dues à Anguina a?nsinckiae (Steiner & Scott, 1934) Thorne, 1961 sur la plante Amsinckia 
intermedia Fischer & Meyer (Borraginacées) est décrite. Ces galles sont associées aux tissus floraux et restreintes aux cinq 
inflorescences les plus élevées. Environ 93 % des galles sont situées sur les deux inflorescences les plus élevées. Dans une 
inflorescence  donnée,  les  galles  sont  limitées  aux six fleurs  inférieures,  avec  environ 82 O/o des  galles  réparties  entre  la  fleur  la  plus 
basse  et  celle  située  immédiatement  au-dessus.  Une  telle  répartition  suppose  une  attaque du nématode en début  de  floraison. Le 
comportement  observé  pourrait  dépendre  de  l’humidité  disponible  pour  le  nématode au moment de l’infestation.  Les  régulateurs 
de croissance  de  la  plante  pourraient  également  agir  sur  l’infestation  et  le  nombre  de  galles. 
Common fiddleneck, Amsinckia intermedia Fischer & 
Meyer (Boraginaceae),  is a  winter annual weed that is 
widespread in small grains, alfalfa, orchards, pastures 
and  rangelands  in California (Pantone, Brown & Wo- 
mersley, 1985). Economic concem about its presence 
stems  from  the  fact  that  the w ed contains pyrrolizidine 
alkaloids which, if ingested, can cause hepatic unsuf- 
ficiency,  megalocytosis, and fibrosis in the livers of 
cattle, hogs, and  horses (Fowler,  1968). Given  the  cur- 
rent  regulations of herbicide use, there are few effective 
postemergent  herbicides registered in  California to 
control  common  fiddleneck  in alfalfa (Pantone, Brown 
& Womersley, 1985). Thus,  the  development of biocon- 
trol  methods have become of paramount  importance.  In 
accordance with this, Nagamine  and  Maggenti (1980) 
suggested the potential importance of the nematode 
Revue  Nématol., 9 (2) : 185-189  (1986) 
Anguina amsinckiae (Steiner & Scott, 1934) Thome, 
1961 as a biological weed control  agent,  but  no  research 
has been  done to assess the practicality of this proposal. 
Unlike some species of Anguina that are initially 
ectoparasitic  but  become  endoparasitic  on  entering  the 
developing inflorescence, Anguina amsinckiae is exclus- 
ively ectoparasitic  and  does  not directly penetrate  host 
tissues to initiate gall formation  (Godfrey, 1940). Nema- 
todes  feeding  on  the  immature  inflorescence  stimulates 
the  primordial  flower  parts (petals, sepals, carpels and 
stamens)  to  become  hyperplasic  and  surround  the  nema- 
todes  in  a gall (Godfrey, 1940). Feeding  continues  within 
the gall, and  reproduction  occurs  at  the expense of the 
plant’s own reproductive  organs. 
Our present  research is concerned with assessing the 
potential of Anguina amsinckiae as a  biocontrol  agent 
185 
D. J. Puntone & C. Womersley 
for  common  fiddleneck. An important  aspect of this is 
the  observation that gall distribution  within  the  inflor- 
escence of the  host  plant  is typically limited to  the basal 
flowers (Steiner & Scott, 1934), suggesting  that specific 
factors may operate to limit the  extent of gall formation. 
We  undertook the  present work to investigate  more  fully 
this unusual  distribution of nematode galls with a view 
to : i) gaining a deeper insight into host-parasitic re- 
lationships  between Angztina amsinckiae and common 
fiddleneck  and ii) enhancing  the  biocontrol  potential of 
the nematode. 
Fig. 1. Amsinckiu intemedia. Inflorescence  position  coded  by 
number (INI, IN2,  etc.).  (Numbers in parentheses  indicate  the 
percentage of the  total  number of galls (n = 141) found  within 
each  inflorescence). 
186 
Materials and  methods 
On March 20, 1984, nematode-galled specimens of 
common  fiddleneck were sampled at a  site 24 km south 
of San Jose, California in  the  Santa  Clara Valley (inter- 
section of Monterey  Road  and Crowner Avenue). We 
believe that this is the site of nematosis  that was investi- 
gated by Godfrey (1940) in  1936,48 years prior to Our 
studies.  Using  random  number tables, the  coordinates 
of a  6 x 6 meter  plot were generated  within  the  study 
site and al1 plants (n = 89) within the plot harvested. 
Each  plant was examined  for the presence of galls, and 
the size and position of each gall, the inflorescence in 
which it was situated, and the flower it replaced, re- 
corded.  Inflorescence  and flower positions of each 
common fiddleneck  individual were coded as follows : a) 
IN1-IN7, where IN1 represents the uppermost (most 
mature)  inflorescence  (Fig. 1); b) Fl-F7, where Fl rep- 
resents the lowermost,  (most  mature) flower within a given 
inflorescence  (Fig.  2 A). Common  fiddleneck flowers are 
arranged in determinant inflorescences, referred to as 
helicoid cymes (Hitchcock et al., 1969). Thus,  the basally 
located flower is the oldest  and  blooms  first (Fig. 2 A). 
A two-sample t-test that does not involve a pooled 
estimate of a common variance (Steel & Torrie,  1980) 
was used to compare the mean diameter of galls at 
different  inflorescence and flower positions. In addition, 
a  loglinear mode1 (Fienberg, 1980) simultaneously  tested 
the flower  and  inflorescence  galling  frequencies. 
Results 
Nematode-induced flower galls  were found to be 
associated exclusively with the floral tissues, the  degree 
of galling  being  affected by both  the age of inflorescence 
and the age of flower within the inflorescence. Galls 
were restricted to  the five most  mature  inflorescences in 
al1 plants studied. The uppermost inflorescence (IN1) 
contained 78 O/o of the galls found (Fig. 1). Gall inci- 
dence in  the remaining  infested  inflorescences  showed  a 
marked  decrease  with IN2 containing 14.8 O/O and IN3, 
IN4, and IN5 collectively containing less than 8 O/O of the 
total  galls (i.e. 3.5,2.2  and 1.5 O/o, respectively). A  similar 
pattern of gall distribution to that observed between 
inflorescences was also apparent within a given inflor- , 
escence. Only the six basally located flowers contained 
any galls, and approximately 82 O/O of the galls were 
located in either F1 or  F2 (Fig. 2 A), these  being the  most 
mature flowers. 
&Ils for;r,ed on cozmon fiddleneck by Angttina 
amsinckiae grow over  a  period of four to  eight weeks to 
a maximum size of approximately 20 mm  in diameter. 
An interesting trend  can  be seen in  the size and position 
of the galls. Within IN1  the size of the galls decrease 
with  increasing flower number (Fig. 3). Consequently, 
the  mean gall diameter of IN1, F1 was larger than  the 
Revue Nématol., 9 (2) : 185-189 (1986) 
1 
Galls caused by Anguina  amsinckiae on Amsinckia  intermedia 
Fig. 2. Amsinckia intemedia. A : Flower position coded by number (Fl, F2, etc.). Fl-F6 as illustrated are replaced by galls. 
(Nurnbers  in  parentheses  indicate  the  percentage of the  total  number of  galls (n = 141)  found  in  place  of  each  flower.) B : Plant 
stature  immediately  prior  to  floral  initiation; C : Form of a  mature  inflorescence  (Note  the  seeds  within  the  sepals of the  lowermost 
flower : Fl); D : Seedling or rosette  stage; E : Form  of  a  young  inflorescence  subtended  by  floral  bracts. 
Revue Nématol., 9 (2) : 185-189 (1986) 187 
D. J.  Pantone & C. Womersley 
I N I .  F1 I i (  (3.48, 52) 
IN1. F2 I (3.44. 32) 
IN1, FGT2 (2.13, 28) 
INGTI. F1 I I I  (2.81. 22) 
INGTI, F2 (2.37. 8 )  i 
' 2 ' 4  6 ' 8  10 12 14 18 18 
MILLIMETERS 
Fig. 3. Box and whiskers diagram of gall size measured by 
diameter.  Dashed  lines  in  the  boxes  indicate  the  sample  means; 
solid  lines  in  boxes  indicate  the  medians.  Fifty  percent  of the 
sample  values  are within the  boxes;  the  left  side  of  the  boxes 
indicates  the  25th  percentile,  and the right  side  of  the  boxes 
indicates  the  75th  percentile. The lines  extending  away  from 
the  edges of the box  (whiskers)  indicate  to the  left  he 
minimum  values  and to the  right  he  maximum  values. 
Numbers  in  the  parentheses  are  standard  deviation  and  sample 
size  (i.e.  galling  frequency),  respectively. (IN1 = Inflor- 
escence 1; INGTl = Inflorescence greater  than 1; FI = Flower 
1; F2 = Flower 2; FGT2 = Flower greater  than 2.) 
mean gall diameter of IN1, FGT2 (Inflorescence 1, 
Flower greater  than 2) (Z = 2.33, P < 0.05). F1 is older 
than  F2;  F2 is  older than E3, and so on.  Therefore, the 
gall that replaces F1 is probably older than galls that 
replace F2  or F3. Older galls  have had  a  chance  to grow 
more and,  therefore,  are larger. The same analogy can  be 
made  for galls within  different inflorescences but  on  the 
lowermost flower (Fl). For example, the mean' gall 
diameter of IN1, F1 was larger than  that of INGT1, F1 
(Inflorescence greater than 1, Flower  1) ( Z  = 2.13, 
P < 0.05). 
Using a loglinear mode1  which included  the  effects of 
inflorescence, flower, and inflorescence-flower interac- 
tion, we compared  the frequency of nematode galls at 
different inflorescence and flower positions. The fre- 
quency  data was grouped as indicated  in Figure 3. Note 
that  there were no galls within INGT2 at  FGT2.  The 
effect of inflorescence (x' = 22.89, d.f. = 1, 
P < 0.0005) was more  important  than flower (x' = 8.44, 
d.f. = 2, P < 0.025) in  determining  the gall frequency. 
No interactive effects between the inflorescence and 
Îiower were detected (xz = 2-87, dl .  = 2, P = n.s.). 
Four  multiple  comparisons were made : F1  and F2, F1 
and  FGT2,  F2  and  FGT2,  and  IN1  and  INGTI.  The F1
frequency was greater  than  F2 (Z = 3.00, P < 0.05) and 
FGT2 (Z = 3.19, P < 0.05). However, we were unable 
to  conclude  from  the data  that  the  F2  frequency was 
significantly  greater than  FGT2 (Z = 0.66, P = n.s.). 
188 
Comparing  the frequencies of galls within inflor- 
escences, the  IN1  frequency was greater than 
INGl (Z = 4.78, P < 0.05). 
Discussion 
The success of Anguina amsinckiae in  inducing 
gall formation seems to  be  dependent  on  its ability to 
locate  susceptible flower primordia, since more mature 
flowers are probably immune to nematode infection 
(Godfrey, 1940). Statistical analyses of  gall distribution 
demonstrate that  the uppermost inflorescence  and  lower- 
most flower within an inflorescence are significantly 
more  frequently galled by the  nematode.  This indicates 
that  the observed gall distribution,  and  thus  susceptible 
flower location, is not due to chance. Although it is 
probable  that  a number of factors  influence  the success 
of gall induction  and its restriction to specific inflor- 
escences and areas within them, OUT observations suggest 
that  the  most  important  factors  are  host  growth  patterns 
and  moisture availability around  the inflorescences. 
A dramatic  change  in  the  form  and  stature of common 
fiddleneck occurs immediately after  flowering is initia- 
ted.  Prior  to this, the weed  is compact,  the foliage dense, 
and the internodes are short (the rosette stage) (Fig. 
2 D). It is presumed  that  the  effects of environmental 
factors such as  wind and  sunlight  would  be  reduced by 
virtue of this compact morphology, resulting in the 
maintenance of a relatively constant  environment within 
the  plant  structure.  In  particular,  the base of the  rosette 
which is comprised of many whorls of tightly overlap- 
ping leaves that  originate  near the soi1 surface (Fig. 2 D) 
would appear to provide a high degree of protection 
from  the effects of a  fluctuating  external  environment 
compared to any other above-ground portion of the 
rosette. We have observed concentrations of nematodes 
on  the moist surfaces of overlapping leaves in Young 
seedlings close to  the  soil-plant  interface (D. J. Pantone, 
unpubl.). However, this  protection  is  subsequently re- 
duced to a minimum at the initiation of and during 
flowering  when the height of the  plant increases  two to 
threefold (Connor, 1965) with a concomitant increase in 
internode  length  and leaf spacing (Fig. 1). The effects of 
this,  in  terms of nematode displacement  are probably 
twofold. Firstly, rapid stem elongation  results  in  the  total 
disruption of compact  structure  and  the  exposure of the 
aerial portion of the  plant to  a much  harsher environ- 
ment where wind and sunlight may reduce both free 
moisture  on  the plant's surface and  the relative humidity 
occurs, the sheathing and overlapping leaves present  at 
the  terminal growing tip of the  stem (Fig. 2 B) may be 
instrumental in simultaneously providing shelter for 
infective nematodes and a means by which they are 
translocated  to  the  earliest  developing inflorescence 
(INI). This is supported by  the  observations of Godfrey 
Revue Nématol., 9 (2) : 185-189  (1986) 
G f  el& S ï 3 ï ï G ü î î h ~  &-. s?.CGiidj', as Stem e!GiigaüGïl 
Galls caused by Anguina  amsinckiae on Amsinckia  intermedia 
~ 
(1940) Who was only able to find groups of infective 
larvae lying between the young leaves of the terminal 
and  lateral growing points during  stem elongation. 
With  the above in mind, we hypothesize the following 
as being the probable mode of nematode infection, 
resulting in  the observed  distribution of  galls. Initially, 
those  nematodes that  are able to locate the developing 
apex of the  plant at  the onset of stem  elongation will 
tend  to  be within the protected  environment  provided by 
the young leaves (Godfrey, 1940). Thus, even though 
stem  elongation  disrupts  compact structure (Fig. 2 B), 
the shelter  provided by the leaves at  the apex of the stem 
ensures  that high relative humidities and surface  water 
are maintained within the apically developing inflor- 
escence (INI).  This in tum will allow a favorable  en- 
vironment for infective nemaiodes, and will favor gall 
formation  on  the earliest developing flowers. Sub- 
sequently,  as IN2 begins to form, the continued change in 
plant morphology will permit further removal of surface 
moisture  and  restrict he movement of nematodes  either 
from  IN1 or  from  the  base of the  plant  to  IN2.  With 
continued growth, the extent of surface water loss by 
evaporation will be  such  that  at  the ime of IN6  and  IN7 
development (Fig. l), nematode  movement will be  to- 
tally curtailed,  resulting in  the noninfection of othenvise 
susceptible  floral  meristems. 
A similar scenario may also explain the preferential 
galling of the lowermost flowers (Fl-F6) within a given 
inflorescence. The F1 forms  before the cymose inflor- 
escence elongates (Fig. 2 E). Analogous to  the condi- 
tions  that  occur  when IN1 is forming, the tightly  curled 
inflorescence  and  floral  bracts that occur  when F1 first 
forms provides a microenvironment that is sheltered 
from  the effects of desiccation. Later as the inflorescence 
elongates (Fig. 2 C), the floral  meristems will be  sub- 
jected to increased exposure to the extemal environ- 
ment,  resulting  in a reduction in relative  humidity  near 
the flowers, curtailing  nematode  movement. 
Godfrey (1940) reported that Anguina amsinckiae 
stimulates  the  floral  meristems to differentiate  into 
galls by ectoparasitic feeding. Apparently, only very 
young flowers whose tissues have not differentiated  into 
more  mature  floral  organs  are  susceptible. If A. amsinc- 
kiae is to cause the flower to form a gall, the nematode 
must feed on meristematic  floral  tissues.  Consequently, 
Accepté  pour  publication le 3 janvier 1986. 
the period when the flower is susceptible is probably 
quite short. If the  maturation of the floral meristems 
could  be slowed, the period of susceptibility  to  nemato- 
sis may be lengthened, and the incidence of galling 
increased.  Plant growth inhibitors  may provide a means 
of artificially slowing  down  floral  maturation and 
thereby  enhance the degree of galling. 
ACKNOWLEDGEMENTS 
The authors would  like  to  thank D. DiPietro  for  preparing 
the illustrations, and M. L. Stanton and R. F. Nonis for 
helpful  discussions. 
REFERENCES 
CONNOR, D. J. (1965).  Seed  production  and  seed  germination 
of Amsinckia  hispida.  Aust. J. exp. Agric. anim. Husb., 5 : 
495-499. 
FIENBERG, S. E. (1980). T h e  Analysis of Cross-Classifed  Cate- 
gorical Data, 2nd  Edition.  Cambridge,  Mass., MIT Press, 
198  p. 
FOWLER, M. E. (1968). Pyrrolizidine alkaloid poisoning in 
calves. J. Am. vet. med. Ass, 152 : 1131-1137. 
GODFREY, G. H. (1940).  Ecological  specialization  in the stem- 
and  bulb-infesting  nematode, Ditylenchus  dipsaci var. am- 
sinckiae.  Phytopathology, 38 : 41-53. 
HITCHCOCK,  C. L., CRONQUIST, A., OWNBEY,  M. & THOMPSON, 
J. W.  (1969). Vascular  Plants of the Paci5c Northwest, Part 4, 
Ericaceae  through  Canzpanulaceae, Seattle,  USA,  Univ. 
Washington  Press,  510  p. 
NAGAMINE,  C. & MAGGENTI, A. R. (1980).  Blinding  of  shoots 
and  a leaf  gall in Amsinckia  intemedia induced by Anguina 
amsinckiae Steiner & Scott,  1934)  (Nemata,  Tylenchidae), 
with  a  note  on  the  absence of a  rachis  in A. amsinckiae. J. 
Nematol., 12 : 129-132. 
PANTONE, D. J., BROWN, S.  M. & WOMERSLEY, C.(1985). 
Biological  control  of  fiddleneck. Cal$ Agric., 39 : 4-5. 
STEEL, G. D. R. & TORRIE, J. H. (1980). Principles and 
Procedures of Statistics :A  Biometric  Approach, 2nd  Edition, 
New  York,  McGraw-Hill Book Co.,  633  p. 
STEINER, G. & SCOTT, C. E. (1934).  A  nematosis  of Amsinckia 
caused by a new variety of Anguillulina dipsaci. 3. agric. 
Res., 49 : 1087-1092. 
Revue Névnatol., 9 (2) : 185-189  (1986) 189 


The distribution of flower galls caused by Anguina amsinckiae on the weed, common fiddleneck, Amsinckia intermedia

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