Ashokkumar, P.

Vadivelu, S.

Horizon / Pleins textes

Description of developmental stages 
of Hemicriconemoides  mangiferae Siddiqi, 196 1 
(Nemata : Criconematidae)(l) 
Pullikuth ASHOKKUMAR* and Sivagami VADIVELU 
Department of Nematology, Tamilnadu Agncultural University,  Coimbatore, India. 
SUMMARY 
The genital  tract  length,  stylet  length  and  body  length  were  found to be  major  criteria in differentiating  the  life  cycle  stages  of 
Hemicriconemoides mangiferae. Al1 juvenile stages except second stage possessed twelve longitudinal rows of spines arranged 
through the length  of  the  body. The second-stage  juvenile  possessed  a  spine-less  cuticle.  Greatest  increase in body  length  and  ovary 
length  was  observed  between  second  and  third  stage  and third  and  fourth stage  respectively.  Length  of  stylet  increased  greatly 
between fourth and  adult  stage. Sex differentiation  occurred in the  fourth  stage.  Third  stage  juvenile  was  identified  from  second 
stage  by the greater  ovary  length.  A  few  adult  females  were  observed  with  single  flexure  in  the  distal  end  of the ovary. 
RÉSUM~ 
Description des stades juvéniles de Hemicriconemoides  mangiferae Siddiqi, 1961 (Nemata : Cnconematidae) 
Les  principaux  critères  pouvant  servir à différencier  les  stades  juvéniles  de Hemicn'conemoides  mangiferae sont  la  longueur du 
tractus  génital,  celle du stylet et celle du corps. Tous les  stades  juvéniles  sauf  le  deuxième  présentent  douze  rangées  longitudinales 
d'épines  sur  toute  la  longueur du corps. La  cuticule  des  J2  est  inerme. La plus  importante  croissance  de  la  longueur du corps  et 
de  celle de l'ovaire  est  observée  entre  les  J2 et les J3, et les J3-t les  J4,  respectivement, La longueur du stylet  s'accroît  fortement 
au passage  de J4 à adulte. La différenciation  sexuelle  a  lieu  chez  les  J4.  Les 53 peuvent ême différenciés  des  J2  par  la  plus  grande 
longueur  de  l'ovaire.  Quelques  femelles  adultes  présentent un unique  repli  de  l'extrémité  distale  de  l'ovaire. 
Attempts  to  study  the ontogeny  and to describe the 
life-cycle stages of the species of Criconematidae are few 
and far between (Knobloch, 1978). Due to the inad- 
equate details on  the developmental  morphology and  the 
existing close relationship between genera of Cricone- 
matidae workers have  placed juvenile stages across 
genera (Mehta & Raski, 1971), occasionally describing 
them as << new species B. Dasgupta, Raski and Van 
Gundy (1969) emphasised  the  need to describe the larval 
stages of al1 species to  understand  the relationship 
between species. The males of most species of Hemi- 
criconemoides are uncommon  which reiterates the  need 
to describe the juvenile stages at length. The present 
study describes the individual life cycle stages of H. 
mangiferae Siddiqi, 1961, a parasite of wide range of 
crops and most  frequently  found  in tropical and sub- 
tropical regions. 
Materials and methods 
Nematodes were extracted by centrifugal-flotation 
technique (Jenkins, 1964) from soi1 samples collected 
from a sapota  orchard in Tiruchirapalli, India. Individ- 
uals were isolated for  study  from a single sample  con- 
taining al1 stages of H. mangqerae. Specimens were 
processed  through  Seinhorst olutions (Seinhorst, 1959). 
Measurements were made  using a filar micrometer and 
from camera lucida tracings. Individual stages were 
separated by virtue of their body length and gonad 
length, though a few transitional specimens were con- 
firmed  through  measurements. Al1 the stages were 
available for study. 
* I  
(1) A part of M. Sc.  (Agric.)  thesis  of  senior  author. 
* Present  address : Nentatology Unit, International Crops  Research Institute for the Semi-And Tropics,  Patancheru, Andhra Pradesh 
502 324, India. 
Revue Nénzatol. 13 (3) : 31 7-322 (1990) 317 
P. Ashokkumar & S. Vadivelu 
Results  and  discussion 
MORPHOMETRICS 
The body length of H. mangiferae increased from 
0.1450-0.1733 mm for  second-stage juveniles to 
0.4094-0.4875 mm for adult females. The growth in 
body length was greatest between the second and  third 
stages (74.8 "O) and least between the  fourth  and  adult 
stages (24.2 "0). The  number of body  annules was almost 
constant from stage to stage (R = 123, CV = 4.2). 
Annule  width  increased from 1.9 pm  for second stage 
juveniles to 4.0 pm  for  adult females. Apparently, the 
increased  annule  width resulted in  the increased body 
length  from stage to stage. Body  width increased from 
14.0 pm for  second stage to 24 pm  for  adult females. 
between second stage and third stage. The develop- 
mental  pattern of the anterior cone  portion of the stylet 
was the same as for  the entire stylet. The oesophagus 
also  showed  a  similar pattern of growth, with increase in 
length  being greatest (22.5 "O) between fourth  and  adult 
stages and least (8.8 "O) between the second  and  third 
stages. 
The female  reproductive  system  increased from 
18.0-23.3 pm for second stage to 56.3-296.9 pm for 
adult females (Fig.  1). The growth of  ovary was greatest 
between the  third  and  fourth stage juveniles  (241.8 "O) 
and least between the  fourth  and  adult stages (38 "0). 
~ L O M E T R I C S  
The " a ratio indicated the  adult females to be the 
thinnest  and  the second-stage  juveniles the stoutest. The 
third  and  fourth stage juveniles were similar in  stature. 
The " b " ratio increased  with  nematode  maturity  being 
greatest (36.6 %) between  second and  third stage juv- 
eniles,  which  coincided  with the time of greatest increase 
in body length. Anal openings were obscure in early 
stages of development, so the " c " ratio was not com- 
pared. 
- i , 
A B C  D E F 
DESCRIPTION F DEVELOPMENTAI-  STAGES 
n 
50 II 
J 
Fig. 1. Development of gonad in Hemicriconemoides mangi- 
ferae. A : Second  stage; B : Late  second  stage; C : Third  stage; 
D : Late  third  stage; E : Fourth  stage  ovary; F : Fourth stage 
testis; G-1 : Adult  ovary; 1 : Reflexed  ovary in  adult; J : Adult 
testis. 
Growth  in  body  width was greatest between the second 
and  third stage (31.3 "O) and least between the  fourth  and 
adult stage (8.1 "0). The length of stylet increased from 
42.7 pm  in  the second stage to 61.5 pm in  the  adult 
female. Growth in stylet length was greatest (16.5 '/O) 
between fourth and adult stage and least (10.8 "O) 
Second stage juvenile 
Body arcuate when fiied with a mean of 119 annules. 
Annules do not bear spines or scales and are smooth. 
The head  structure was similar to  that of adult  female 
with variation only in  the width and  height of head. The 
stylet was strongly developed with forward projecting 
spear knobs and averaged  42.7 pm .in total length 
(Table 1). The genital primodium in  the arly  second  stage 
was almost oval, about  18  pm long. In late  second stage: 
this lengthened in a developing  gonad to 23.3 pm. The 
genital primordium was comprised of four clearly differ- 
entiated cells in  the early second stage and lengthened to 
form a six to eight celled sausage-shaped  gonad, in  the 
late second-stage. The  anus was not seen. The tail was 
similar in shape to  that of the  adult tail and varied  only 
in width at  the posterior region (12.9 pm). 
In moulting, the second stage juvenile cuticle length 
was 173.3 Pm; the gonad in developing third stage 
juvenile in second stage (Fig. 1) cuticle was 23.3 pm. 
Stylet length was 46 pm and anterior cone of stylet 
31 pm. A specimen was observed  with  developing third 
stage juvenile in second stage cuticle, which possessed 
spined  annules in  the posterior region and characters of 
second stage (smooth cuticle) in the anterior region, 
indicating that  moulting  proceeded  from  the posterior 
region. 
Among  the characters, greatest variation was observed 
in  the  knob height (CV = 11.4) and  total body  length 
(CV = 10.3). 
318 Revue Nématol. 13 (3) : 31 7-322 (1990) 
Developmental  stages  of Hemicriconemoides  mangiferae 
Table 1 
Morphometric  and  allometric  characteristics 
of the life-cycle  stages  of Hemicriconemoides  mangiferae 
Character Life Cycle  Stage 
Second 7'hird Fourth Adult female 
(n = 8) (n = 12) (n = 14) (n = 14) 
MORPHOMETRICS (Pm) 
Body  length 
Body  width 
Oesophageal  length 
Stylet  length 
Prorhabdion  length 
Knob  height 
Knob  width 
Annule  width 
Female  gonad  length 
R 
R ex 
R oes 
RZ 
ALLOMETRICS 
' a  ratio 
b ratio 
c  ratio 
155  (16.0)* 
(145.0-173.0)** 
14.6  (0.8) 
(14.2-15.6) 
66.5  (4.8) 
(63.7-72.0) 
42.7  (2.9) 
(41,O-46.0) 
29.7  (1.2) 
(29.0-31.0) 
2.7  (0.3) 
(2.4-3.0) 
4.5  (0.4) 
(4.1-4.8) 
1.92  (0.1) 
(1.88-2.0) 
20.0  (3.0) 
(18.0-23.0) 
119 (1.2) 
27  (0.6) 
(118-120) 
(27-28) 
33 (0.6) 
(30-33) 
- 
10.56  (0.5) 
(10.2-11.1) 
2.3  (0.1) 
(2.3-2.4) 
- 
271 (18.1) 
(250.0-281.0) 
18.8  (2.2) 
(16.1-20.8) 
72.3  (5.1) 
(70.0-78.1) 
47.3  (1.5) 
(46.0-49.0) 
40.0  (4.5) 
(36.0-44.3) 
3.9  (0.1) 
(3.8-4.0) 
4.8  (0.2) 
2.60 (O. 1) 
42.0  (2.7) 
(4.7-5.0) 
(2.50-2.7) 
(40.0-45.0) 
120 (1.5) 
(119-122) 
30 (0.7) 
(26-35) 
34 (1.0) 
(31-47) 
- 
14.43  (0.9) 
3.8  (0.3) 
(13.5-15.2) 
(3.4-4.1) 
- 
354 (17.9) 
24.0  (1.4) 
(344.0-375.0) 
(22.0-24.0) 
87.0  (9.3) 
(78.8-97.0) 
53.0  (1.4) 
(52.0-54.4) 
44.3  (3.8) 
(40.0-47.0) 
4.2  (0.3) 
6.9  (1.0) 
3.60  (0.6) 
(3.8-4.4) 
(6.2-8.0) 
(2.80-4.00) 
143.3  (18.0) 
(131.3-164.2) 
125 (2.3) 
30 (0.6) 
(122-126) 
(30-31) 
35 (3.5) 
(33-38) 
- 
15.1  (1.0) 
(14.0-15.6) 
4.1  (0.7) 
(3.4-4.8) 
- 
439 (3.8) 
(410.0-488.0) 
26.0  (3.0) 
(22.0-34.0) 
106.5  (8.0) 
(96.8-125.0) 
61.5  (5.0) 
(53.0-74.1) 
46.0  (4.7) 
(41.0-53.6) 
5.1 (1.8) 
(4.0-5.0) 
7.1  (1.3) 
(6.2-9.0) 
4.00 (0.3) 
(3.10-4.40) 
198.0  (41.0) 
128  (8.0) 
32 (3.3) 
(156.3-296.9) 
(125-143) 
(29-38) 
37 (4.1) 
(36-43) 
84 (7.4) 
(70-92) 
17.0  (2.0) 
(13.9-20.8) 
4.1  (0.4) 
16.3  (2.2) 
(3.7-4.7) 
(14.2-22.2) 
* Mean  and standard deviation. 
** Range. 
Revue Nématol. 13 (3) : 317-322 (1990) 319 
P. Ashokkuvnar di S. Vadivelu 
i%ird stage juvenile similar to those in second stage. In the early stage of 
Body arcuate to straight when heat relaxed with a development, the third stage genital primordium was 
mean of  120 annules  and melve rows  of spines in each 40 pm long  with  seventeen clearly differentiated cells. 
annule arranged longitudinally over the length of the No change in tail shape was  observed but for the 
body. Head annules and shape and stylet structure were possession of spines on  the annules (Fig. 2). 
A B 
Fig. 2. Juvenile  stages of Hemicnconernoides  rnangijerae. A : Developing  third  stage  inside  second  stage  cuticle; B : Third  stage; 
C : Developing fourth stage  inside third stage  cuticle;  D :Fourth stage - E-G : Juvenile  cuticle  annules. E : Second  stage; F : Third 
stage; G : Fourth  stage; H : AduIt  female  cuticle. 
The growth in body  length was uniform (CV = 6.7) 
as in second stage. Similar was lengthening  on  the stylet 
(CV = 3.2).  However, the  head height  and  width 
showed great variations of  27.7 and 20.4 % respectively, 
quite unlike the second stage. 
Fourth stage fernale juvenile 
Body  assumed a variety  of shapes, from near straight 
to slightly arcuate, with  a  mean of 125 body annules. 
The annules possessed  twelve  rows  of spines as in  the 
third stage. The shape of head and stylet remained 
unchanged though their sizes changed with maturity. 
The length of stylet ranged from 52-54.4 Pm. In this 
stage the  gonad was  143.3 pm long  and  more  developed 
than  in  the arlier stages. Genital  primordium  increased 
from  25  in early fourth stage to  numerous cells in  later 
stage where the region  proximal to vagina  was  hyaline. 
The germinal  zone was clearly differentiated. In  some 
specimens a suggestion of vagina was observed even- 
though vulval opening was wanting. 
The pattern of growth of oesophagus was quite 
dissimilar to that of any other stage, for there was 
appreciable  lengthening of the oesophagus. Due  to  the 
above variation, the " b " ratio also showed greater 
instability (CV = 16.2). 
3 20 Revue Neinatol. 13 (3) : 31 7-322 (1990) 
Developmental  stages of Hemicriconemoides  mangiferae 
Pre-adult  male 
Some fourth moults contained males. The fourth 
stage cuticle was 375 pm with clearly defined testis. The 
cuticle of pre-adult males also possessed twelve longi- 
tudinal rows  of  scales as in other juvenile  stages. Spicule 
and  gubernaculum were  well formed  measuring 
17.2-18.3 pm and 2.8-3.1 pm respectively. Stylet was 
relatively shorter than  that of the  fourth stage preadult 
female juvenile and ranged  between 48.0-51.0 pn with 
a mean of  49.2 pm. However, the stylet was shed  along 
with the cuticle during  moulting  into  adult male, with no 
new process  replacing it. 
B 
25 P 
Fig. 3. Adult  stages  of Hemicriconemoides nzangiferae. A-B : 
Adult  female; C-D : Adult  male; E-G : Tai1  shapes in  adult 
female. 
Revue Nématol. 13 (3) : 31 7-322 (1990) 
Sex differentiation occurred at  the fourth-stage when 
well defiied testis and ovary  were observed.  Anal  open- 
ing was obscure in al1 juvenile stages. 
Adult  female 
A minor deviation from the original description by 
Siddiqi (1961) of adult  female in H. mangiferae was seen 
in the location of the excretory pore which was five 
annules anterior to R oes. Similar discrepancy in the 
location of excretory pore was observed earlier in Crico- 
nemoides parvulus (Edward & Misra, 1965). Siddiqi 
(1961,  1977) described two tail shapes (Fig. 3 E & F)  in 
adult females. An intermediate shape (Fig. 3 G) was 
observed in  the same population. Similar tail shapes  are 
not  uncommon  in  other species  of Hemicriconemoides, 
which cautions the use of tail shape alone in species 
identification. Adult  females of Hemicriconemoides 
possess outstretched ovary without flexures as a general 
rule. A few  females in  the present  study showed  a  single 
flexure in the distal end which was also observed by 
Dasgupta,  Raski  and Van Gundy (1969), in  other spe- 
cies. 
Adult  male 
Though males of H. mangiferae are  documented  to  be 
common, only a single adult male was found in the 
population.  Parthenogenic  reproduction  may  be th   rule 
in  such cases. The measurements of the individual are 
L = 358.2 pm; a = 24.0; b = 5.7; c = 12.0; body 
width = 14.9 pm; oesophageal  ength = 63.4 pm; 
tail = 30.0 pm; testis = 73.3 pm; spicules = 23.3 pm; 
gubernaculum = 4.2 pm; T = 36.3. 
Annules were fine  and  about 1.5 pm wide  near  middle 
of the body. Lip comprised of five annules and a labial 
disc. Annules of head were continuous  with  body  an- 
nules. Stylet absent and oesophagus degenerate. Caudal 
alae reduced  with coarse crenate  margins  ending  before 
the tail tip. 
Fassuliotis (1962) described the life history of H. 
chitwoodiEsser, 1960, to contain  three  moultings;  one in
egg, and two in soil.  However Dasgupta,  Raski  and  Van 
Gundy (1969) found  four moultings and opined  Fassu- 
liotis' observation to have omitted  pre-adult stages. 
Kumar (1980) found sex differentiation to occur in  the 
third stage of H. cocophilus (Loos, 1949) Chitwood & 
Birchfield, 1957, while in H. mapzgiferae and H. chit- 
woodi sex differentiation occurred in  the  fourth stage. 
Fassuliotis also observed the spines of  juvenile stages of 
H.  chitwoodi to possess à 1 pm long setae-like process 
which is lacking in H. mangiferae. The  number of  rows 
of spines are the  same in juveniles  of H. nzangiferae, H. 
chitwoodi and H. strictathecatus Esser, 1960. But in- 
formation  on  the  shape of spine, gonad and stylet length 
will be  useful  in differentiating the  former two while the 
latter  could  be identified by rounded  spear  knobs. 
Juvenile stages of Henzicycliophora do not possess 
spines nor scales (Brzeski & Zuckerman, 1965). The 
321 
P. Ashokkumar Br S. Vadivelu 
possession of spines in  the juvenile  stages of Hemicn'co- 
_.-- nemoideswould be useful in separating these two genera. 
From these  observations it may be  suggested that Cric~- 
nema and Hemicnconemoides  are more closely related to 
each  other  than  to Hernicycliophora. 
ACKNOWLEDGEMENTS 
We gratefully  acknowledge the  helpful  suggestions  offered 
by Drs C. V. Sivakumar, and T. S. Muthukrishnan. The 
financial  assistance  granted by Indian  Council of Agricultural 
Research  is  sincerely  acknowledged. 
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3 22 


Description of developmental stages of Hemicriconemoides mangiferae Siddiqi, 1961 (Nemata : Criconematidae)

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