Mullens, B.A.

Poinar, G.O.

Name not available

Heleidomermis magnapapula n. sp. (Mermithidae : Nematoda) parasitizing Culicoides variipennis (Ceratopogonidae : Diptera) in California

Horizon / Pleins textes

Heleidomermis  magnapapula n. sp. (Mermithidae : Nematoda) 
parasitizing Culicoides variipennis 
(Ceratopogonidae : Diptera) in California 
George O. POINAR, Jr. and Bradley A. MULLENS 
University of California, Berkeley, CA 94720  and  University of California,  Riverside, CA 92521, USA. 
SUMMARY 
Heleidomennis  magnapupula n.  sp.  is  described  as  a  parasite  of the biting  midge, Culicoides variipennis (Coquillett)  in  southern 
California. The size and  shape of the  amphidial  pouches  and  spicules  and  form  of  the  cephalic  papillae  separate H. magnapupula 
n.  sp.  from  previously  described  species.  Features of the  preparasitic  juveniles  are  presented.  Host  larvae  occur  in  dairy  wastewater 
ponds  and the adults  are  a  major  vector  of  bluetongue  virus  to  North  American  ruminants. 
RESUME 
Heleidowzermis magnapapula n.  sp.  (Mermithidae : Nematoda)  parasite 
de Culicoides variipennis (Ceratopogonidae : Diptera)  en  Californie 
Description  est  donnée  de Heleidomennis  magnapupula n.  sp.,  parasite du Ceratopogonide Culicoides variipennis en  californie 
du Sud. La taille et la forme des poches amphidiennes et des spicules, ainsi que la forme des papilles céphaliques séparent H. . 
magnapupula n.  sp.  des  espèces  déjà  décrites.  Les  caractéristiques  des  juvéniles  préparasites  sont  présentées.  Les  larves  hôtes  se 
rencontrent  dans  les  mares  contenant  les  eaux  usées  des  laiteries  et  les  insectes  adultes  constituent  le  principal  vecteur du virus 
du blue tongue " des ruminants en Amérique du Nord. 
~~ ~~~~ 
Mermithid  parasitism  has  been  noted  on several 
occasions from  biting midges of the genus Culicoides, 
but proper identifications have been rare (see Wirth, 
1977). During  studies  on  the biology of Culicoides 
variipennis (Coquillett) in dairy wastewater ponds in 
southern  California,  mermithid  infections were noted in 
several populations. After preliminary observations on 
nematode life history, preserved  mermithids  and  para- 
sitized host larvae were sent to the first author for 
further life history and systematic  studies. 
Host larvae of C. variipennis were collected from  the 
surface 1-2 cm of mud  at  the edges of dairy wastewater 
ponds. Mud was sieved to remove late instar larvae, 
which were held in  tap water in Petri dishes until  the 
mermithids emerged. Some hosts and female mermi- 
thids were held  individually to determine the  number of 
parasites  emerging per host, the  duration of oogenesis, 
and the number of infective juveniles per mermithid 
female.  Larvae of C. variipennis and  a Chironomus sp. 
were later  placed  into the Petri  dishes  to  determine the 
mode of entry.  For  taxonomic  studies,  adult  nematodes 
were killed in 60" water, fixed in  TAF and processed to 
glycerin. 
The nematodes  were  determined to be  a new species 
of the genus Heleidonzennis. In  the quantitative  portion 
of the following  description, the range of the  character 
is given in parenthesis  following the mean value, 
Revue  Neinatol. 10 (4) : 387-391  (1987) 
Heleidotnermis magnapapula n.  sp. 
(Figs  1 -1 O) 
Mermithidae Braun, 1883; 
Heleidolnermis Rubzov, 1970. 
MEASUREMENTS 
FenzaZes (n = 10) : L = 1.0 cm (0.9-1.4); greatest 
diameter = 139 pm (107-164); distance from head to 
nerve  ring = 231 pm (206-263); V = 43 (26-58); length 
and width of vagina = 50 pm (35-65) x 56 pm (42-69); 
diameter of amphidial  opening = 4 pm (3-5); length of 
amphidial  pouch = 9 pm (8-1 1);  egg  diameter = 42 pm 
(32-50) x 52 pm (43-61). 
Males (n = 10) : L = 0.5 cm (0.4-0.7); greatest 
diameter = 82 pm (50-95); distance from head to nerve 
ring = 224 (206-238); length of spicules = 70 pm 
(53-83); greatest  width of spicule  shaft = 8 pm (6-12); 
length of tail = 234 pm (190-301); body diameter at 
cloaca = 78  pm (63-89); diameter of amphidial  opening 
= 5 pm (4-7); length of amphidial pouch = 9 pm 
(8-12). 
Holotype (female) : L = 1.1 cm; greatest diameter 
= 113 pm;  distance  from  head to nerve  ring = 263 pm; 
387 
Figs  1-10. Heleidornemzis mugnupapula n.  sp.  1 : Ventral  view  of  male  tail  (mag.  same  as  in  Fig.  10); 2 : Ventral  view  of  female 
head; 3 : Lateral  view  of  female  head  (mag.  same  as in Fig. 2); 4 : Lateral  view  of  male  head  (mag.  same  as  in  Fig. 2); 5 : Variations 
in spicule  size  and  shape. The upper  spicule  is  the  normal  form  and  the  lower  one  is  the  most  common  variation  (mag.  same  as 
in Fig. 2); 6 : Cross  section  of  male; 7 : Enface  view  of  male  (mag.  same  as  in  Fig. 2); 8 : Lateral  view  of  infective-stage  juvenile 
(mag.  same  as in Fig. 2); 9 : Lateral  view  of  vaginal  area;  10 : Lateral  view of male  tail. 
388 Revue Nématol. 10 (4) : 387-391  (1987) 
Heleidomermis magnapapula n. sp. 
~ ~~ ~~~ ~~ 
V = 41;  length  and  width of vagina = 51 pm x 53 Pm; 
diameter of amphidial opening = 3.2 pm; length of 
amphidial pouch = 9 pm; egg diameter = 61 pm x 
50 pm. 
Allotype (male) : L = 0.5 cm;  greatest  diameter 
= 76 pm; distance  from  head to nerve fins = 220 p; 
length of spicules = 67 pm; greatest  width of spicule 
shaft = 8  pm;  length of tail = 212  pm;  body  diameter 
at cloaca = 82 Pm; diameter of amphidial opening 
= 5 pm; length of amphidial pouch = 9 pm. 
Infective-stage juveniles (n = 10) : L = 182 hm 
(164-200); greatest  diameter = 13 pm (10-16). 
DESCRIPTION 
Adults : Small to medium length white nematodes 
with  a  smooth  cuticle  lacking  noticeable  cross  fibers in 
the  adults;  adult cuticle 5-8 pm  thick at  the level  of the 
amphids; head homeocephalic, rounded with two an- 
terior  lateral  head  papillae in one  plane and  four sub- 
medial head papillae arranged in a second plane just 
posterior to the lateral head papillae. Mouth shifted 
ventrally, opening near the tips of the lateral head 
papillae; mouth opening always anterior to the four 
submedial papillae. Posterior to the four submedial 
papillae is a  hypodermal  constriction and just  beneath 
this constriction is a circle  of six papillae arranged in dorsal, 
ventral,  lateral  ventral  and  lateral  dorsal  positions.  These 
papillae  range  from  being highly developed with distinct 
nerve innervations to being  almost  rudimentary. They 
are treated here as neck papillae, rather than being 
interpreted as part of the  head  papillae complex. The 
nerve endings  on  the  submedial  papillae  are  unique  and 
occur in well defined  longitudinal  bands in contrast to 
the lateral papillae which are  terminated by small pap- 
illose nerve  endings. The anterior  lateral  papillae  could 
be  considered as mouth  papillae and  the  four submedial 
papillae as head papillae. The position of the amphids 
is variable.  They never occur  anterior to  the  neck 
papillae  and  are  sometimes  at the same level; usually  the 
openings are posterior to the neck papillae. The am- 
phidial  openings  are  circular and shifted slightly dorsal; 
amphidial pouch spherical to slightly elliptical; eight 
hypodermal cords; vulva opening circular; vulva flap 
absent; vagina barrow-shaped, nearly circular; vagina 
canal straight, terminating at a junction of opposing 
branches of the uteri; spicules short, paired, separate, 
distal  tips  rounded, proximal portion  bent  anteriorly;  tail 
long;  genital  papillae  arranged on  the ventral,  lateral  and 
dorsal  (near  the  tail  tip)  surfaces;  pharyngeal tube 
continues almost to the cloaca in the male. On some 
females,  a  pair of small papillae  occurred on  the ventral 
or lateral portions of the tail. Nerve endings running 
from the hypodermis  through the cuticle were common 
over the body of both sexes. 
Revue Nématol. 10 (4) : 387-391 (I987j 
Postparasitic  juveniles : The final.molts  occur while 
the nematode is still  inside  the  host. Thus no  free-living 
postparasitic juveniles were found. Shed postparasitic 
cuticles removed from  the host showed no tail append- 
age. 
Infective-stage  juveniles : Embryonation,  hatching  and 
the first molt occur inside the female nematode. The 
second stage infective forms emerge from the female 
through  the vulvar  opening. The infective  stage is short 
and broad, with a thin stylet, a pair of penetration 
glands, a  stichosome  containing  eight stichocytes, a 
small  reduced  intestine and a  genital anlage. A faint  anal 
opening is present. 
TYPE HOST AND LOCALITY 
Culicoides  van'ipennis (Coquillett)  (Diptera : Cerato- 
pogonidae).  Dairy  wastewater  pond on  the Aukeman , , 
dairy farm,  Mira  Loma,  Riverside Co, California, USA. 
TYPE SPECIMENS 
Holotype (female) and allotype (male) deposited at 
the  Department of Nematology,  University of Califor- 
nia, Davis, California. Paratypes deposited at the La- 
boratoire des Vers, Muséum national d'Histoire natu- 
relle, Paris. 
DIAGNOSIS AND RELATIONSHIPS 
There are two previously described species in the 
highly unusual genus Heleidomemzis, H. vivipara Rub- 
zov, 1970 from  Karelia,  USSR, and H. ovipara Rubzov, 
1974 from  the  Tunkin Valley of the Burjat,  USSR. The 
latter  species is oviparous while the former is ovovivi- 
parous. The present species differs from both of the 
above in both quantitative and qualitative characters. 
The females of H. vivipara are considerably smaller 
(5.2-6.8 mm) than those of H. magnapupula n. sp. 
(8.6-13.7 mm). The amphidial  pouches in H. magnapa- 
pula n.  sp.  are  nearly spherical, measuring only 8-1 1 pm 
in both sexes  whereas in H vivipara they are 17-20 p m  
and in H. ovipara, 18-20 pm. The difference in the 
amphidial  opening  between  male and female (4-6 pm vs 
3-5 pm respectively) is not great in H. magnapapula n. 
sp. but is striking in H. vivipara (3  pm  in  females  and 
10 pm  in males). The egg  diameter of H. magnapupula 
n. sp. (32-61 pm) is greater than  in H. vivipara (30 pm) 
and H. ovipara (30 Pm). 
Since H. magnapupula n.  sp. is ovoviviparous, it 
might be considered most close to H. vivipara. How- 
ever, H. vivipara has straight spicules without modi- 
fied proximal portions, elliptical rather than spherical 
amphidial  pouches,  longer  infective-stage juveniles 
and  normal cephalic  papillae  lacking  bands of papillary 
nerve endings. 
389 
G. O. Poinar, Jr. & B. A. Mullens 
~ ~~ 
DISCUSSION 
H..  magnapapula n.  sp.  differs from  the majority of 
mermithids in several points. The final molt occurs 
within the body of the host. The eggs hatch  and  the  first 
molt  occurs within the body of the  female.  There is an 
anterior circle of two lateral  papillae followed by a lower 
circle of four morphologically distinct submedial pa- 
pillae followed by a lower circle of neck papillae. 
The presence of genital papillae on the lateral and 
even dorsal tail of the male is equally unusual for 
mermithids. The infective  stages of H. magnapapula n. 
sp. possess only eight  stichocytes,  a  character  shared only 
by some terrestrial mermithids of the genera Mermis 
(Poinar & Hess, 1974) and Pheromermis (Kaiser, pers. 
comm.). It is interesting to  note  that  members of Mermis 
also possess a  pair of lateral  anterior mouth papillae and 
a lower circle of four  submedial  papillae. 
The present species shares both spicular and head 
papillary characters with the Heleidomermis reported 
from C. variipennis in similar habitats in New York 
State  (Mullens & Rutz, 1982) and  the New  York 
population is thus also considered  to  be H.  magnapapula 
n.  sp. The occurrence of Heleidomermis in populations 
of C. vanipennis appears  to  be  widespread in  the  United 
States since aside from California and  New York, this 
host-parasite  relationship has been found  in horse pens 
in Alabama (Hribar, pers. comm.) and highly saline 
habitats in southwestern Virginia (Zimmerman, pers. 
comm.). 
BIOLOGICAL NOTES 
Infected larvae of C. variipennis were collected from 
dairy wastewater ponds  at  four  farms  in  southern 
California. Two of the four ponds were permanent, 
while the other two held  water  for six to nine  months 
prior to sampling. Al1 of the  ponds  had some level of 
manure loading, which  favored  high  host  populations. 
Parasitism  at  one  pond, which held  water  for at least  a 
year prior  to  sampling, was approximately 10 O/o in late 
September. The rate of parasitism  can Vary seasonally, 
however, as discussed by Mullens  and  Rutz (1982). 
It is likely that  the  high  salt  and  ammonium  content 
provides  a  harsh  habitat, yet one  that is tolerated,  for  the 
nematode. This is perhaps why certain  modifications of 
the life cycle have occurred in H. magnapapula n. sp. 
Maturation to the  adult stage  inside the insect  restricts 
the  time of contact  between the  mature mermithids  and 
the external  environment. The remainder of the cycle  is 
also accelerated since  mating  occurs  immediately  after 
host  emergence and  the infective  stages  hatch 4-6 days 
later  (at 20"; 8-9 days at 15") and  can penetrate  a  host 
as soon as they leave the female  nematode.  Embryogen- 
esis and hatching  within  the  mother  nematode  can  be 
regarded as a further  adaptation  to  limit  contact of the 
infective juveniles with  the  manure-laden water. In  tap 
water at 20", the  infective juveniles survived 4-6 days. 
3 90 
Figs  11-12.  11 : Adult  female of Heleidomemzis magnapapula 
n. sp. emerging from a fourth instar larva Czdicoides varii- 
pennis; 12 : Adult Culicoides variipennis containing  a  develo- 
ping  juvenile of Heleidomemzis magnapapztla n. sp. 
When placed  together  with second and  third  stage  larvae 
of C. variipennis, the infective stages rapidly  penetrated 
through the larval cuticle and entered the hemocoel 
(Fig. 13). Such aggressiveness was also noted to  occur 
when second and  third stage Chironomus larvae  were also 
placed in  the infection  chamber.  Penetration  occurred 
normally but the juveniles  were  killed  within two hours by 
a  melanization  reaction (Fig.  14). The duration of 
parasitic  development was not  noted but based on  host 
life history, is  judged to be  about 14 days. Most of the 
mature nematodes  emerge  from fourth instar  host  larvae 
(Fig.  11) but emergence was also noted  to  occur from 
third instar larvae and pupae. Several adult C. varii- 
9ennis were observed to harbor  mermithids  as well 
Revue Nématol. 10 (4) : 387-391 (1987) 
Heleidomermis magnapapula n. sp. 
Figs  13-14.  13 : Two  juveniles  of Heleidonzemzis ntagnapapula 
n. sp. penetrating the cuticle of a second instar Culicoides 
van'ipennislarva; 14 : Two  juveniles  of Heleidonzemzis magna- 
papula n. sp. that were  melanized  after  entering  the  hemocoel 
of a  second  stage Chironomus sp.  larva. 
Accepté pour publication le 27 janvier 1987. 
(Fig. 12) and this is probably the main vehicle of 
dispersal for H. magnapupula. Though prior  studies in 
New York did not yield more than two parasiteslhost 
(Mullens & Rutz, 1982) as many as six nematodes 
emerged  from  a single host  larva in  the present  studies. 
In cases where hosts harbor both male and female 
mermithids,  it is possible that  the  pair  could  mate while 
still within the insect. Isolated female mermithids did 
not produce developing eggs whereas thirteen mated 
females produced an average of 1 709 (1 099-2 553) 
infective juveniles each. 
The host, C. van'ipennis, is a major vector of blueton- 
gue virus to  North American  ruminants. It is unclear at 
present  whether  parasite  introductions  or  cultural  prac- 
tices might  increase  the level  of Culicoides parasitism in 
wastewater  ponds. The hosts  can  be  produced in large 
numbers in laboratory colonies, so the possibility of 
mass-culturing  the  parasite exists. However, this nema- 
tode lacks a life stage  suitable  for  long-term  storage  or 
easy field  transport.  Further  studies may elucidate 
cultural factors (e. g. adjusting the level of manure 
loading) that would favor  parasite activity. 
REFERENCES 
MULLENS, B. A. & RUTZ, D. A. (1982).  Mermithid  parasitism 
in Culicoides van'ipennis (Diptera : Ceratopogonidae) in 
New  York  State. Mosquito News, 42 : 231-235. 
POINAR, Jr., G. O. & HESS, R. (1974). Structure of the pre- 
parasitic juveniles of Filipjevimennis leipsandra and some 
other Mermithidae (Nematodea). Nematologica, 20 : 163- 
173. 
RUBZOV, 1. A. (1970). [A new  species and  genus of mermithids 
from  biting  midges.]  In : Novye i maloizvestnye vidy foewzy 
Sibiri. SO izd.  Nauka,  Novosibirsk, 3 : 94-101. 
RUBZOV, 1. A. (1974).  [New  species  of  mermithids  from 
midges.] Parasitologiya, 8 : 212-219. 
WIRTH, W. W. (1977). A review  of the pathogens  and  parasites 
of the biting  midges  (Diptera : Ceratopogonidae). J. Wash. 
Acad. Sci., 67 : 60-75. 
Revue Nématol. 10 (4) : 387-391 (1987) 391 


Heleidomermis magnapapula n. sp. (Mermithidae : Nematoda) parasitizing Culicoides variipennis (Ceratopogonidae : Diptera) in California

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