Table Of ContentJ. mt. Soc. sth. Afr. 1991
Vol. 54, No.2, pp. 9-15
Stichotrema robertsoni spec. n. (Strepsiptera:
Myrmeco/acidae): the first report of sty/opization in
minor workers of an ant (Pheidole sp.: Hymenoptera:
Formicidae)
by
JEYA RANEY KATHIRITHAMBY
Department of Zoology, South Parks Road, Oxford OXI 3PS, England.
This is the first report of the occurrence of stylopization in minor workers of
Pheidole sp. found in a nest. Previous reports of stylopized Formicidae have been
of single males found in light and black light traps. The strepsipteran Slicholrema
robertsoni spec. n. a parasite of Pheidole sp., is described. The heteromerous host
relationship of the heterotrophic type in the family Myrmecolacidae (Strep
siptera) is outlined, and superparasitism in this species is discussed.
9). INTRODUCTION
0
0
2 Strepsiptera are obscure, cosmopolitan, entomophagous parasitoids whose
d hosts include about thirty-four families and seven orders of Insecta (Kathirithamby
e
at 1989a). The family Myrmecolacidae is found in the Oriental, Australian, African,
d
( Neotropical and Nearctic Regions. Adult strepsipteran males are free-living but females
er are neotenic and permanently endoparasitic in the host, except in the family Menge
h
s nillidae. An additional peculiarity in Myrmecolacidae is heteronomy (WaIter 1983). In
bli this unusual pattem of parasitism, better known in Hymenoptera, the males have a quite
u
P different host to the females.
e Nietner first found a strepsipteran parasitic in a worker ant in Ceylon and he
h
y t Sent the specimen to J. Spence. Westwood (1861) described the species Myrmecolax
b niet1Ulri, and Saunders (1872) placed this species in a new family Myrmecolacidae. Nearly
d
e 80 years later OglobJin (1939) investigated the hosts of Myrmecolax. In 1931 he found
t
n Solenopsis xyloni MacCook (= pylades) (Formicidae) with a male puparium of Myrmecolax
a
r in Puerto Aguirre (Argentina). After this he found several large workers ofS . richteri Fore!
g
e and S. quinquecuspis Fore! with puparia or empty male puparia. In 1934 he found a soldier
c
n of Pheidole radoszkowskii ssp. reflexans Santschi with a male puparium.
e
c Previous to this, in 1928, he found Acontiothespis maculatus (Saussure) (Or
r li thoptera) with a female strepsipteran which was described as Mantidoxenos argentinus in
e
d the family Stichotrematidae. Likewise in 1932 he found a cricket with a female of the
n
u Stichotrematidae. No males were found among the Orthoptera he studied. The virgin
ay females of Mantioxenos produced no progeny. A still previous report of stylopized
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Orthoptera was by Voeltzkow (1890) from East Africa. Hofeneder (1910; 1920)
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10 J. ent. SOC. sth. Afr. Vol. 54, No. I, 1991
described the female adult and first ins tar larvae of Stichotrema dallatorreanum, and
mentioned that the material had no males or male puparia.
As all the males Ogloblin (1939) collected were from ants and the females from
Orthoptera he decided to compare the 1St instar larvae. He found that the 1st instars in
Camponotus, Pseudomyrmex and Solenopsis (Formicidae) were similar to the 1St instars of
Mantidoxenos (parasitic in Orthoptera), while 1st instars from females found in crickets
were similar to the 1st ins tar exuviae found in Pheidole (Formicidae). Ogloblin (1939)
therefore established the unique dual host nature or heteronomy as mentioned by Walter
(1983) (males developing in Formicidae and females in Orthoptera or Mantodea), and
suggested the synonymy of the family Stichotrematidae with Myrmecolacidae.
Since Oglobin's investigation only Hofeneder (1949), Luna de Carvalho
(1972a), Teson & Remes Lenicov (1979), Gangne (pers. comm.) and Kathirithamby &
Johnston (unpublished) have found stylopized Formicidae. Hofeneder and Gange found
single specimens while Luna de Carvalho trapped 20 stylopized male Crematogaster sp. in
black light in Angola. Large numbers of fertile and infertile males, alate females, and
major and minor workers of the fire ant Solenopsis invicta Buren were found to be
parasitized by male Caenocolax fenyesi Pierce (Kathirithamby & Johnston unpublished).
Other than Ogloblin, Luna de Carvalho (1972a) was the only one to establish both the
hosts of a myrmecolacid. He found that the males of Stichotrema barrosmachadoi (Luna de
Carvalho) parasitize Crematogaster sp. (Formicidae) and the females parasitize Sphodro
mantis lineola pinguis (La Greca) (Mantodea). He did not find any stylopized worker ants.
That stylopized Formicidae are not frequently found is perhaps due to the
profound changes in b.ehaviour (Ogloblin 1939). Stylopized bees and wasps on the other
hand, although said to undergo changes in behaviour (Salt 1927), are among the most
). frequently collected hosts (the others being Homoptera).
9
0 Young (1987) collected and studied the female strepsipteran Stichotrema dalla
0
2 torreanum Hofeneder which parasitizes Segates decoratus Redtenbacher (Orthoptera: Tetti
d
e goniidae) in New Guinea. In spite of extensive trapping and examination of nests of
t
a thirteen species of ants, he did not find a single stylopized specimen with a male
d
( myrmecolacid. Just one stylopized queen of Camponotus sp. has been trapped by Gagne
r
e (pers. comm.) in Misima Island (New Guinea). The male of Stichotrema dallatorreanum was
h
ublis doef stchriisb espde bcyie Ks owgaasn f aonudnd O ilniv ethirea c(e1p96h4a)l oatsh oCraaexn oochf oSla. xd aaclluattioprerneiasn, ebuumt wLuhenna tdhee Caeadrevaaglhuos
P (1972 b) synonymized the earlier species with the latter.
e
h Hosts of only ten of the eighty five species of Myrmecolacidae that have been
t
y described so far under the four genera Lychnocolax, Myrmecolax, Stichotrema and Caenocholax
b
d are known (Westwood 1861; Hofeneder 1910, 1949; Luna de Carvalho 1972a, 1973;
te Hirashima & Kifune 1974; Teson & Remes Lenicov 1979; Kifune 1983 Kathirithamby
n
a & Johnston unpublished), the rest have been described from free-living males that have
r
g come into traps. Thirty five species of Stichotrema males have been described but only the
e
c host of Stichotrema barrosmachadoi and S. wygotkiwky are known. Of the three Stichotrema
n
e females described all the hosts are known (Kifune 1983). Kifune and Hirashima (1980)
c
r li give a key to twenty eight species of Stichotrema males. This study describes the new
de species Stichotrema robertsoni spec. n. found in Natal, South Mrica, from workers of
un Pheidole sp. (Acc. no. C271) (Formicidae). The host species has not been determined as
y there are no unstylopized major workers. The nest was found in a dune forest in open
a
w dead branches. This is the first record of stylopized worker ants.
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Kathirithamby: first report of stylopi<:ation in minor workers of Pheidole II
).
9
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ublis Figs 1-4. SviEewM ooff vaeendteraalg uvise wo fo fS thicehaodtr eomf na druolbte mrlsaolnei Sstipcehoct.r emn.n r3o: btSrlEsoMni sopfe cm. anl.e 2c: eSpEhMalo othf elactae raolf
P Stichotremn robertsoni spec. n. 4: SEM of stylopized minor worker of Pheidole sp. Arrow -
e male cephalotheca.
h
t
y
b
ed DESCRIPTION
t
n
a Stichotrema robertsoni spec. n., Figs 1-3.
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g
e Male: (Fig. I). Light brown in colour. Head width (including eyes)
c
n 0,37-0,40 mm. Pronotal width 0,23-0,24 mm and is the same as the head between the
e
c eyes. Mandibles small, and maxillary palpi long, rod-shaped (0,12-0,13 mm). Number
r li of ommatidia ± 15.
e
d Antennae 7-segmented with fifth, sixth and seventh segments almost of equal
n
u lengths (fifth = 0,22-0,23 mm; sixth = 0,16-0,18 mm; seventh = 0,20 mm). Fourth
ay segment the shortest (0,02 mm). Third plus flabellum 0,40-0,42 mm; and flabellum
w comes up to the tip of the sixth segment.
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12 J. ent. SOC. stk. Afr. Vol. 54, No. I, 1991
Prescutum length 0,13-0,16 mm; scutellum length 0,05-0,06; postlumbium
length 0,07 mm and width 0,13-0,15 mm; postnotum length 0,18 mm.
Hind wing with only one CuA vein and with no detached veins between R, and
R • MA not reaching wing margin.
5
Aedeagus with no lateral spines or dorsal process. Tip of aedeagus hook-shaped
(Fig. 2).
Total body length and wing expanse are not given as the males were extracted
from the puparium and hence had not excreted the meconium.
Male cephalot/uca: (Fig. 3). Transverse length 0,40 mm, longitudinal length
0,32 mm. Light brown in colour with eyes and mouth parts as shown in Figure 3.
Female: Unknown.
R£marks: This new species closely resembles S. pasteelsi Luna de Carvalho
(1956) from Angola but differs from it in that the fifth, sixth and seventh antennal
segments are almost as long as each other (in S. pasteelsi sixth segment is half the length
of seventh, and sixth and seventh together half the length of fifth); the basal segment of
the maxilla is less than an eighth in length to the pal pi (in S. pasteelsi the palpus is shorter
than the basal segment); MA of wing terminating away from wing margin (in S. pasteelsi
it terminates very near wing margin); and the shape of the lower margin of the tip of the
aedeagus is simple (in S. pasteelsi the lower margin of the tip is S-shaped).
MATERIAL EXAMINED. Holotype <5, SOUTH AFRICA: Natal, Lake Sibayi,
eastern shore 27,22S 32,43E IO.12.86 (Robertson) (in alcohol with cephalotheca) (South
African Museum).
Paratype <5, SOUTH AFRICA: data as above (in alcohol with cephalotheca)
(South Mrican Museum).
).
9
00 HETEROMEROUS HOST RELATIONSHIPS
2
d Heteronomy (where males of parasi to ids have different hosts to the females) is
e
t found in only one family of Strepsiptera. Walter (1983) coined the term heteronomy and
a
d divided it into three types. The simplest form is diphagous parasitism, where the mother
(
r uses the same host species but different oviposition sites for her eggs (males develop as
e
h ectoparasites and females as endoparasites in the same host species). This leads to
s
bli heteromerous hyperparasitism (males develop as hyperparasites at the expense of male
u or female conspecifics, individuals of other species, or both). Lastly, heterotrophic
P
e parasitism, represents a more complex and extreme form of behaviour where the mother
h
t selects a totally different host for the male and female eggs (males develop in totally
by different hosts to the females).
d In Strepsiptera the 1st instar larvae are produced viviparously by the neotenic
e
nt female. On emergence the free-living 1st ins tars that parasitize exopterygote hosts, such
ra as Orthoptera, Mantodea and Hemiptera (except those that live in temporary habitats),
g
e reach their hosts by direct entry, as the nymphs of the hosts are found in the same
nc habitats as the adults. In Strepsiptera that parasitize endopterygote hosts such as ants,
e
c bees and wasps the free-living 1St instar larvae have to be 'carried' into the nest by, for
r li example, a foraging worker bee/ant in order to reach the developing eggs/larvae hidden
e
d in the cells. Evidence for this has been recorded by Young (1987) who found workers of
n
u Camponotus papUil Emery in New Guinea with 1st ins tar larvae of Stichotema dallatorreanum
y clinging to their abdomens, and Luna de Carvalho (I972a) found stylopized Sphodro
a
w mantis lineola pinguis (parasitized by female Stichotrema barrosmachadoi) in Angola being
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Kathirithamby: first report if stylopization in minor workers of Pheidole 13
devoured by ants of Crematogaster sp. (the host of male S. barrosmachadoi). Linsley &
MacSwain (1957) found a phenomenon whereby the 1St instar larvae of Stylops pacifo;us
Bohart were taken into the crop of the bee Andrean complexa Viereck while it visits a
flower. On returning to the nest A. complexa regurgitates the nectar (and the 1St ins tar
larvae) on to the dry pollen ball in the cell and on the cell walls. After completion of
provisioning an egg is laid and the cell is sealed. When the larva of A. complexa hatches
it is parasitized by the 1st ins tar larva of S. pacijicus. The eggs of A. complexa were also
sometimes found to be parasitized.
When the 1st instar enters the host it moults to the 2nd instar, and the
subsequent larval instars undergo apolysis without ecdysis, as in Elenchus tenuicornis
Kirby (Kathirithamby et at. 1984). The 1St ins tar cuticle is readily visible through the
cuticle of the ant host, and of the 47 specimens of Pheidole sp. examined here, only 2 had
more 1st instar cuticles in the host as compared to the number of fully developed male
S. robertsoni larvae/pupae present. All the rest had the same number of 1St instar cuticles
as the number of fully developed male larvae or pupae.
Sexual dimorphism has been reported in the 1St instars of the Myrmecolacidae.
Luna de Carvalho (1972b) described two forms of 1St instars in Stichotrema dallatorreanum.
Kifune (1983) found this also in StichotTema yasumatsui Kifune parasitizing Euscyrtus sp.
(Orthoptera: Gryllidae) in Thailand. If the dimorphism is indeed sexual then most of the
1st ins tars that entered Pheidole sp. must be males.
In the neotenic female strepsipteran the fully developed viviparous 1St ins tar
larvae are found on the outside and the less developed ones in the inside. Hence there
might be a timing sequence in the production of the male and female 1St ins tars in
Myrmecolacidae, although this may raise intriguing questions about the mode of sex
determination. Once the 1st instar larvae emerge a chemical cue might enable them to
9). find an ant to which they could cling, so as to be carried into the appropriate nest.
00 It is fairly common for female hymenopteran parasitoids to develop in large
d 2 hosts and the male in smaller hosts. This is seen for example in various Ichneumonidae,
e particularly species attacking pupae, and in the Aphelinidae (Clausen 1972). Although
t
da it is a totally different situation in Strepsiptera where it is the 1st instar larva that does
r ( the host selection, the type of size difference in the host is a feature of the only properly
he studied case of heteronomy in Myrmecolacidae (Luna de Carvalho 1972a), since the
ublis dfeemvealloe pims einn tt hien ltahrigse rf aomrtihlyo pitse rpaanr tahnedno mgeanlee siins. aMn aanett.a Aetn oatt.h e(ru unpnuubsul.a)l hreapvreo dpurcotvievde
e P experimentally that Stichotrema asakinai Hirashima and Kifune from the subtropical
h Okinawa Island, parasitic in the long-horned grasshopper Mecopoda elongata L., is
t
y parthenogenetic. Until several cases of heteronomy in Myrmecolacidae have been
b
d studied it seems premature to speculate on the evolutionary sequence of heterotrophic
te parasitism in this family, but it is perhaps worth commenting that ants are often the most
n
a constant and abundant insects in a given type of vegetation, offering vast numbers of
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g contact opportunities to strepsipteran 1st instar larvae.
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e SUPERPARASITISM
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r li The occurence of a high percentage of superparasitism (multiple parasites in a
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d host) in a single sample is rare in Strepsiptera, although superparasitism does occur in
n
u low frequencies in Strepsiptera parasitizing hymenopteran hosts. The other instances
y where a high percentage of superparasitism was fairly commonly observed was in
a
w Delphacidae (Homoptera) parasitized by Elenckus vaTleyi Kathirithamby and in Fulgo-
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J. ent. Soc. sth. Afr. Vol. 54, NO.1, 1991
roidae (Homoptera) parasitized by Deinelenchus australiensis Perkins from Brisbane
(Kathirithamby Ig8gb). Two Pheidole sp. had as many as four larvae/pupae of
S. robertsoni indicating that up to three or four larvae may develop simultaneously (Table I).
However, this does not necessarily exclude competition between the larvae. The male
puparia extruded from the intersegmental membranes from both the tergites and stemites
(Fig. 4). Male puparia do not often extrude from the stemites but in ants the abdomen is
held at an angle to the surface due to the petiole and therefore the free-living adult male can
emerge from the puparium without difficulty. Luna de Carvalho (1972a) reports that in
Crematogaster sp. the male puparia extruded only from the dorsal surface.
TABLE I. Number and percentage of instances of host Pheidole sp. showing different degrees of
parasi tism by Stichotrema robertsoni spec. D.
Number of S. robertsonilhost Host Percentage
I larva 8 17,0
2 larva 2,1
3 larva 2,1
I pupa 23 48,9
2 pupae 4 8,5
3 pupae I 2,1
I larva + I pupa 2 4,3
I larva + 2 pupae 5 10,6
I larva + 3 pupae 2 4,3
Total 47
9). ACKNOWLEDGMENTS
0
0 I am most grateful to Dr H. Robertson orthe South African Museum, Cape Town,
2
d for collecting and sending me this most unusual material. My sincere thanks to Dr N.
e
t Waloff and Professor W. D. Hamilton who very kindly commented on the manuscript.
a
d My thanks are also due to Mrs B. M. Luke for the scanning electron micrographs and
(
r for the preparation of the plates for publication, and to the Leverhulme Trust for the
e
h Research Fellowship.
s
bli
u REFERENCES
P
e
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a HOFENEDER, von K. 1910. Stichotrema n. g. Dalla-Torreanum n. sp. Eine in einer Orthoptere
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e g lebende Strepsiptere. Zoologischer Anzeiger 36: 47-49.
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he VOELTZKOW, A. 1890. Faunistische Ergebnisse einer Reise durch das Wituland mit besonderer
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t
y WESTWOOD, J. O. 1861. Notice of the occurrence of a strepsipterous insect parasitic in ants
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t
n YOUNG, G. R. Ig87. Notes on the life history of Stichatrerna dallatorreanum Hofeneder (Strepsiptera:
a
r Myrmecolacidae) a parasite of Segetes decoratus Redtenbacher (Orthoptera: Tettigoniidae)
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e from Papua New Guinea. General and Applied Entomology 19: 57-64.
c
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ce Accepted 18 June 1990.
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