Naturwissenschaften 77,189- 190 (1990) © Springer-Verlag 1990
Phylogeny of Arthropod Immunity
An Inducible Humoral Response in the Kalahari Millipede,
Triaenostreptus triodns (Attems)
E. van der Walt and E. McClain
Department of Physiology, Medical School
A. Puren and N. Savage
Department of Medical Biochemistry, University of the Witwatersrand Medical
School, Parktown 2193, Johannesburg, South Africa
Humoral immunity has been dem-
onstrated in a number of different in-
vertebrates, for example earthworms,
crabs and snails [1]. However, amongst
the arthropods work has focussed on
more highly evolved short-lived species
of insects such as the silk worm, wax
moth, fruit fly and others [2, 3]. Un-
fortunately, information on how ar-
thropods other than insects respond to
bacterial infection is limited. Long-
lived terrestrial arthropods like
scorpions and millipedes may have
evolved different mechanisms for cop-
ing with pathogens.
This paper reports on an inducible anti-
bacterial response to gram-negative
bacteria (E. colt) in the Kalahari mil-
lipede, Triaenostreptus triodus (Diplo-
poda: Spirostreptidae). The potent
humoral response to infection appears
to be similar to that found in short-
lived insects. Although T. triodus
produces several proteins in response to
bacterial challenge as illustrated by po-
lyacrylamide gel electrophoresis, only
one protein expressed bactericidal ac-
tivity when subjected to the gel overlay.
This is the first report of a humoral re-
sponse in a long-lived diplopod. In-
ducible proteins responsible for anti-
bacterial activity in arthropods may
therefore have a long phylogeny.
The Kalahari millipede (Fig. 1) is one of
the most successful arthropod species
in the arid regions of South Africa,
Botswana and Namibia. They are espe-
cially abundant in the Kalahari desert
after rain. Here, these long-lived "Son-
gololos" feed on the newly sprouted
vegetation, especially the leaves and
yellow flowers of Tribulus sp., so com-
monly covering the Kalahari sands.
They also feed on detritus, algae, fungi
and a myriad of small mammal scat
Naturwissenschaften 77 (1990)
found on the desert floor. After surface
activity of about 4 months they return
underground to await next year's rains.
Certainly their life style and feeding
habits are conducive to exposure and
attack from bacteria. In a North
American millipede, Orthoporus or-
natus microbial mortality has been ob-
served [4]. T. triodus is an ideal animal
in which to study immune responses in
the laboratory, as aside from its life
style possibly replete with pathogens,
large quantities of hemolymph can be
sampled from the same individual with-
out harm.
Millipedes were collected at Nossob in
the Kalahari Gemsbok Park, South Af-
rica (20°30"N; 21°50"E). The mil-
lipedes were kept at room temperature
(24°C) in glass aquaria on Kalahari
sand and fed on a diet of rolled oats
and lettuce. Because of the reported
synthesis of wound-healing proteins
upon injection of any pathogen [5] and
the necessity of using pyrogen-free
water and saline to make up all solu-
tions, non-injected as well as saline-in-
jected millipedes were used as controls.
Fig. 1. The Kalahari millipede Triaenos-
treptus triodus, showing both sampling and
injection site (arrowed)
© Springer-Verlag 1990
Saline-injected controls often produced
proteins that were slightly positive on
the gel-overlay method, a phenomenon
also noted by other workers [6]. The
bacterium used was the gram-negative
Escherichia eoli K12. This organism is
commonly used in immune studies. The
bacteria were cultured in 93 x 15 mm
sterile Petri dishes containing either
Nutrient Agar or McConkey Agar
(Merck, Germany). Bacterial suspen-
sions for injection were made up by
scraping the bacteria off the culture
plates with a heat-sterilized spatula and
suspending them in insect saline (0.7 %
w/v NaC1). The bacterial suspensions
were counted under a microscope in
an Improved Neubauer Counting
Chamber (Spencer, Brightline, USA)
under oil. Hemolymph was collected by
inserting a 26G hypodermic needle be-
tween two adjacent segments in the
mid-dorsal region (Fig. 1). Hemolymph
was drained into an Eppendorf tube
kept on ice. Samples were taken at va-
rious time intervals after injection
(24, 48, 72, 96 h). This was done to de-
termine the maximum temporal syn-
thesis of antibacterial proteins. To de-
termine whether any antibacterial activ-
ity was induced by the injection of
E. coli the plate assay technique was
first employed [7]. Specific antibac-
terial activity in the proteins separated
by acidic electrophoresis was detected
by means of a gel overlay [3, 8]. Vac-
cinated and control hemolymph
samples were separated towards the
cathode in a 10% non-denaturing
acidic polyacrylamide gel (pH 4), in
duplicate. After electrophoresis one gel
was incubated in nutrient broth with
0.2 M potassium phosphate buffer pH
7.4 for 1 h. The gel was then overlayed
with nutrient agar which was seeded
with 105 bacteria E. coli K12 per ml.
The gel overlay was incubated at 35 °C
for 24 h to develop zones of inhibition
[3]. The duplicate gel run under
identical conditions was stained to
detect the proteins.
When subjected initially to the plate as-
say method, growth of E. coli was un-
affected by control hemolymph (Fig.
2A). However, hemolymph taken from
a millipede 48 h after infection inhib-
ited E. coli growth (Fig. 2B). This is
seen as a clear zone of inhibition whose
magnitude appears similar to that
found for various vaccinated insect
species subjected to this method [6, 7].
189