J . Liian. SOC.(Zool.), 45, no. 305, p . 209
With 30 tezt-figures
Printed in Great Britain
Descriptions of the hitherto unknown stages of
Parasitus copridis Costa (Acari :Mesostigmata)
with notes on its biology *
BY MICHAEL COSTA?
Kibbutz Mislmar Haemek, Israel
Communicated by G . Owen Evans, F.L.S.
(Accepted far publication M a y 1964)
INTRODUCTION
I n a recent work on the mesostigmatic mites associated with C o p i s hispnus (Coleoptera: Scarabaeidae) in Israel (Costa, 1963), I described the deutonymph of Parasitus
copridis Costa, 1963. As the result of subsequent laboratory studies of this species, I have
obtained the eggs, larvae, protonymphae and adult stages. The present contribution contains descriptions of these stages together with preliminary notes on the biology of the
mite and on the nature of its association with the beetle.
DESCRIPTIONS OF T H E EGG, LARVA, PROTONYMPH A N D ADULTS
Egg :The egg is 325-390 p long and 250 p wide. Its shell is pearly white and shiny. The
shell is covered externally with a whitish sticky substance by which the egg is glued to the
substratum.
Larva :The 6-legged larva is whitish in colour and only weakly sclerotized. The idiosome,
is 470-500 p long and 265-270 p wide (at tho level between coxae I1 and 111).Seventeen
pairs of simple setae are inserted on the dorsum, the 3 posterior marginal pairs are lateroventral in position. Only setae 22 are appreciably longer than the remaining setae and
reach the length of 150 p. Some of the setae, most noticeably 22, are weakly pilose. The
distribution and the relative lengths of the setae are shown in Fig. 1.
The venter bears the usual 3 pairs of sternal setae. Four additional pairs of setae are
inserted on the integument posterior to coxae 111.The adanal setae are 115p long and the
extremely long anal seta reaches 315 p. The venter is figured in Fig. 2. The tritosternum
(Fig. 3) has a long shaft that exceeds the pilose laciniae in length. Two smooth lateral
branches accompany the laciniae.
The gnathosoma (Fig. 4)bears 2 pairs of gnathosomal setae of which g.s.2 is slightly
longer (55 p). Ten rows of minute deutosternal teeth are discernible. The chelicerae
(Fig. 5 ) are well sclerotized, the movable finger bears 3 teeth, the fixed finger bears 4 teeth.
The approximate lengths of the legs (excluding pretarsi) are: 1-585 p ; 11-455 p ;
I I I 4 7 5 p . All the tarsi bear claws andpulvilli. Leg chaetotaxy :Fig. 6 (I,11,111)represents
the actual camera lucida drawings of the legs. As sometimes the leg is not in a strictly dorsoventral position (0.g. the distal part of leg I),the corresponding diagrammatic representation (Fig. 7-I, II, III) is corrected by a n imaginary rolling of the leg into the right position. The larval leg chaetotaxy of P.copridis shows only slight differences in the position
of setae from that of Pergamasus sp. (Evans, 1963).
* This study waa supported by a grant from the General Federation of Jewish Labour in Israel.
t State Teacher’sCollege-Seminar Hakibbutzim ‘Oranim’,P.O.B. Kiryat Tivon, Israel.
MICHAELCOSTA
210
Protonymph: The protonymph is whitish in colour and very little sclerotized. The
idiosoma is 660-735 p long and 395-425 p wide. The anterior dorsal shield does not differ
in the degree of sclerotization from the soft integument and its outlines are discerned only
with difficulty. The shield bears 11 pairs of setae of which i3, r5 (135 p) and 22 (100p ) are
slightly pilose. The distribution and the relative lengths of the setae are shown in Fig. 8.
The most dia.gnosticfeature of the protonymph is its pygidial shield, which is its most
‘ I
5
Figs. 1-5. P . copridis, larva. 1. Dorsum. 2. Venter. 3. Tritosternum. 4. Ventral side of
gnathosoma. 5. Chelicera.
sclerotized structure. The shield is sculptured and the ridges of the ‘scales’ are very prominent. The anterior margin of the shield is only weakly defined. The shield bears 5 pairs of
simple setae. Three small, weakly sclerotized platelets are situated between the anteriordorsal and the pygidial shields. The tectum (Fig. 9) is three-pronged.
The venter is figured in Fig. 10. I n the tritosternum (Fig. 11)the shaft is longer than the
pilose laciniae. Three pairs of sternal setae are present and because of the poor ventral
sclerotization, no sternal shield could be discerned. The anus is situated on a fold, and the
‘anal shield’ is sclerotized only in its posterior margin. The anal fold is flanked by a pair of
Descriptions of Parasitus copridis Costa (Scari: Mesostigmata)
211
adanal setae which are slightly longer than the anal seta. Five pairs of setae are inserted
ventrally between the sternal and the anal area. The very short rudimentary peritreme is
situated opposite coxa IV.
The gnathosoma has the typical shape of the parasitids (Fig. 12), 12 rows of tiny deutosternal teeth could be observed. The chelicerae (Fig. 13) are well sclerotizod, the movable
finger bears 3 teeth, the immovable finger boars a number of small teeth in addition to 1
large central tooth.
The approximate lengths of the legs (oxcluding pretarsi) are: 1-895 p ; 11-605 p ;
111-620 p ; IV-895 p. All the tarsi are provided with claws and pulvilli.
Female: The female is heavily sclerotized, the idiosoma is 1190-1480 p long and 750810 p wide (at its widest line on the posterior dorsal shield). The anterior part of the idiosoma has very pronounced shoulders and parallel sides, it widens considerably posterior to
the dividing line between the anterior and posterior dorsal shields. Both shields are markedly sculptured with scale-like ornamentations. The anterior dorsal shield is fused with the
peritrematal shield which itself is fused with the exopodal and ventral shields (Fig. 18).
I
II
6
111
1
II
111
7
Figs. 6-7. P . copridis, larva. Fig. 6. Legs I, 11, I11 respectively, dorsal view. Fig. 7 .
Diagrammatic representation of the leg chaetotaxy, legs I, 11, I11 respectively.
The anterior dorsal shield bears 23 pairs of setae. Setae il (100p ) , i3 (10.5p) r5 (153p ) and
22 (137 p ) are robust and pilose throughout their length, the remaining setae are needleshaped and most of them are slightly pilose. The distribution and the relative lengt,hsof the
setae are shown in Fig. 14. Two lateral setae are inserted on the soft integument between
the dorsal and the peritrematal shields, the anterior of the 2 setae is often inserted (not in
all the cases) on a small separate shield (Fig. 18).The posterior dorsal shield bears only 1
pair of robust and pilose setae (122p ) on its posterior part, the remaining setae are needleshaped. The setae increase in size and pilosity from the centre of the shield outwards and
backwards. The posterior dorsal shield folds around the sides of the body and forms a
considerable part of the ventral armour, leaving only a narrow strip of integument between
it and the ventral shield (Fig. 17).The tectum is basically three-pronged, it is rather variable in shape (Fig. 15 a, b, c).
The tritosternum has a long shaft, its pilose laciniae exceed the shaft only slightly in
212
MICHAEL
COSTA
length. The sternal shield is devoid of any ornamentation, it bears 3 pairs of simple
setae. In most cases the 1st sternal setae are asymmetricallyforked into 2 unequal branches.
The metasternal shields are separated from the sternal shield only by a fine suture. The
epigynial shield is triangular and has a narrow elongate apex. On its inner surface it bears a
transverse row of about a dozen small blunt teeth, and in front of them it is delicately
13
Figs. 8-13. P . copridis, protonymph. 8. Dorsum. 9. Tectum. 10. Venter. 11. Tritosternum.
12. Ventral side of gnathosoma. 13. Chelicera.
reticulated. The sclerotizationsof the endogynium can be clearly seen through the epigynium, the endogynial ring and its spines are very characteristic (Fig. 19).The genital shield
is demarcated from the ventri-anal shield by fine lines. The ventri-anal shield (Fig. 17) is
irregularly shaped, it bears 9 pairs of setae in addition to the anal setae. The posterior
ventral setae (105p) are robust and pilose throughout their length, they exceed the remaining needle-shapedsetae in length. The adanal setae are inserted near the posteriorend ofthe
anus, the anal seta is robust and pilose. The anal shield projects backwards beyond the
Descriptions of Parasitus copridis Costa (Acari: Mesostigmata)
213
outline of the dorsal shield, and the cribrum is partially folded. The size of the area between
the ventri-anal and the dorsal shields depends on the degree of distension of the mite and is
Figs. 1 6 - 1 7 . P . copridis, female. 14. Dorsurn. 15n, b, c. Variation in shape of tecturn.
16. Ventral side of gnathosoma. 17. Venter.
rather variable. Three pairs of setae are usually inserted on this strip of soft integument,
but the number varies and may be asymmetrical. The well-discernible metapodal shields
are incorporated in the ventri-anal shield. The stigma is situated anteriorly to coxa IV,
the peritrematal tubule extends anteriorly beyond coxa I to the base of the gnathosoma.
The peritrematal shield is fused t o the exopodal and anterior-dorsal shields.
214
MICHAELCOSTA
The gnathosoma is shown in Fig. 16. Setae g.s.1. and g.s.2 are simpleandneedle-shaped;
g.s.3 are exceedingly long and wavy; g.s.4 are slightly flattened and have a ‘broken’ tip.
The corniculi are well sclerotized, the membraneous inner malae have each a long internal
projection and are fringed on the outer border. Ten rows of deutosternal teeth were discernible. The specialized setae of the palp-femur and the palp-genu are simple and spatula
shaped. The movable finger of the chelicera bears 3 teeth, the immovable finger bears a
number of small teeth (Fig. 20).
The approximate lengths of the legs (excluding pretarsi) are: 1-1325 p ; 11-850 p ;
111-940 p ; N-1325 p. AU the tarsi are provided with claws and pulvilli. Each of tarsi
11, I11 and I V bears 4 flattened distal setae.
”;(
21
Figs. 18-22. P. copridis, female. 18. Lateralview, part. 19. Genital region. 20. Chelicera. Male.
21. Tectum. 22. Chelicera.
Male: The male is heavily sclerotized and completely encased in armour. The idiosoma
is 1130-1295 p long and 630-710 p wide. The dorsal shield is divided by a very distinct
suture, without any trace of soft integument between the two parts of the shield. The
shoulders are well pronounced and the sides of the body are parallel, the shield is sculptured
and ornamented similarly to that of the female. Four small strongly sclerotized areas are
discernible near the hind margin of the anterior dorsal shield. The chaetotaxy of the
anterior dorsal shield is similar to that of the female. Setae i l (75 p ) , i3 (81 p ) , r5 (133 p)
and 22 (110 p ) are robust and pilose throughout their length. The setae of the posterior
dorsal shield are simple and needle-shaped, only the more marginal setae are slightly
pilose. The posterior pair of robust setae which is present in the female is absent in the male.
The distribution and the relative lengths of the setae are shown in Fig. 23.
The tectum (Fig. 21) is very different from that of the female. It has a strong median
Descriptions of Parasitus copridis Costa (Acuri: Mesostigmatn)
215
protuberance with two lateral branches, its shape varies only in minor details (shape of the
branches and the anterior margin of the median projection).
The tritosternum of the male is rudimentary, its remnants are situated in front of the
genital aperture (Fig. 24). The sternal and ventral setae are simple and needle-shaped, only
J
26
u
25
27
Pigs. 23-27. P . copridis, male. 23. Dorsum. 24. Venter. 25. Ventral side of gnathosoma.
26. Tarsus 11, ventral. 27. Leg 11, lateral.
the anal seta and a pair of posterior ventral setae (near the front margin of the anal area) are
robust and pilose. Four pairs of pores are distinct in the sternal-metasternal region. The
metapodal area is stronger sclerotized than the remaining ventral armour. Peritremes as in
the female.
216
M~CRAELCOSTA
The gnathosoma (Fig. 25) differs extremely from that of the female. The well sclerotized
corniculi are branched and inserted on very long stalks. The membraneous inner malae are
elongate, they are fringed on their outer margin. All the gnathosomal setae are simple and
needle-shaped, g.s.3 are the longest (118p) and g.s.2 are about half their length. The palptrochanter bears only 1 seta which is inserted on a strongly sclerotized tubercle. Only 7
rows of tiny deutosternal teeth are discernible.
The chelicerae are shown in Fig. 22. The spermatophoral process shows a fine denticulation near its distal attachment to the movable finger. The movable finger bears 1tooth, the
immovable finger bears a row of tiny toothlets posterior to the pilus dentilis.
The approximate lengths of the legs (excluding pretarsi) are: 1-1220 p ; 11-885 p ;
111-955 p ; IV-1295 p. Tarsus I V is very slender and long (425p ) . Leg I1 is armed, the
femur bears a finger-shaped protuberance and a small tubercle, the genu and tibia bear
small tubercles only (Fig. 27). Tarsi 11, I11 and I V bear each 4 flattened setae distally
(Fig. 26).
Notes: The sexual dimorphism of P. copridis is striking and more marked than in other
species of the genus known to me. It is expressed mainly in the following characters : size
and chaetotaxy, shape of tectum, gnathosoma (gnathosomal setae, shape of corniculi and
internal malae, number of rows of deutosternal teeth, shape and chaetotaxy of palptrochanter), development of tritosternum.
ON THE BIOLOGY OF
P. Copidis
The association of the deutonymphal stages of many species of mesostigmatic mites,
mainly Parasitidae and Uropodidae, with insects is well known. The deutonymphs are the
commonest form of many species and are often the only stage known. For that reason
many species of Parasitidae (and Uropodidae) are based on deutonymphs only. I n most
cases not much is known about the nature of the association and our state of knowledge is
summarized by Evans et al. (1963)by the statement : ‘ The majority appear to use the insect
as a means of transport such as the deutonymphal stages ofParasitus, Uropoda, Trichouropoda and Caloglyphus which inhabit dung and other decaying matter frequented by the
host’(p. 173).
The only investigation known to me where the biology of a phoretic mesostigmatic
mite has been worked out is that for Poecilochirus necrophori which is phoretic on Necrophorus humerator. Neumann (1943) has concluded that in nature the deutonymphs of
P. necrophori live as symphorists and paraphages of the beetles, using the beetles as a
means of transport and feeding on fly-maggots and bits of carrion encountered by the host.
Neumannwasable t o obtainall the lifestages ofP. necrophorioffthehost inpetri dishes,and
he concludedthat the duration for the development ofone generation lasted only8-9 days.*
A previous investigation (Costa, 1963) showed a close association between Parasitus
copidis and the scarabaeid beetle Copris hispanus. Eighty-five per cent of the examined
beetles carried deutonymphs, the average infestation being 6.6 deutonymphs per beetle
and a maximal infestation of 37 nymphs on 1 beetle. The first indications of a close
biological association came through some rather spurious observations.
Although the biology of C . hispanus is well known (Lengerken, 1952; Rommel, 1962a)
no reinvestigation of the biology of this species has been done in Israel. C . hispanus is very
common in Israel during the winter months (November-March). I n a n attempt to link the
biology of the host with that ofthe mites, beetles were collected and put into jars filled with
earth and with fresh cow dung added on the top. On the 1.i.1963 a male and a female C .
hispanus with a normal mite count (videCosta, 1963) were put into a culture jar (the mites
were not especially counted, but the population seemed ‘normal’ by a look a t the beetle
* Since this paper was completed, my attention has been drawn t o the excellent account by
Rapp (1957) of the biology of Parasitus coleoptratorum (L. 1758).
Descriptions of Parasitus copridis Costa (Acari: Mesostigmta)
217
through the dissecting microscope). On the 29.i.1963 the beetles were excavated and
examined with the followingresults :
On 8 beetle : P. copridis 95 deutonymphs
P. hispani 2 8, 1
A . halleri 2 dn, 98, 8
C. caputmedusae 1 dn
M . merdarius 1 $!
On
beetle: P. copridis 58 deutonymphs
A . halleri 7 dn, 4 8, 2
A . gurei 2 dn, 2 8
C. caputmedusae 1 protonymph
M . merdarius 7 9
The large increase in the numbers of 1’.copridis within less than 30 days became immediately obvious and puzzled me because no adult mites were observed. A preliminary
attempt to rear the deutonymphs of P. copridis was made. Ten deutonymphs were
isolated in a small culture jar (diameter 45 mm., height 20 mm.) with a close fitting lid.
28
29
30
Figs. 28-30. P . copridis, deutonymphs, semidiagrammatic. 28. Freshly emerged deutonymph
(24 hours old). 29. Male deutonymph. 30. Female deutonymph.
The floor was covered with filter paper and a piece of fresh cow dung was added. I n contrast to Neumann’s observations on P. necropliori nothing happened and after 5 weeks the
deutonymphs were still present without having had moulted. They looked normal and
were active, and although not much is known about their feeding habits they did not seem
to be underfed. During the experiment the dung was changed about every 3 days. After
5 weeks the experiment was abandoned.
I n a later experiment the deutonymphs were kept alive for 79 days under the same conditions until the experiment was discontinued. Although small collembolans were sometimes
added, the mites were never observed feeding a t this stage of the observations. Onlyonce, in
other material, a deutonymph was seen with a smaller mite (?Allipliis) in its chelicerae.
During the experiment i t was easy to count the mites because they tended to stay close
together, usually near the upper rim of the jar or on its lid.
On the 11.v.1963a female C. hispanus was caught a t night with many deutonymphs of
P . copridis adhering to her. The beetle together with the mites were transferred into a small
culture jar and a piece of fresh cow dung was added. Four days later adult mites started to
15
218
MICHAELCOSTA
appear in the culture jar in the following sequence : 15.v.-2 3 ; (16.v.-new dung added) ;
17.v.-2 d ; 19.v.-l d, 1 $2; (2l.v.-beetle transferred into a new jar with fresh dung);
23.v.- 19;24.v.-2 0 ; 26.v.-23. On the 27.v. freshly emerged deutonymphs were observed in the culture for the first time, the earlier stages having been overlooked. The newly
hatched deutonymphs differed strikingly from those I had obtained from the beetle
(Figs. 28,29,30). They are smaller and the dorsal shields cover almost the whole dorsum.
At first they are whitish in colour but with the tanning of the integument they become darker. After several days their colour is reddish-brown and rather dark (andnot light-yellowish as in the deutonymphs obtained from the beetles). The nymphs are very active and
run about with great speed in the culture jar. To the naked eye they resemble in colour
and behaviour the deutonymphs of P. firnetorurn and were a t first actually mistaken for
such. Only the examination of mounted specimens revealed that they were ‘small’ deutonymphs of P. copidis. After that they were easily recognized even under the low magnification of a dissecting microscope, by the extremely long setae on the posterior dorsal
shield. On the 30.v. 2 3 and 3 9 appeared in the culture and small whitish larvae were
observed for the first time. On 31.v. many protonymphs were present in the culture and
until the 2.vi. all had moulted into deutonymphs. On the 4.vi. an additional male emerged
and the beetle was transferred into a new culture jar. On the 9.vi. 4 $2 emerged and the
experiment was discontinued. During the 25 days of the experiment a total of 11 8 and
119 of P. copridis was collected.
The earlier emergence of the males is obvious and might be even the stimulus for the
moulting of the female deutonymph. Neumann (1943) states that the males of P. necrophori copulate successfullyonly with freshly moulted females. This does not seem to be the
case with P. copridis. In a recent series of observations (Winter 1963-64) the copulation of
P . copidis was observed several times. Copulation takes place also between ‘ old’ partners
and could be observed as long as 9 days after the male and the female mites were put
together. Recurrent copulation between the same partners has been observed several times
and it follows in general the description of Karg (Karg, 1 9 6 2 ~ )The
. male follows the
female and tries to climb on to her back. By lateral movements the male tries to reach the
ventral side of the female and upon success his venter is turned against the female venter.
Legs I1 of the male grasp legs IV of the female near their bases and a t the same time
he presses his palps against coxae I11 of the female. The arched legs I of the male are situated between the female gnathosoma and her anterior legs. After having reached this
position the male inserts his chelicerae into the female genital aperture. The spermatophore hasnot beenseen. Copulationlasts about 2 minutes.
The appearance of larvae and their development into deutonymphs showed that the
dung contained sufficient nutriment for the development of the mites. With the addition of
fresh cow dung to soil, a very rich fauna of nematodes and small collembolans soon appears
on the dung-soil interface. As it seemed possible that the mites feed on this fauna or on the
dung, preliminary investigations of their feeding habits were started. As a culture of the
small nematode Panagrellus sp. was a t hand, this species was tried out as food. The nematode, which reaches about 2.5 mm. in length is easily cultured in sour quaker oats or sour
paste products. As the species is viviparous an assortment of many sizes is offered to the
mites. All stages of P. copridis devour the nematodes eagerly, often eating 3 4 nematodes
a t one meal. The chelicerae grasp the nematode a t one end, soon mash it into pulp while
their alternate movements can be easily observed under the dissecting microscope. A
larva of P. copidis may start to feed on a nematode 3-4 times its own size. Panagrellus sp.
is suggested as staple food for laboratory experiments also because it is very hardy: the
nematodes remain alive on the humid plaster of paris of the mite-rearing chamber for
more than a week after having been taken out from the culture medium.
During January, 1964, 2 pairs of P. copridis were isolated in small rearing chambers a t
room temperatures. I n both cases copulation was observed several times, both sexes fed
readily on the nematodes and the females laid oggs. One female lived for 24 days, laying a
Descriptions of Parasitus copridis Costa (Acari: Mesostigmta)
219
total of 33 eggs in the following sequence (per day) which started three days after isolation:
3, 3, 3, 2, 2, 2, 2, 2, 2, 2, 2, 1, 1, 1, 2, 1, 0, 0, 0, 1, 1. The second female lived for 18 days,
layinga totalof43 eggsin the following sequence: 5,5,5,4,4,4,4,2,2,2,1, 1, 1, 1, 0, 1,l.
The males were still alive a t the time of writing, having reached the age of 25 and 35 days
respectively. Hypoaspis aculeifer, in comparison, lays 1 egg per day a t 18"C, a total of 2530 eggs per female (Karg, 1 9 6 2 ~ ) .
The development times of the different stages of P. copridis are summarized in Table 1,
and compared with those of H . aculeifer and P. crassipes (after Karg, 1962b).
Table 1. Development time of P. copridis, H. aculeifer and P. crassipes (in days).
Species
P. copridis
P . crnasipes
H . aeuleifel-
Temp.
OC.
July (room
temperature)
January (room
temperature)
9
Ia 2 0
9
18-20
Egg
Protonymph
Deutonymph
-
1-2
1-2
see text
4-9
5-10
5-8
see text
-
6
18
-
2
P D
4-6
14-37
4-7
11-16
-
-
Larva
3
4 months
6-14
The most interesting fact in the development time of P. copridis is the extreme longevity
of the deutonymph (at summer temperatures), which can only be explained as an adaptation to the biology of the beetle (see below).
Beetles of the subfamily Coprinae are distinguished from other scarabaeids by practising
active broodcare (Imms, 1942). At the beginning of the summer both the male and the
female beetle excavate a breeding crypt and drag down a n amount of fresh dung. After a
lapse of some days the female begins to make pill after pill from the dung. During a week
4-5 pills are made and each of them contains an ogg. The larva, eating its way through the
dung developes inside the pill, pupates, and the imagines lay dormant until the beginning of
the rainy season. The brood-pills are covered by a thin layer of mud which hardens gradually until it is 'stone-hard'. The new adults are apparently unable to break their way
through this hard shell until this is softened by the rain. I n Israel the appearance of the
beetles in numbers coincides with the first rains which penetrate the soil to a depth of
20-5 cm. The structure of the dung-pills is such, that they are 'hermetically' closed, and no
mite can possibly make its way through their outer layer. The presence of mites in the
brood-pills has been expected by me (Costa, 1963)and has been confirmed in a short note by
Rommel(1962b), a paper which reached me only after completing my manuscript.
A t the end of winter 1962 experiments with several couples of beetles were started.
P . copridis infested beetles were put into large rearing glassesand fresh cow dung was added.
If the beetles are active and start to bring dung into the soil, adults of P. copridis can be
found wandering on the dung or the soil within 3-5 days of the introduction of the fresh
dung. Several days later larvae and protonymphs can also be collected. This has been
observed during all seasons of the year.
On the 4.vii.1963 1pair of beetles (actually the only breeding ones during the season) was
found to have had completed its breeding crypt several weeks before. Four brood-pills
were already present, the mite infested female watching them. One pill was opened and
contained a large larva of C. hispanus. Nine deutonymphs of P. copridis were enclosed in
the pill, they w0re very active and photonegative. Although the pill was closed again with
mud, i t cracked and the larva died subsequently.
On the 18.vii. the remaining pills were opened and all of them contained grown larvae.
Two pills contained in addition about a dozen deutonymphs of P. copridis whereas 1 pill
did not containmites. The pillswere closed and sealedwith wet mud. One pill was opened on
the 4.viii-it contained a fully developed pupa of the beetle, t,he deutonymphs were still
present and active.
220
M~CHAEL
COSTA
On the 21.x. the pills were opened again and 3 adult beetles (all rather small females)
were found. The pills had an extremely hard shell and were very dry. One pill had cracked
before, and although the beetle was normal no mites were found. The deutonymphs of
P.copridis are very susceptible to low humidity. Even while on an active beetle in avial,
they dry out and soon die if no wet filter paper is added to the vial. Of the remaining 2 pills
1 contained the beetle only (probably the original mite less pill) and the other contained
about a dozen deutonymphs of P. copridis in addition to the beetle. The beetle became
immediately active and made attempts to walk away with the mites adhering to it. As it
succeeded t o escape during the night, the experiment terminated here. I n this case the
deutonymphs remained enclosed in the pill for a t least 109 days, and probably for a fortnight longer. As the rains during this season started to fall about a month after my opening
the pills, the expected longevity for the deutonymphs of P. copridis seems t o be a t least
140-50 days. The life span of the deutonymphs is of course much shorter when the mites
are brought by the beetles into contact with fresh dung. The minimal life span of the deutonymphs has not been determined yet.
During the rearing experiments a marked mould-depressing influence of the beetles
was noted: fresh dung enclosed in a culture jar was covered within 2 days (July, room
temperature) with a rich growth of mould. Mould never developed in the presence of a
Copris beetle. Wondering if this would have any influence on the development of mites,
some preliminary investigations were made.
The following three conditions were set up on the 19.vii. 1963 in small culture jars:
I-a piece of fresh dung on filter paper ;
11-a piece of fresh dung on a layer of soil;
111-as in I with a Copris beetle included;
all jars were stocked with a dozen deutonymphs of P.copridis. The development was as
follows:
2l.vii.
I-no change;
11-mould starts to develop;
111-3 6 and 1 0 of P.copridis have emerged.
26.vii. I-no change;
I I - d y two deutonymphs have remained alive;
111-additional 1 6 and 1 of P.copridis present.
3l.vii. I-no change;
11-all deutonymphs found dead, covered in fungus mycellia.
111-no change ;
I n a repetition of the experiment mould formation was rather quicker in jar I1and all the
deutonymphs died within 2 days. It seems quite clear that the mites were overcome by the
mould.
I n the breeding jars of the beetles i t sometimes happens that the beetles ignore the fresh
dung and bury themselves immediately. I n spite of this, especially if large numbers of
deutonymphs were present on the beetle, several mites can be seen on the surface of the
dung. I n a case like this, the dung became covered with mould several days after its
introduction to the rearing glass, only the summit of the heap wasstill mould-less.Although
several adults of P.copridis wandered freely on the soil and the dung in spite of the mould,
about halfa dozen deutonymphs were clustered together on the mould free summit. They
remained there for some days and became exceedingly excited by every disturbance (like
lifting the lid of the jar). A portion of the dung was cleaned by scraping the mouldy surface
away and the seemingly fresh dung from underneath was revealed. The deutonymphs
that were clustered together for several days, dispersed immediately and waked all over
the fresh surface.
Descriptions of Parasitus copridis Costa (Acari: Mesostigmnta)
221
The mould depressing effect remains for some time after the removal of the beetle. It is so
strong that a piece of dung which had been associated with a beetle for a week, did not
become attacked by the mould for over 10 days, even after it had been placed in a jar
which was half filled with mould, growing from a piece of dung. A jar was set up with dung
and beetle, after 9 days the beetle was removed. A week later still no mould was present
and 10 deutonymphs of P . copridis were added. During the following 5 days all the nymphs
remained alive and active, but none of them moulted into an adult. A female C o p i s
(without mites) was added and within 3 minutes all the mites had collected upon it. On the
following day 3 6 and 2 9 of P. copridis had emerged. All this points to the conclusion that
the presence of the beetle itself is necessary in order to induce the deutonymphs to moult
into adult mites.
DISCUSSION
Tho close association of P. copridis and C. hispanus has been shown, but many new
problems have arisen and remain unanswered. It is not known a t which stage the mite
enters the brood-pill, nor is it known which factor of the presence of the beetle is necessary
in order t o induce the nymphs to moult into adults. The advantages of this close association are quite clear for the mite: C o p i s beetles are always attracted to fresh dung and by
their activities they depress the formation of mould which seems to be harmful to the mites,
and a t the dung-soil interface develops a rich fauna of nematodes, collembolans and
various other arthropods which may serve as food for the mites. Karg (1961) has investigated the feeding habits of several gamasides and has correlated them with the cheliceral
structure. The structure ofthe chelicera of P. copridis is very similar to that of Pergamasus
miselluswhichisdescribed by Kargasan ‘oligophagousgamaside’t,hatfeedsoncollembolans
and nematodes. It is conceivable that P. copridis has the same feeding habits in nature.
It seems therefore that the mites are always carried by the beetles to the optimal habitat.
The mites escape the dangers of the hot and arid summer by taking refugein the brood-pills
and with the emergence of the adult beetles they are carried to fresh dung heaps where they
are able to reproduce and multiply.
Although it was assumed (Costa, 1963) that Copris hispanus is a specific host for
Parasitus copridis, the following additional hosts have been found during extensive
collecting : Bubas bubalus, Onitis humerosus (both scarabeids) and Hister uncinatus (a
coprophagous histerid). The degree of infestation of these beetles by P. copridis is lower
than that of C. hispanus and their role in the biology of P. copridis has not yet been determined.
SUMMARY
The egg, larva, protonymph, female and male of Parasitus copridis Costa, 1963 are
described and figured. The following are new hosts for the mite: Bubas bubalus, Onitis
humerosus and Hister uncinatus. Preliminary notes are given on the biology of P. copridis
and the nature of its association with Copris hispanus. The mould depressing effect of the
beetle and its influence on the behaviour of P. copridis is noted. The longevity of the deutonymphs of P. copridis was observed to be a t least 109 days and is estimated to be 140-50
days.
ACKNOWLEDQEMENTS
Many thanks are due to Dr G. 0. Evans (British Museum (NaturalHistory) ) for reading
the manuscript.
MICHAELCOSTA
222
REFERENCES
COSTA,
M., 1963. The mesostigmatic mites associated with Coprw hispunus (L.) (Coleoptera, Scarabaeidae) in Israel. J . Linn. SOC.,(Zool.), 45 (303): 25-45.
EVANS,G. O . , 1963. Observations on the chaetotaxy of the legs in the free-living Gamasina (Acari:
Mesostigmata). Bull. Brit. Mus. (nat. Hist.,) Zool., 10: (5): 277-303.
EVANS,G. O., SHEALS,
J. G. & MACFARLANE,
D., 1961. The Terrestrial Acari ojthe British Isles, vol. I,
219 pp. London.
IMMS,
A. D., 1942. A general Textbook ojEntomology, 727 pp. London.
KARG,W., 1961. 6kologische Untersuchungen von edaphischen Gamasiden (Acarina,Parasitiformes).
2. Teil.Pedobiologia, 1 : 77-98.
KARO,
W., 1962a. Rauberkche Milben i m Boden, 64 pp. Wittenberg Lutherstadt.
KARG,W., 1962b. Zur Systematik und postembryonalen Entwicklung der Gamasiden (Acarina,
Parasitiformes)landwirtschaftlich genutzter Boden. Mitt. zool. Mus. Berlin., 68 ( 1 ) : 23-119.
LENGERKEN,
H. VON. 1952. Der Mondhornkajer und seine Verwandten, 57 pp. Leipzig.
RAPP,A. 1957. Zur Biologie und Ethologie der Kafermilbe Parasitus coleoptratorum L. 1758 (Ein
Beitrag zum Phoresie Problem). Zool. Jahrb. Syst. 86 (3-4): 303-66.
ROMMEL,
E., 1 9 6 2 ~ Erniihrungsbiologie
.
und Brutpflegeverhalten des Spanischen Mondhornkiifers
C o p i s hispanus (L.) (Coleopt., Scarab.). Biol. Zentrbl., 80 (3): 327-46.
ROMMEL,
E., 19626. Milbenbefall bei den Mondhornkafern Copris hispanus (L.)und Copria Zunaris (L.)
(Coleopt.,Scarab.). Nachrichtenbkztt der Bayerkchen Entomologen, 11 (12):117-18.
ADDENDUM
After the completion of the manuscript the following observation was made: 20 deutonymphs aged 5-15 days, all reared from eggs, were divided into 2 equal groups. The
nymphs of group I were put on a female Copris hispanus and those of group I1 were put
into a small rearing cell. The development of the nymphs was as follows :
Date
24 February
25
,,
26
,,
27
,,
28
,,
29
,,
1 March
2-5
6
7 ,,
9,
,)
8
,,
,,
9-15
Total
Group I
Start of experiment
2 6.emerged
2 2 emerged
no change
1 6emerged
no change
7,
>7
9,
,>
1 3 emerged
no change
1 6emerged
no change
5 6,
3 ? , 3 dns
Group I1
Start of experiment
no change
*9
1,
Y,
9,
2,
9,
9)
,,
99
7,
39
,,
37
9,
1 8 and 1 0 emerged
no change
This was the first time after many observations that 2 deutonymphs ofP. copridis have
moulted into adults without having had any contact with a Copris beetle. The comparison
between group I and group I1 shows that in group I more deutonymphs moulted earlier
into adults. The deutonymphs of P. copidis tend to concentrate on the beetle in a rather
small area in front of legs I, where they have much contact with each other. As the deutonymphs of group I1 were reared in a rather small rearing cell, it is possible that the stimulation for the emergence of adult mites from the deutonymphs, can be explained in terms of
population density. A series of experiments checking this possibility has now been
initiated.