Int. J. Insect Morphol. ~ EmbryoL 6(5/6): 231-238. 1977. Pergamon Press. Printed in Great Britain.

S P E R M A T O P H O R E S O F S O M E A C A R O I D M I T E S

( A S T I G A M A T A : A C A R I N A )

D. A. GRIFFITHS

Pest Infestation Control Laboratory, Ministry of Agriculture, Fisheries and Food, Slough, England

and

J. BOCZEK* Agricultural University of Warsaw, 02-766 Warsaw, Ursynow, Poland

(Accepted 4 May 1977)

Abstract--All species of the genera Acarus and Lardoglyphus and Austroglycyphagus geniculatus produce spermatophores which are directly transferred by inserting an aedeagus into the female copulatory passage. The final shape of the spermatophore, as it appears in the receptaculum seminis, is defined by the shape of the sclerotized "bell- shaped" structure leading into the receptaculum. This form would appear to be specific at the generic level. One mating results in the formation of one spermatophore, so that the number of matings accomplished by the female can be deduced by microscopic examination.

Index descriptors (in addition to those in title): Mites of stored products, Acarus, Lardo- glyphus, Austroglycyphagus.

I N T R O D U C T I O N

SPERM transference in the Acari is accomplished in 2 ways. The male produces a spermato- phore from its genital opening, which is then indirectly transferred into the female opening. Or, the male possesses a sclerotized aedeagus which is inserted into the female copulatory opening, thus bringing about a direct transference of male genital products.

The degree of indirect transference of spermatophores varies. For example, in the Cryptostigmata (Woodring, 1970) and some Prostigmata (Oldfield et at., 1970; Sternlicht and Griffiths, 1974) the male produces a spermatophore which it attaches to a substrate. Later, the female finds and takes it into the genital opening. Many of the Mesostigmata and the Metastigmata employ their mouth parts, particularly chelicerae, for the transference and implantation of the spermatophore (Evans et al., 1961). Woodring and Galbraith (1976) describe this phenomenon as it occurs in a Uropodid mite.

Direct transference of sperm material occurs in several families of the Prostigmata and in all members of the Astigmata. It has always been considered that by this method sperm is transferred directly into the female reproductive system without forming it into any kind of package.

To date, direct sperm transference in these taxa has not been known to include the production of a spermatophore. Herein, we report their existence in species representing 3 families of the Astigmata, all associated with stored products.

* This work was par tially supported by a grant from the USDA (PL480-FG.PO-271).

231

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232 D.A. GRIFVtTHS and J. BOCZEK

M A T E R I A L S A N D M E T H O D S Females of a large number of species of the free living Astigmata were mounted on slides and examined for

the presence of spermatophores by transmitted light, using phase contrast and interference phase contrast microscopy. Live mites were placed into a drop of Heintz mountant and the prepared slide warmed for 24 hr at temperatures not exceeding 40°C. The scanning electron micrographs were obtained on a Cam- bridge Scientific Instruments' microscope, mark 2A. Prior to examination, mites from stock cultares were dried using the critical point technique, then made electron conductive by the application of a molecular layer of gold using the sputter coating method.

T H E F E M A L E R E P R O D U C T I V E S Y S T E M

The female reproduct ive system of one of those genera of As t igmata in which spe rmato- phores have been discovered is depic ted in Fig. 1, ano ther was descr ibed by Griffiths

(1970). The copu la to ry open ing which receives the aedeagus is s i tuated on the dorso- la te ra l pos te r io r marg in o f the op i s thosoma. In the Acar idae and Lardog lyph idae (Fig. 2) the opening is su r rounded by a saucer or funnel -shaped sclerotized disc. In the Glycyphagidae , the opening is t e rmina l and su r rounded by a sclerotized pro jec t ion shaped as in Fig. 3. Dur ing mat ing, the aedeagus is appl ied to and penet ra tes the external opening. The degree o f pene t ra t ion varies between species.

The external opening leads by way of a tube of var iable length and thickness to the

J

A 8

FIG. 1. Austroglycyphagusgeniculatus ~ reproductive system. A. Body mounted dorso-ventrally but internal structures distorted through 90°: external opening (e). leading to tube which passes through sclerotized collar (c) and terminates as a boat-shaped struc- ture (b) opening into thin-walled receptaculum seminis (rs); sclerotized girdle (g)supportingpaired sclerotized openings (f) which lead to ovaries. B. Lateral view showing true orientation of collar

with spermatophore (s) positioned in tube. Scale -- 10 txm.

Spermatophores of Some Acaroid Mites 233

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i

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\ , , - . _ _ , / • - - ° L t ~ - - ~ t

', ~ i ,'

e

FIG. 2. Lardoglyphus konoi ~; External opening to bursa copulatrix. Scanning electron micro- graph (SEM). × 2700

FIG. 3. Austroglycyphagus geniculatus ~; External opening to bursa copulatrix, with spermato- phore tail in opening (SEM). x 1500

Fic~. 4. Acarus siro 9; Reproductive system showing distended pear-shaped receptaculum seminis containing spermatophore tails, x 730

FIG. 5. Schematic diagram of reprodt-ctive system of a free-living astigmatid mite. (e) external opening, (rs). receptaculum seminis, (f) sclerotized opening to (ov) ovaries, (od) oviduct (paired),

(go) genital opening, (p) genital plate.

234 D . A . GRIFFITHS and J. BOCZEK

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2

FIGS. 6 & 7. Austroglycyphagus geniculatus. FIG. 6. Aedeagus (SEM). x 5500; FIG. 7. Spermato- phore tail in opening to bursa copulatrix (SEM). x 5000

FIGS. 8-11. Spermatophores viewed by interference and phase contrast microscopy. FIG. 8. A. genicu[atus, x 2600; FIG. 9. L. konoi, x 1700; FIG. 10. A. siro. x 2000, (interference

phase contrast); FIG. l 1. A. siro. x 1900, (phase contrast).

Spermatophores of Some Acaroid Mites 235

receptaculum seminis. In Acarus, this tube is capable of some expansion. The receptaculum seminis is made up of 2 parts: a sclerotized bell-shaped structure which in turn supports a thin-walled distensible sac. In virgin females the sac is undilated so that the thin wall appears very wrinkled. During mating fluid is transmitted through the aedeagus, along the tube into the sac. With successive matings the sac becomes more inflated reaching its maximum size only after a number of matings have occurred (Fig. 4).

Spermatozoa deposited in the receptaculum seminis reach the paired ovaries by passing through a pair of ducts originating on the edge of the "bell". These ducts are always sclerotized arid often of a characteristic shape for a particular genus. The position of the ducts relative to the sac and their extremely fine lumen suggests that spermatozoa may be drawn into the ovaries by pressure or suction. According to Hughes (1959), the oviducts extend forward and meet in a midline just prior to the uterus which leads to the genital opening (Fig. 5). Eggs develop in either ovary, move through the oviducts and eventually emerge from the genital opening which is situated on the ventral surface between coxae II and IIl.

EMISSION AND FORMATION OF THE SPERMATOPHORE

The mating behaviour for one species of Astigmata (Tyrophagus putrescentiae, Schrank) has been described in detail by Boczek (1975). This species does not produce a spermato- phore but the described pattern of behaviour is generally applicable to other free-living astigmatid mites.

One feature of the mating sequence is that copulatory tube with a fast pumping action. in T. putrescentiae and up to 45 min in Acarus

It is doubtful whether the spermatophore is

the aedeagus is moved back and forth in the The movement can continue for 45-50 min siro and Lardoglyphus konoi. present in its final form in the male, since the

aedeagus is a sclerotized tube with a lumen much narrower than the main body of the spermatophore. In Figs. 6-8 the size of the aedeagal opening of Austroglycyphagus genicul- atus (Vitzthum) is compared with the diameter of the spermatophore tail and the spermato- phore body. Since the maximum diameter of the latter is 5 times that of the aedeagal opening, the male genital products can only be transferred as a fluid under pressure. Presumably, when it reaches the bell-shaped structure, the pressure is released and the fluid expands to fill the bell. At this stage it apparently solidifies to form a spermatophore. We believe the characteristic shape of the spermatophore head (Figs. 8-1l) is produced because the "bell" which has its own specific shape acts as a mould. Figures 9 and 12 indicate how this may occur in L. konoi. Woodring and Galbraith (1976) reported that in a uropodid mite, following direct transference, the spermatophore subsequently takes on the shape of the receptaculum seminis. Their observations supports our view that during deposition the spermatophore is plastic.

After its formation in the "bell", the spermatophore moves into the lumen of the sac of the receptaculum seminis where the mass is released, in A. siro the spermato- phore body breaks down completely, leaving a short characteristic bow-shaped tail (Fig. 4). In L. konoi the spermatophore body shape remains relatively unchanged (Fig. 13). In this case the sperm seems to be released when the anterior margin breaks down (Fig. 9).

SPERMATOPHORE PRODUCTION AND EFFECT ON OVIPOSITION Observations made on virgin pairs of .4. siro and L. konoi show that one complete

mating produces one spermatophore. On average, pairs isolated as virgins and kept together

236 D . A . GRIFFITHS and J. BOCZEK

FIG. 12. Lardoglyphus konoi ~; Sclerotized bell-shaped structure with spermatophore within, illustrating how shape of bell influences shape of spermatophore. Sclerotized opening to ovary

arrowed, x 2320

FIo. 13. Lardoglyphus konoi ~; Reproductive system showing distended receptaculum seminis containing 12 spermatophores and subtended by 2 eggs. x 475

Spermatophores of Some Acaroid Mites 237

for 15 days produced one spermatophore per 24 hr, although variation is considerable. For example, virgin pairs of L. konoi produced under these conditions a maximum of 25 and a minimum of 8 spermatophores. After 6 days all females contained some spermatophores but at 4 days some did not. By contrast, according to Oldfield and Newell (1973), males of Aculus cornutus deposited (indirect transference) an average of 35 spermatophores per day.

Parthenogenesis is unknown in the Astigmata and, for those species studied in the laboratory, it is known that more than one mating is required for maximum egg output. Preliminary experiments have shown that for L. konoi insertion of one spermatophore results in the oviposition of an average of 68 eggs with a maximum of 175 over a period of about 27 days. For .4. siro one mating (one spermatophore) produced anaverage of 78 eggs (maximum 125) over about 23 days and a second mating increased egg production by about 30 eggs.

DISCUSSION

This paper illustrates the form, and describes the emission and possible function of spermatophores in some members of the Astigmata. Hitherto, they have never been found in this order, nor have they been considered to be a feature likely to be possessed by the group.

We have examined a considerable number of species representing all the important genera of stored product Astigmata, and have discovered spermatophores in only 3 of these genera. Spermatophores occur in all 6 species of Acarus so far examined, namely .4. siro L., A. farris (Oudemans), A. immobilis Griffiths, A. nidicolous Griffiths, A. chaetoxy- silos Griffiths and A. graeilis Hughes. Both species of Lardoglyphus, ie. L. konoi (Sasa and Asuma) and L. zaeheri Oudemans have spermatophores, and they are also present in Austroglycyphagus geniculatus (Vitzthum) a species recently transferred from Glyeyphagus by Fain and Lowry (1974) on morphological criteria. This view is further strengthened by the fact that spermatophores have not been found in any of the species of Glycyphagus.

Our observations suggest that where a spermatophore occurs in the Astigmata it is mutually possessed by all species within a genus. Since the general shape of the spermato- phore seems to be similar at the generic level, it may be useful as a generic taxonomic character,

The genus Tyrophagus, which is closely related to Acarus does not possess a spermato- phore. One significant difference between these genera is that in Tyrophagus the shape of the aedeagus varies considerably, to an extent whereby shape is used for specific identi- fication. In all 10 species of Acarus there is no detectable difference in the shape of the aedeagus, which is a short cone-like organ. The uniformity in aedeagus shape exhibited by Aearus spp., compared with the extreme variation in Tyrophagus, may relate to spermato- phore production.

Khalifa (1950) describes the formation and structure of the spermatophore in the moth, Galleria mellonella L. In general shape, formation, deposition in the female and ultimate breakdown the spermatophore of this species closely resemble spermatophores in acarid mites. It is interesting to note that acarid mites and this moth, representing 2 distinct and widely separated classes of arthropods, possess very similar means of spermatophore production.

238 D . A . GRIFFITHS and J. BOC2EK

R E F E R E N C E S

Bocz~K, J. 1975. Reproduction biology of Tyrophagus putrescentiae (Schr.) (Acarina: Acaridae). Proc. I st Int. Work Conf. Stor. Prod. Entomol. Savannah, GA, USA. (Oct. 7-11, 1974): 154-59.

EVANS, G. O., J. G. SHEALS and D. MACFARLANE. 1961. The Terrestrial Acari o f the British Isles. British Museum, London.

FA1N, A. and W. J. LOWRY. 1974. A new genus and two new species of Glycyphaginae from Australia. Bull. Ann. Soe. R. Entomol. Beige. 110: 215-24.

GRIFFITHS, D. A. 1970. A further systematic study of the genus Acarus L,, 1758 (Acaridae: Acarina) with a key to species. Bull. Br. Mus. Nat. Hist. ( Zool.) 19(2): 85-118.

HUGHES, T. E. 1959. Mites or the Acari. London Univ., The Athlone Press, London. KHALIFA, A. 1950. Spermatophore production in Galleria mellonella L. (Lepidoptera). Proc. R. Entomol.

Soc. Lond. (A) 25: 33-42. OLDFIELD, G. N., R. F. HOBZA and N. S. WILSON. 1970. Discovery and characterization of spermatophores

in the Eriophyoidea (Acari). Ann. Entomol. Soc. Amer. 63: 520-26. OLDFIELD, G. N. and I. W. NEWELL. 1973. The role of the spermatophore in the reproductive biology of

protogynes of Aculus cornutus (Acarina: Eriophyidae). Ann. Entomol. Soc. Amer. 66: 160-63. STERNLICHT, M., and D. A. GRIFFITHS. 1974. The emission and form of spermatophores and the fine structure

of adult Eriophyes sheldoni Ewing. (Acarina: Eriophyoidea). Bull Entomol. Res. 63: 561-65. WOODRING, J. P., and C. A. GALBRAITH. 1976. The anatomy of the adult Uropodid Fuscouropoda agitans

(Arachnida: Acari), with comparative observations on other Acari. J. Morphol. 1500): 19-58.