Oribatid Mites

Onderstepoort Journal of Veterinary Research, 67:49-55 (2000)

Oribatid mites (Acari, Oribatida) as intermediate hosts of tapeworms of the Family Anoplocephalidae (Cestoda) and the transmission of Moniezia expansa cysticercoids in South Africa

R. SCHUSTER1, L. COETZEEz and J.F. PUTTERILL3

ABSTRACT SCHUSTER, R., COETZEE, L. & PUTTERILL, J.F.2000. Oribatid mites (Oribatida) as intermediate hosts of tapeworms of the Family Anoplocephalidae (Cestoda) in South Alrica. Onderstepoort Jour- nal of Veterinary Research, 67:49-55 Six species of adult oribatid miles (Galumna racilis, Kilimabates pilosus, Kilimabatessp., Scheloribates fusifer, Muliercula ngoyensis and Zygoribatula undulata) and two immature stages belonging to the superfamilies Galumnoidea and Ceratozetoidea were isolated from a lawn (mixed Pennlsetum and Cynodonspp.) at OnderstepoortVeterinary lnstitute, South Africa.The mites were subsequently used in an infection trial using Moniezia expansa eggs.Tapeworm cysticercoids were recovered in G. racilis, K. pilosus, Kilimabates sp., S. fusifer, M. ngoyensis and Z. undulata, as well as in immatures of Cera- tozetoidea. The percentage of infected mites was 7,6, 6,3, 16,4, 66,7 ,57,1 , 60,0 and 46,7 "/" respectively. lmmatures of Galumnoidea did not become infected. The highest number of cysticercoids isolated from one individual was six from an adult S. fuslfer. Keywords: lntermediate hosls, Moniezia expansa, oribatid mites, transmission of parasites

INTRODUCTION The involvement of oribatid or "beetle" mites in the life cycle of anoplocephalids was shown for the first The cestode lamily Anoplocephalidae consists of time by Stunkard (1937). Stunkard experimentally more than 165 species of which the following spe- infected Galumna mites with eggs of M.expansaand cies are of veterinary importance: Anoplocephala observed the development of larvaltapbworm stages magna, A. pertofiata, Anoplocephaloides mamillana, in their body cavities. The life cycle was then com- Moniezia expansa, M. benedeni, Avitellina centri- pleted by feeding the cysticercoids to a helminth-free punctata, Stilesia globipunctata, S. hepatica, Thy- raised lamb. saniezia ovilla and Thysanosoma actinoides. (Hiepe, Buchwalder & Nickel 1985; Denegri, Bernardina, A literature survey made by Denegri (1993) showed Perez-Serrano & Rodriquez-Caabeiro 1 998). lhal127 oribatid species belonging to 27 families are known to serve as intermediate hosts to 27 anoplocephalid tapeworm species.

Little is known regarding the role of oribatid mites as 1 transmitters of anoplocephalid tapeworms in Africa. lnstitute for Parasitology and Tropical Veterinary Medicine, The only study on this aspect ol the mites in Africa Freie Universitdt Berlin, Kdnigsweg 67,14163 Berlin, Germany was made by Graber & Gruvel (1969) in Tchad. 2 Department of Acarology, National Museum, PO. Box 266, Bloemfontein, 9300 South Alrica The objective of this study is to determine which 3 Electron Microscopy Unit, Division of Pathology, Onderstepoort species of oribatid mites commonly occuring in cul- Veterinary lnstitute, Private Bag X05, Onderstepoort 0110 tivated grassland, are able to transmit anoplocepha- South Africa lid cestodes as well as the duration and success rate Accepted for publication 22 December 1999-Editor of transmission.

49 Oribatid mites (Acari, Oribatida) as intermediate hosts of tapeworms in South Africa

MATERIALS AND METHODS ber, containing moistened filter paper discs, but with- out lood. The moisture chamber was then stored at lsolation of oribatid mites 4'C in a refrigerator. Examination of the grass cut- ln order to exclude spontaneous infections, oribatid tings in the funnel showed that all mites had lelt the mites were collected from grass samples from an un- grass sample within two days. grazed lawn (mixed Pennisetum and Cynodon spp.) To determine the species of mites, temporary mounts at the Theiler Guesthouse of the Onderstepoort Vet- were made on cavity slides with glycerine and exam- lnstitute, Africa. the erinary South Since trialwas car- ined using a compound light microscope. ried out in the dry winter season in August 1998, the lawn was irrigated 2 d prior to sampling in order to stimulate mites to emerge f rom the soil and enter the Scanning electron microscopy vegetation. Grass samples were cut in the early Ten individuals of each mite species were placed into morning using scissors and transferred to a Berlese fine meshed nylon SEM preparation containers funnel, placed in a sun-lit situation (Fig. 1). A Petri- (Electron Microscopy Sciences, FortWashington, PA placed dish filled with tap water, at the funnel exit, 19034, USA) and sealed. The containers were im- trap for mites from the grass acted as a exiting mersed in boiling water to heat kill the mites after cuttings. which the containers were inserted into the cylinder The Petri-dish was examined for mites twice daily of a 10 cm3 syringe. Treatment solutions were drawn using a stereo microscope. Mites floating on the up into the syringe and after the relevant treatment water surface were transferred to a moisture cham- period, expelled again.

RADIATION

FlG. 1 Scheme of a Berlese funnel for collecting oribatid mites. FIG.2 Scheme of incubation vessels for oribatid mites. 1. Funnel 1. Base of large dish 2. Sieve 2. Base of small dish 3. Petri-dish with water 3. Lid of large dish 4. Substrate (grass sample) 4. Filter paper

50 R. SCHUSTER, L. COETZEE & J.F. PUTTERILL

Specimens were washed twice in a saturated deter- tional two forms of immature mites were found to be gent solution (Krugel & Du Preez 1995) for 90 min Galumnoidea and Ceratozetoidea species, probably in each treatment and rinsed five times in sterile G. racilis and Kilimabafes sp. respectively. double distilled water. Samples were dehydrated through an ascending series of ethanols (50, 70, 90, Adults of G. racilis, Kilimabates sp. and Z. undulata, 95, and 3 X 100%-90 min/step) and then critical as well as immatures of Ceratozetoidea were present point dried from 100% ethanol through carbon diox- in high numbers, while K. pilosus, S. fusifer and M. ngoyensis ide. Specimens were mounted individually onto coni- occurred in moderate densities, and only cal brass viewing stubs. Samples were finally a few specimens of immature Galumnoidea were iso- grass cleaned with a fine single-haired brush and sputter lated from the samples. coated with gold. Mites were viewed individually at The highest percentage of infection of mites exposed an acceleration voltage of 3-8 kV using an Hitachi to M. expansa eggs was found in S. fusifer, Z. undu- 5-2500 Scanning Electron Microscope (Hitachi, To- lata, M. ngoyensisand the immature Ceratozetoidea kyo, Japan). (Table 1). Most infected mites contained low numbers of tapeworm larvae, with the highest burden of six Experi mental i nfection cysticercoids being removed from a specimen of S. fusifer (Table 2). At day 25 aller incubation, it was ln three simultaneous experiments, a suspension of found that all positive mites still harboured tapeworm (n M. expansa eggs = + 10,000), obtained from ter- larvae in the elongated invagination stage, while fully minalsegments of tapeworm strobilae removed from developed cysticercoids (Fig. 3) were only found 28 the small intestine of a naturally infected lamb, was d after incubation.The infected mites did not contain placed onto a disc of moistened filter paper in a Petri- any mite eggs, while low numbers of mite eggs (one dish. Starved mites were then added to the Petri-dish to three) were found in only one third of the adult and remained in contact with the tapeworm eggs for mites which were negative for cysticercoids. one week at room temperature. After this period, 100-150 specimens of each mite species were trans- paper placed ferred onto another filter disc and in the DISCUSSION lid of a large Petri-dish (Fig.2). Mites were restricted to the centre of the filter paper disc by covering them This is the first experimental observation of the in- with a smaller lid of another Petri-dish. Humidity was termediate hosts of M. expansa in South Africa. Data regulated by periodically adding water to the filter reveal for the first time that G. racilis, K. pilosus, Kili- paper. The whole system was covered by the base mabates sp., S. fusifer, M. ngoyensis and Z. undu- of the large Petri-dish and stored in an incubator at latacan act as intermediate hosts for this tapeworm 28'C for four weeks. Pieces of fresh potato and species. Oribatid mites belong to the normal soil humus from the collection site served as food for the fauna of natural terrestrial biotopes or grass lands. mites. Every third day the system was removed f rom the incubator and opened for airing at room temperature for ten min, during which time dead mites were TABLE 1 Percentage of experimentally infected oribatid mites removed. positive tor M. expansa cysticercoids

Mite Number of Number of Percentage Examination of mites for cysticercoids species mites mites with of positive examined cysticer- mites Starting on the 25th day of incubation, mites were coids removed from the moisture chamber and dissected under a stereo microscope. They were transferred Galumna racilis 53 4 7,55 to a drop of water on a slide and crushed using a Galumnoidea dissecting lancet. The content of the body cavity was immatures 28 0 0,0 removed with dissecting needles and examined un- Kilimabates light microscope the 40 X der a using objective. pilosus 48 J 6,25 Kilimabates sp. 55 o 16,36 RESULTS Ceratozetoidea immatures 45 21 46,66 Among the oribatid fauna of the Onderstepoort Vet- Scheloribates erinary lnstitute, representatives of the following six fusifer 42 28 66,66 species were found as adults on a lawn viz., Galum- Muliercula na racilis P6rez-lfrigo, 1987; Kilimabates pilosusMa- ngoyensis 35 20 57,14 hunka, 1985; Kilimabafes sp., Scheloribates fusifer Zygoribatula Berlese, 1908; Muliercula ngoyensls Coetzer, 1968 undulata 35 21 60,00 and Zygoribatula undulata Berlese, 1917. An addi-

51 Oribatid mites (Acari, Oribatida) as intermediate hosts of tapeworms in South Af rica

TABLE 2 Number of M. expansa cysticercoids removed f rom the body cavity of oribatid mites after artif icial infection

Number of cysticercoids per mite Mite species 012

Galumna racilis 49 z 1 1 0 0 0 Galumnoidea immatures 28 0 0 0 0 0 0 Kilimabates pilosus 45 2 1 0 0 0 0 Kilimabates sp. 46 5 4 0 0 0 Ceratozetoidea immatures 24 16 4 1 0 0 0 Scheloribates fusifer 14 10 4 b 5 2 1 Muliercula ngoyensis 15 10 I 1 0 0 0 Zygoribatula undulata 14 14 4 3 0 0 0

FlG. 5 Gnathosoma of Galumna racllis (500 X)

They are absent or occur only in low numbers in cul- tivated fields and gardens (Weigmann 1984; Skubala & Dziuba 1995). The epidemiological role of various oribatid mite species is determined by their susceptibility to tapeworm eggs and the natural occurrence FlG. 3 Fully developed Moniezia expansacyslicercoid removed of mites on pastures. from oribatid mites According to Saldybina (1953) and Kassai & Mahun- ka (1965), the body size, the size of the mouth open- ing and the structure of the mouth-parts are the main attributes of an oribatid mite enabling it to act as an intermediate host for anoplocephalid cestodes. Oribatid mites can only become infected when they mechanically destroy the outer shell of the tapeworm eggs (Caley 1975), while larger mites are able to swallow tapeworm eggs whole (Fig.4, 5, 6, 7). ln the latter case the oncosphera are not able to hatch and the egg passes through the alimentary tract of the mite (Ebermann 1976). This may explain the lower percentage of infected specimens in the larger mites in this sludy, viz., Galumna and Kilimabates. Fig. 4 and 5 show the difference in size of the gnathosoma between S. fusifer (Fig. 4) and G. racilis (Fig. 5). Fig. 5 and 6 show the strongly armoured mouthparts of S. fusifer. The prevalence of infected mites under naturalcon- ditions is usually low and does not exceed 3 % (Prokopic 1962; Ejtminavcjute 1963; Bankov 1965; Kassai & Mahunka 1965; Al'kov 1972; Skorski, Barutzki & Boch 1984; Barutzki & Parwar 1986; Schuster 1988) while under experimental conditions, up to 90% of mites may become infected (Schuster FlG. 4 Gnathosoma of Scheloribates luslfer (500 X) 1988). Since the development of cysticercoids within

52 R. SCHUSTER, L. COETZEE & J.F. PUTTERILL

FlG. 6 Rutella and chelicerae of Scheloribates fusifer (2500 X) FlG. 7 Chelicera of Scheloribates fusifer (4000 X) the intermediate host is a volume demanding proc- firmed these data and showed that, if incubated ess, the number of cysticercoids per mite is limited at 28"C, mites stillhad undeveloped tapeworm and usually does not exceed one to three cysticer- larvae at day 25, while fully developed cysticercoids coids/larvae per individual. More than ten larvae per occurred on d 28. Under natural conditions, and at mite are seldom found (Jurasek 1962). temperatures between 1 6-20'C, the developmental duration is approximately three months (Kuznecov previous Our own investigations confirmed results of 1966). Epidemiological studies on the prevalence of studies that infected mites usually do not carry mite monieziosis in final hosts in Europe showed seasonal eggs (Schuster 1995) or have considerably fewer variations. Moniezia expansa has a high prevalence eggs compared to uninfected control specimens in spring (April to June) while M. benedenl causes (Trowe 1997). However, due to the low infection rate monieziosis in autumn (September to November). of oribatids under natural conditions, the presence According to Andreeva & Akbaev (1993), the infec- of the parasite and its sterilizing effect on the mites, tion peak of final hosts with anoplocephalid cestodes does not influence the mite population. The low fer- depends on the activity of the mites and their pres- tility rate in the current study could be the result of ence in grass after rainfalls in spring and autumn. unfavourably dry conditions at the time of collection. Van Nieuwenhuizen, Verster, Horak, Krecek & Grimbeek (1994) concluded that soil moisture and ln the literature cited, cysticercoids were established temperature interact to increase the relative humid- in adult oribatid mites and only Narsapur (1978) re- ity in the canopy of the vegetation. Apparently this ported the developmenlol Moniezialarval stages in mites to migrate from the to the immature mites. lt was noted that only the nymphal stimulates the soil 'l vegetation during summerwhen soilmoisture is high. stages of Platynothrus peltifer (Koch 839) could be However, they found a significant higher number of infected and not the adult mites. ln our own investi- mites on the vegetation in the early morning than gations immature stages of Ceratozetoidea showed during the rest of the day, and suggested that the a much higher cysticercoid prevalence than the adult mites migrate back into the soil to escape the unfa- stages (genus Kilimabates).This might be explained vourable conditions of midday. Despite irrigation by a lower susceptibility of adult mites in this group. during dry periods, there is an increase in the number The developmental duration of cysticercoids is of mites during summer, when rainlall is high (Van mainly temperature dependant. Narsapur & Prokopic Nieuwenhuizen et a|.1994) and soil moisture seems (1979) suggested that, for experimental purposes, it to be one of the most important environmental fac- was necessary to incubate infected mites at 28"C. tors regulating the vertical movement of the mites Under these conditions, infective cysticercoids are (Metz 1971 ; Sheela & Haq 1991). The risk of infec- available at day 27. Our own investigations con- tion for the final host is therefore greatest during

53 Oribatid mites (Acari, Oribatida) as intermediate hosts of tapeworms in South Africa

months of high rainfall and early in the morning, de Fort-Lamy. Revue d' Etevage et de Mddecine decreasing as the day becomes warmer. V6t6rinaire des PaysTropicaux,22:521-527. HIEPE, T., BUCHWALDER, R. & NICKEL, S. 1985. Veteriniir- It seems as if there is a whole suite of factors influ- medizinische Helminthologie, in Lehrbuch der Parasitologie, encing the success of the various species of oribatid edited by T. Hiepe. Jena: Gustav Fischer Verlag. mites as intermediate hosts of Moniezia, e.g. size of JURASEK, V. 1962. Vyvin moniezii v umele invadovanych ori- the mite (Sengbush 1977;Xiao & Herd 1992), struc- bateidoch (Acarina). Folia Veterinaria. 6:93-1 00. ture of the mouthparts (Caley 1975), habitat preler- KASSAI, T. & MAHUNKA, S. 1965. Studies on tapeworms in ru- ences and behaviour of the mites (Wallwork & Rod- minants. ll. Oribatids as intermediate hosts of Moniezia spe- riquez 1961). This study indicates that under local cies. Acta Veterinaria H u ngarica, 1 5:227 -249. conditions in South Africa, the Oripodoidea(Schelori- KRUGEL, L. & DU PREEZ, L.H. 1995. An evaluation ol methods bates fusifer, Muliercula ngoyensis, Zygoribatula un- suitable for cleaning keratodonts of anuran larvae. Proceed- dulata) is the most successful in terms of suscepti- ings of the Electron Microscopy Society of South Af rica,25:67 . bility to the cysticercoids, although they are not KUZNECOV M.l. 1966. Vospriimcivost'oribatid k onkosferam M. necessarily the most abundant. expansa i M. benedeni I rol' otdel'nych vidov klescej v epizootologii moniezioza. Tematiceskij sbornik rabot po gel'mintologii, 12:97-105.

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