Epifaunistic Parasites of the Four-Striped Mouse, Rhabdomys pumilio, in the Western Cape Province, South Africa Author(s): Sonja Matthee, Ivan G. Horak, Jean-Claude Beaucournu, Lance A. Durden, Eddie A. Ueckermann and Melodie A. McGeoch Source: The Journal of Parasitology, Vol. 93, No. 1 (Feb., 2007), pp. 47-59 Published by: Allen Press on behalf of The American Society of Parasitologists Stable URL: http://www.jstor.org/stable/40058734 Accessed: 15-06-2017 13:54 UTC

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This content downloaded from 157.140.126.17 on Thu, 15 Jun 2017 13:54:42 UTC All use subject to http://about.jstor.org/terms J. ParasitoL, 93(1), 2007, pp. 47-59 © American Society of Parasitologists 2007

EPIFAUNISTIC ARTHROPOD PARASITES OF THE FOUR-STRIPED MOUSE, RHABDOMYS PUMILIO, IN THE WESTERN CAPE PROVINCE, SOUTH AFRICA

Sonja Matthee, Ivan G. Horak*, Jean-Claude Beaucournuf, Lance A. Durdent, Eddie A. Ueckermann§, and Melodie A. McGeoch|| Department of Conservation Ecology and Entomology, Private Bag X1, Stellenbosch University, 7602, South Africa, e-mail: [email protected]

abstract: Flea, lice, mite, and associated with 510 Rhabdomys pumilio were collected at 9 localities in the Western Cape Province, South Africa. The aims of the study were first to quantify the species richness, prevalence, and relative mean intensity of infestation of epifaunistic arthropod species associated with R. pumilio, and second to determine temporal variations in the mean abundance of the parasitic . Each mouse was examined under a stereoscopic microscope and its parasites were removed, identified, and quantified. The epifaunal population was made up of more than 25,000 individuals and included 8 flea, 1 sucking louse, 1 1 mite, and 13 ixodid tick species. Female-biased sex ratios were noted for 9 (30%) of the ectoparasite species. Three undescribed mite and 1 undescribed tick species were recovered, and new locality records for 2 flea, the louse, and 2 mite species were documented. A phoretic host association between a nonparasitic mite species, Psylloglyphus uilenbergi kivuensis, and 3 flea species, Chiastopsylla rossi, Hypsophthalmus temporis, and Listropsylla agrippinae, was recorded. The mean abundance of the parasitic mite and insect species were higher during the cold wet season, whereas were more numerous during the warm dry months. The large number of ectoparasite species on R. pumilio, a locally abundant and regionally widespread species, is of medical and veterinary importance particularly in relation to the transmission of pathogens such as Anaplasma marginale, Babesia caballi, and Babesia canis to domestic ; Rickettsia conori; Yersinia pestis', and the viral disease Crimean-Congo hemorrhagic fever to humans.

Because of their large numbers, short generation intervals, Previous parasitological studies conducted on R. pumilio re- and their capacity for rapid and maintained population growth, corded the intensities and prevalence of ixodid ticks at several small mammals play an important role in maintaining ecosys- localities throughout South Africa, including 1 locality in the tems. It is also evident that the ecology of small mammals is Western Cape (WC) Province (Rechav, 1982; Horak et al., partly driven by parasites, which, in some instances, may di- 1986, 2005; Howell et al., 1989; Horak and Boomker, 1998; rectly be responsible for natural population fluctuations Petney et al., 2004). Most of these studies were conducted at a (Holmes and Price, 1986; Scott, 1987; Hudson et al., 1998; single locality and involved monthly or bimonthly sampling of Torchin et al., 2001). The four-striped mouse, Rhabdomys pum- less than 9 mice per mo (Rechav, 1982; Horak et al., 1986; ilio, is a locally abundant and regionally widespread species Howell et al., 1989; Petney et al., 2004), whereas 1 study in- that occurs endemically throughout southern Africa (De Graaf, volved a single annual sampling of a total of 25 mice over a 1981). It has successfully adapted from natural to urbanized 10-yr time period (Horak and Boomker, 1998). Temporal vari- habitats and may be regarded as a pest species in certain agri- ation in the intensities of infestation of some tick species was cultural areas because of frequent population explosions. Rhab- recorded in 2 studies conducted in the Eastern Cape Province domys pumilio is a host for several species of parasites, but few (Rechav, 1982; Petney et al., 2004). The number of tick species quantitative data are available for its parasite community (Tip- collected during these studies ranged between 1 and 8, and spe- ton, 1960; Zumpt, 1961; De Meillon et al., 1961; Till, 1963; cies composition differed among geographic regions (Horak et Ledger, 1980; De Graaf, 1981; Horak et al., 1986, 2005; Howell al., 1986, 2005; Howell et al., 1989; Petney et al., 2004). Be- et al., 1989; Segerman, 1995; Horak and Boomker, 1998; Pet- tween 3 and 6 species were recovered at 1 locality in the WC ney et al., 2004). Some of the parasites that infest R. pumilio (Horak et al., 1986; Horak and Boomker, 1998), 4 and 6 species are of importance in the etiology of zoonotic diseases in hu- at 2 localities in the Eastern Cape Province (Howell et al., 1989; mans, and they may be involved in the transmission of diseases Petney et al., 2004), and 8 tick species in Free State Province of domestic and wild animals (Walker, 1991). In addition, a (Horak et al., 2005). However, the accuracy of the species rep- survey conducted between 1972 and 1981 of species resentation for the particular geographic region determined by associated with plague in South Africa revealed antibodies to these studies may be confounded by variations in the sample effort as 25 or fewer mice were examined in most of them the plague bacterium Yersinia pestis in R. pumilio and other in the Eastern Cape Province (Shepherd and Leman, (Walther et al., 1995; Poulin and Morand, 2004). 1983). Little is known about the diversity of ectoparasites, especially of fleas, lice, and mites, associated with small mammals in the WC. This region encompasses the Cape Floristic Region (CFR), Received 21 December 2005; revised 25 April 2006; revised 18 July which, because of its high level of plant diversity and ende- 2006; accepted 21 July 2006. mism, is a global biodiversity hot spot (Myers et al., 2000). It * Department of Veterinary Tropical Diseases, Faculty of Veterinary has been suggested that much of the diversity and endemism Science, University of Pretoria, Onderstepoort, 0110, South Africa. associated with this region is due to a heterogeneous topogra- t Laboratoire de Parasitologie et de Zoologie, Faculte de Medecine, 35043 Rennes Cedex, France. phy exposed to cyclic changes during the Pleistocene (Midgley $ Department of Biology and Institute of Arthropodology, Georgia et al., 2005). The rich floral components also support a mag- Southern University, Statesboro, Georgia 30460-8042. nitude of diverse fauna (Picker and Samways, 1996). However, § ARC-Plant Protection Research Institute, Private Bag XI 34, Queens- the likelihood of whether the high plant diversity in this region wood, Pretoria, 0121, South Africa. is mirrored by a high invertebrate diversity, particularly of ec- || Centre for Invasion Biology, Department of Conservation Ecology and Entomology, Private Bag XI, Stellenbosch University, 7602, South toparasites, has received little attention (Picker and Samways, Africa. 1996).

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This content downloaded from 157.140.126.17 on Thu, 15 Jun 2017 13:54:42 UTC All use subject to http://about.jstor.org/terms 48 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 1, FEBRUARY 2007

Table I. Locality information and number of Rhabdomys pumilio (n = 510) examined in the Western Cape Province, South Africa, 2003-2004.

Locality GPS* No. of sites Sample size Sample date

Nature reserves Hottentotsholland 34.05308 S, 19.18311 E 5 42 26 Nov. 2003 Jonkershoek 33.98798 S, 18.95541 E 4 41 4 Sept. 2004 Riverlands 33.29272 S, 18.34436 E 4 24 13 Sept. 2004 Helderberg 34.05678 S, 18.86751 E 3 50 8 Dec. 2003 Elandsberg Res 33.44032 S; 19.05064 E 3 98 16 Feb. 2004 (41, 16, 9, 32)t 1 June 2004 7 Sept. 2004 29 Nov. 2004

Agricultural areas De Rust 34.17366 S, 19.90833 E 5 518 Oct. 2003 Zevenwacht 33.91749 S, 18.73224 E 3 43 3 Nov. 2004 Cordoba 34.03428 S, 18.84764 E 2 57 6 Nov. 2004 Elandsberg Agr 33.44794 S; 19.02741 E 3 104 16 Feb. 2004 (46, 24, 8, 26)t 1 June 2004 7 Sept. 2004 29 Nov. 2004

* GPS = global positioning system. t Number of R. pumilio sampled during February, June, September, and December 2004, respectively.

Using R. pumilio as a model entity, the first aim of this othane study (for R. pumilio) or released at the trap site (any nontarget spe- cies). Each mouse was individually placed in a premarked plastic bag was to quantify the species richness, prevalence, and relative and frozen for later examination. The entire thawed was system- mean intensity of infestation of epifaunistic arthropod atically species examined under a stereoscopic microscope by using forceps to on a small mammal species in the WC. By sampling a remove large ectoparasites. All fleas, lice, mites, and ticks were collected; number of host individuals from 9 localities, we hoped identified to ex- to species, where possible; and counted. Adult ticks were pand the current knowledge of ectoparasites of mammals collected in the from vegetation, from clothes of researchers, or from resident CFR and to provide a comprehensive list of the epifaunistic domestic dogs at some of the study sites. The use of the terms prevalence (the number of hosts infected with arthropod fauna occurring on R. pumilio. The species list1 or also more individuals of a particular parasite species divided by the will supply information on the importance of R. pumilio number as a of hosts examined for that parasite species), relative mean in- host of ectoparasite taxa of veterinary and medical importance. tensity (a standardized comparison of the average intensity of each of As a second aim, we wanted to provide data on temporal the several var- species in the host sample), and species richness (the number iation in the mean abundance of the ectoparasitic taxa of associ-species present in a collection) follows the definitions as outlined in Bush et al. (1997). ated with R. pumilio in the WC. The latter aim not only will give a better understanding of the dynamics of particular ec- toparasite species in this region but also will contribute baseline RESULTS information toward selecting appropriate sampling periods to address macroecological and parasite community ecology Although ques- the aim was to trap 40 or more R. pumilio at each tions. of the 9 localities, this number was unfortunately not possible to achieve at Riverlands, where we only managed to trap 24 MATERIALS AND METHODS mice during a 4-wk trapping period (Table I). Rhabdomys pum- ilio populations are well known to show a strong seasonal fluc- The project was approved and permits were issued by the Ethical tuation in the WC (David and Jarvis, 1985). This fluctuation Committee of the University of Stellenbosch and the Western Cape Nature Conservation Board, respectively. Rhabdomys pumilio was evidentwere in the host density records for the 2 Elandsberg trapped at 9 localities in the WC (a winter rainfall region). The localities, localities with the population reaching its trough in September included 5 pristine lowland Fynbos/Renosterveld regions and followed 4 border- by a summer peak (December-February; Table II), in ing agricultural areas (Table I). The localities all lay within a 200-km agreement with David and Jarvis (1985). Therefore, the host radius. All were approximately 400 m above sea level, and various antelope and small mammal species were associated with each.density Live fluctuation pattern recorded here is considered to be a traps (Sherman-type) with peanut butter and oat bait were used seasonal to trap effect and not a consequence of trapping without re- between 24 and 57 mice per locality during October to December placement. In total, 33 ectoparasite species (representing 17 (spring and summer months; generally dry and warm conditions) in genera) were collected from 510 R. pumilio in the WC (Table 2003 and 2004 (Table I). The aim was to trap 40-60 mice in the shortest time possible at each of the localities. Adult mice (mass > 40 II). g) Ofwere these 510 individuals, 317 were reproductively active mainly sampled during this trapping period. In addition, seasonal adults trap- (187 males, 130 females), and 193 were reproductively ping of R. pumilio was conducted over 8 trap nights (1 trap night nonactive equals adults (98 males, 95 females). The number of tick a 12-hr period) every 3-4 mo (February, June, September, and Decem- species recovered represents 39.4% of the total ectoparasite spe- ber) at 2 adjacent localities within proximity to each other (Table I). The traps were checked daily during each trapping period. cies composition, followed by the mites (33.3%), fleas (24.2%), Once trapped, the animals were identified and either killed withand theFlu- sucking louse (3.1%). Ticks represented 77.7% of the

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Table II. Epifaunistic arthropod species list for 510 Rhabdomys pumilio in the Western Cape Province, South Africa, 2003-2004.

Order Suborder Family/subfamily Species

Fleas Siphonaptera Chimaeropsyllidae Chiastopsyllinae Chiastopsylla numae (Rothschild, 1904) C. rossi (Waterston, 1909) Chimaeropsyllinae Hypsophthalmus temporis (DeMeillon, 1940) Ctenophthalmidae Dinopsyllinae Dinopsyllus ellobius (Rothschild, 1905) D. lypusus (Jordan & Rothschild, 1913) D. tenax (Jordan, 1930) Hystrichopsyllidae Listropsyllinae Listropsylla agrippinae (Rothschild, 1904) Pulicidae Xenopsyllinae Xenopsylla hirsuta group Louse Phthiraptera Anoplura Polyplacidae Polyplax arvicanthis (Bedford, 1919) Mites Parasitiformes Mesostigmata Laelaptidae Laelaptinae Androlaelaps dasymys (Radford, 1939) A. fahrenholzi (Berlese, 1911) Androlaelaps sp. Laelaps giganteus (Berlese, 1918) Laelaps sp. near tillae (Taufflieb, 1959) Laelaps sp. L. paraspinosa (Tipton, 1960) Macrochelidae Macrocheles sp. Macronyssidae Ornithonyssus bacoti (Hirst, 1913) Trombiculidae Uncertain genus (1 specimen) Acariformes Astigmata Winterschmidtiidae Psylloglyphus uilenbergi kivuensis (Fain & Beaucournu, 1976) Ticks Parasitiformes Ixodida Amblyomminae Amblyomma sylvaticum (De Geer, 1778) Haemaphysalinae Haemaphysalis aciculifer (Warburton, 1913) H. leachi (Audouin, 1827) Hyalomminae Hyalomma truncatum (Koch, 1844) Ixodinae Ixodes alluaudi (Neumann, 1913) /. bakeri (Arthur & Clifford, 1961) /. rubicundus (Neumann, 1904) Ixodes sp. Rhipicephalinae capensis (Koch, 1844) R. follis (Donitz, 1910) R. gertrudae group R. lounsburyi (Walker, 1990) R. simus (Koch, 1844)

total number of ectoparasites collected followed by the sucking the third most numerous mite. The 3 new species will be de- louse (12.4%), mites (7.4%), and fleas (2.5%) (Table III). scribed in a separate publication. An unidentified trombiculid Eight flea species belonging to 5 genera were recovered (Ta- (chigger) larva was found on 1 mouse. In addition, chigger ble II). Chiastopsylla rossi was the most numerous flea species larvae also were present on a few mice, specifically anterodor- and was present on 27.5% of the mice. Listropsylla agrippinae sally on the body near the base of the tail. Unfortunately, the was the second most numerous flea followed by Hypsophthal- intensity of infestation and prevalence of these mites were not mus temporis. Female-biased sex ratios were recorded for these recorded. A nonparasitic predatory mite, Macrocheles sp. and 3 species (Table III). a winterschmidtiid mite, Psylloglyphus uilenbergi kivuensis, Polyplax arvicanthis was the only louse species recovered also were present. The mite P. u. kivuensis was phoretically and was present on approximately 60.0% of mice (Tables II, associated with 3 flea species (C. rossi, H. temporis, and L. III). Nymphs (instars I, II, and III combined) were the most agrippinae) collected from 6 mice. Female-biased sex ratios numerous life stage, and the number of female lice exceeded were recorded for all mite species represented by more than 20 that of the males (Table III). individuals. Eleven mite species representing 6 genera were recovered Thirteen ixodid tick species, representing 5 genera, were re- (Table II). Of these species, Androlaelaps fahrenholzi was the covered from the mice (Table II). Ticks of the Rhipicephalus most numerous and was present on 50.2% of R. pumilio. Lae- gertrudae group were the most numerous and prevalent (82.2%; laps giganteus was the second most numerous mite. In addition, Table III). Similar numbers of Haemaphysalis leachi, Hyalom- 3 undescribed mite species were recorded, Androlaelaps sp., ma truncatum, and Ixodes bakeri were recovered, whereas the Laelaps sp. near tillae, and a Laelaps sp. The latter species was prevalence on the rodents of H. leachi, H. truncatum, and the

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Table III. Fleas, lice, mites, and ticks recovered from 510 Rhabdomys pumilio in the Western Cape Province, South Africa, 2003-2004. Proportions for higher parasite taxa are indicated in bold.

Sex ratio Relative mean Ectoparasite species Larvae (%) Nymphs (%) Adults (%) (6*: 9) intensity (%) Prevalence (%)

Fleas 100 1:1.37 2.47 46.7 Chiastopsylla numae 1 00 1:1 0.0 1 0.2 Chiastopsylla rossi 1 00 1 : 1 .27 1.15 27.5 Dinopsyllus ellobius 1 00 1 : 1 .09 0.09 4.5 Dinopsyllus lypusus 100 1:0.75 0.03 1.0 Dinopsyllus tenax 100 1:0.53 0.11 4.5 Hypsophthalmus temporis 100 1:2.40 0.46 15.5 Listropsylla agrippinae 100 1:1.31 0.62 17.8 Xenopsylla hirsuta spp. 100 0:3 0.01 0.4 Louse Polyplax arvicanthis 0 45.30 54.70 1:1.37 12.43 59.2 Mites 0.05 10.63 89.32 1:12.14 7.40 68.2 Androlaelaps dasymys 0 23.08 76.92 1:11 0.3 8.4 Androlaelaps fahrenholzi 0 17.45 82.55 1:8.14 3.75 50.2 Androlaelaps sp. 0 28.57 71.43 1:14 0.08 1.4 Laelaps sp. near tillae 0 2.13 97.87 1:22 0.18 5.9 Laelaps giganteus 0 0.15 99.85 1:128.80 2.5 38.4 Laelaps paraspinosa 0 0 100 0:1 0.004 0.2 Laelaps sp. 0 0.96 99.04 1:50.50 0.4 2.6 Ornithonyssus bacoti 0 0 100 0:2 0.01 0.2 Macrocheles sp. 0 0 100 0:1 0.004 0.2 Trombiculidae sp. 100 0 0 0.004 0.2 Psylloglyphus uilenbergi kivuensis 0 100 0 0.01 1.2 Ticks 91.42 8.30 0.27 1:26.50 77.70 90 Amblyomma sylvaticum 100 0 0 0 0.01 0.2 Haemaphysalis aciculifer 97.60 2.40 0 0 0.01 11.0 Haemaphy sails leachi 93.21 6.79 0 0 6.23 31.4 Hyalomma truncatum 80.20 19.80 0 0 6.04 26.5 Ixodes alluaudi 27.27 27.27 45.45 0:5 0.04 1.8 Ixodes bakeri 75.65 20.81 3.54 1:23.50 5.32 43.0 Ixodes rubicundus 100 0 0 0 0.02 0.4 Ixodes sp. 78.45 21.46 0.09 0:1 4.32 32.4 Rhipicephalus gertrudae group 95.24 4.76 0 0 54.45 82.2 Rhipicephalus lounsburyi 0 100 0 0 0.17 4.7

immature stages of an undescribed Ixodes species was similar (26.5-32.4%). Larvae were the most numerous of the life stages collected (91.4%), followed by nymphs (8.3%). In total, 1,238 adult ticks belonging to 10 species, were collected from the vegetation, researchers' clothing, domestic dogs, an angulate Table IV. Adult ticks collected tortoise, from vegetation,and a shrew human at clothing, the study dogs, sites (Table IV). Of these, a shrew, and a tortoise at ticksthe study of sites.the R. gertrudae group, followed by H. leachi and ticks of the Ixodes pilosus group, were the most numerous. No. of adult ticks collected The seasonal mean abundance and prevalence of 7 fleas Tick species Males Females Total {Chiastopsylla numae, C. rossi, Dinopsyllus ellobius, Dinop- syllus lypusus, Dinopsyllus tenax, L. agrippinae, and Xenop- Amblyomma marmoreum 0 1 1 sylla hirsuta group), the single louse (P. arvicanthis), 1 mites Amblyomma sylvaticum 10 1 11 {Androlaelaps dasymys, A. fahrenholzi, Androlaelaps sp., Lae- Haemaphysalis aciculifer 5 1 6 Hemaphysalis leachi 11 129 206 laps sp near tillae, L. giganteus, Laelaps sp., and Ornithonyssus Hyalomma truncatum 0 1 1 bacoti), and 5 tick species (Haemaphysalis aciculifer, H. leachi, Ixodes alluaudi 0 1 1 H. truncatum, L bakeri, and Ixodes rubicundus) were recorded Ixodes pilosus group 8 52 60 on R. pumilio at 2 of the 9 localities. Because of the proximity Ixodes rubicundus 5 28 33 (<2 km) and high similarity observed in the patterns of parasite Rhipicephalus gertrudae 421 489 916 seasonality between the localities, the temporal data for the 2 Rhipicephalus lounsburyi 2 1 3 localities were combined (there were no significant differences, Total 534 704 1,238 P > 0.05, in the mean abundances of 85% of the parasite spe-

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Figure 1. Temporal variation of the flea Chiastopsylla rossi (A); the sucking louse, Polyplax arvicanthis (B); 2 mites, Androlaelaps fahrenholzi (C) and Laelaps giganteus (D); and 2 ticks, Haemaphysalis leachi (E) and Hyalomma truncation (F), collected from Rhabdomys pumilio in the Western Cape Province, South Africa, 2003-2004. Data from 2 localities (Elandsberg Reserve and Elandsberg Agriculture) are combined. Mean abundance for each parasite species is expressed as the total number of individuals of a particular parasite species collected in a sampling month divided by the total number of mice recorded for the month (sample sizes for February, June, September, and December were 87, 40, 17, and 58, respectively). Standard errors are included.

cies between localities within seasons). In general, it increased seems asin spring and then peaked in early summer (Fig. IE). if infestation with the flea, louse, and mite species wasHigh more mean abundance was recorded for H. truncatum during intense during the cooler and wetter winter and spring the months. early and late summer sampling periods (Fig. IF). This relationship was evident for the 2 most numerous flea spe- cies, C. rossi and L. agrippinae (C. rossi presented in Fig. 1A), DISCUSSION the louse P. arvicanthis (Fig. IB), and the 2 most numerous mite species, A. fahrenholzi and L. giganteus (Fig. The1C, presentD). study has yielded an extensive list of epifaunistic Nymphs of 3 mite species (A. dasymys, A. fahrenholzi, arthropod and species, including obligate ectoparasites and phoret- Androlaelaps sp.) were present during the wet and ically cooler associated species, on R. pumilio in the WC. It is gen- months and absent during the dry and warmer months. erally The accepted that parasite species richness increases with the undescribed species of Laelaps was only present during number spring of hosts examined (Walther et al., 1995; Feliu et al., (September). The remaining flea and mite species (all 1997; present Poulin and Morand, 2004). It, therefore, seems likely that in small numbers) did not show any clear seasonal pattern. the ectoparasite In species richness currently recorded can be at- contrast to the above-mentioned taxa, the mean abundance of tributed to the considerable sampling effort and its intensity H. leachi, 1 of the 2 most frequently collected tick species, (many host individuals at several independent localities within

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Table V. Checklist of ectoparasite species recorded on Rhabdomys pwnilio in South Africa. Locality information is provided where available.

Epifaunistic arthropod species Province Reference

Fleas Chiastopsylla numae'f WC Present study Chiastopsylla rossi WC Present study Chiastopsylla capensis WC Haeselbarth et al., 1966 Chiastopsylla cams WC Haeselbarth et al., 1966 Chiastopsylla coraxis n.a.* Segerman, 1995 Chiastopsylla godfreyi n.a. Segerman, 1995 Chiastopsylla mulleri n.a. Segerman, 1995 Chiastopsylla pitchfordi n.a. Segerman, 1995 Ctenocephalides connatus n.a. Segerman, 1995 Ctenocephalides craterus n.a. Segerman, 1995 Ctenophthalmus calceatus n.a. Segerman, 1995 Ctenophthalmus cophurus n.a. Segerman, 1995 Ctenophthalmus eumeces n.a. Segerman, 1995 Ctenophthalmus singularis n.a. Segerman, 1995 Ctenophthalmus stenurus n.a. Segerman, 1995 Ctenophthalmus verutus n.a. Segerman, 1995 Dinopsyllus abaris n.a. Segerman, 1995 Dinopsyllus echinus n.a. Segerman, 1995 Dinopsyllus ellobius WC Present study Dinopsyllus longifrons n.a. Segerman, 1995 Dinopsyllus lypusus^ WC Present study Dinopsyllus tenax WC Present study Epirimia aganippes n.a. Segerman, 1995 Echidnophaga gallinacean n.a. Segerman, 1995 Hypsophthalmus temporis WC Present study Leptopsylla segnis n.a. Segerman, 1995 Listropsylla agrippinae WC Present study Listropsylla basilewskyi n.a. Segerman, 1995 Listropsylla cerrita n.a. Segerman, 1995 Listropsylla chelura n.a. Segerman, 1995 Listropsylla dorippae n.a. Segerman, 1995 Listropsylla prominens n.a. Segerman, 1995 Nosopsyllus incisus n.a. Segerman, 1995 Pulex irritans n.a. Segerman, 1995 Xenopsylla brasiliensis n.a. Segerman, 1995 Xenopsylla eridos n.a. Segerman, 1995 Xenopsylla hirsuta n.a. Segerman, 1995 Xenopsylla hirsuta spp.f WC Present study Xenopsylla mulleri n.a. Segerman, 1995 Xenopsylla philoxera n.a. Segerman, 1995 Xenopsylla piriei n.a. Segerman, 1995 Xenopsylla versuta n.a. Segerman, 1995 Lice Polyplax arvicanthis WC1 'Present study; Ledger, 1980 Mites Androlaelaps dasymys WC12 'Zumpt, 1961; 2Present study Androlaelaps fahrenholzi G1, WC2 'Zumpt collection^; 2Present study Androlaelaps marshalli n.a. Zumpt, 1961 Androlaelaps sp. WC Present study Euschoengastia alticola KZN Zumpt 1961 Euschoengastia rhabdomyia KZN Zumpt 1961 Haemolaelaps rhabdomys G Zumpt 1961 Laelaps sp. near tillae WC Present study Laelaps giganteus EC, FS', G', KZN1, L', M', NC, 'Zumpt collection^; 2Present study NW',WC2 Laelaps lamborni n.a. Zumpt 1961 Laelaps muricola EC, KZN Zumpt 1961 Laelaps paraspinosa\ WC Present study Laelaps pe re grinus M Zumpt 1961

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Table V. Continued.

Epifaunistic arthropod species Province Reference

Laelaps transvaalensis EC, M Zumpt 1961 Laelaps sp. WC Present study Listrophoroid.es mastomys KZN Zumpt 1961 Macronyssus roseinnesi WC Zumpt 1961 Ornithonyssus bacoti WC Present study Trichoecius hollidayi KZN Zumpt 1961 Trombiculidae sp. WC Present study Ticks Amblyomma hebraeum EC1-2 'Howell et al., 1989; 2Petney et al., 2004 Amblyomma sylvaticunr\ WC Present study Haemaphysalis aciculifer WC12 'Horak and Boomker, 1998; 2Present study Haemaphysalis leachi EC1-2, FS3,WC456 'Howell et al., 1989; 2Petney et al., 2004; 3Horak et al., 2005; 4Horak et al., 1986; 5Horak and Boomker, 1998; 6Present study; Hyalomma rufipesf n.a. Theiler, 1962 Hyalomma marginatum FS Horak et al., 2005 Hyalomma truncatum FS1, WC23 'Horak et al., 2005; 2Horak and Boomker, 1998; 3Present study Ixodes alluaudi WC Present study Ixodes bakeri WC Present study Ixodes rubicundus WC Present study Ixodes sp. a WC Present study Ixodes sp. b FS Horak et al., 2005 Ixodes sp. n. near pilosus WC Horak and Boomker, 1998 Margaropus winthemi FS Horak et al., 2005 Ornithodorus zumpti n.a. Theiler, 1962 Rhipicephalus appendiculatust n.a. Theiler, 1962 Rhipicephalus arnoldi'f n.a. Theiler, 1962 Rhipicephalus follis EC12 'Howell et al., 1989; 2Petney et al., 2004 Rhipicephalus gertrudae group FS1, WC23 'Horak et al., 2005; 2Horak and Boomker, 1998; 3Present study Rhipicephalus glabroscutatum WC Horak et al., 1986 Rhipicephalus lounsburyi FS1, WC23 'Horak et al., 2005; 2Horak and Boomker, 1998; 3Present study Rhipicephalus simus EC1-2 'Howell et al., 1989; 2Petney et al., 2004 Rhipicephalus tricuspis"\ n.a. Theiler, 1962 Rhipicephalus sp. a FS Horak et al., 2005 Rhipicephalus sp. b WC Horak et al., 1986

EC = Eastern Cape Province, FS = Free State Province, G = Gauteng Province, KZN = KwaZulu-Natal Province, L = Limpopo Province, M = Mpumalanga Province, NC = Northern Cape Province, NW = North- West Province, WC = Western Cape Province. * The exact locality data for the presence of the ectoparasite species on R. pumilio is not available (n.a.). t Information from Zumpt Collection, part of Mite Collection of Plant Protection Research Institute, Pretoria (E.A. Ueckermann, pers. comm.). t Accidental infestation.

a single geographic region). mite P.In u. kivuensis,addition, for which new the phoretic habitat host associations heteroge- neity of the WC (Midgley also etwere recordedal., (Fain2005) and Beaucournu, and 1993). the inclusion of both pristine areas and areas Several ofbordering the more numerous ectoparasite agricultural species displayed activities may have contributed to species a strong host-female richness. bias. On-host female-biased Most sex of ratios the are ectopar- asite species that we recovered common among have ectoparasitic previously insects such as fleas and licebeen reported on R. pumilio in the WC (Askew,and 1971; South Marshall, 1981). Africa Marshall (1981) (Table noted that fe- V) (Tipton, 1960; Zumpt, 1961; De Meillon male bias occurred et in al.,70 and 78%1961; of collections Theiler, that included 1962; Till, 1963; Ledger, 1980; De Graaf, 17 species 1981;of Anoplura Horak (sucking lice) etand 108al., species 1986, of Si- 2005; Howell et al., 1989; Segerman, 1995; Horak and Boomker, phonaptera (fleas), respectively. In addition, several studies on 1998; Petney et al., 2004). However, this study makes a valu- small mammals in South Africa have noted a similar pattern able contribution in terms of 3 undescribed mite species (sub- for fleas (Horak and Fourie, 1986; Louw et al., 1993, 1995; family Laelapinae) and 1 tick species {Ixodes sp.), new locality Beaucournu et al., 2003). It has been suggested that this im- records for 2 flea species (C. numae and D. lypusus; Segerman, balance is due to the shorter male life span than that of the 1995), for the sucking louse (P. arvicanthis), a laelapid mite female, mainly because of a higher level of activity, smaller (Laelaps paraspinosa Tipton, 1960), and for the nonparasitic size, more time spent off the host, and a greater sensitivity of

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these male parasites to microclimatic conditions (Marshall, natalensis and the multimammate mouse, Mastomys coucha) 1981; Krasnov, Burdelova et al., 2002; Krasnov, Khokhlova et followed by a recent south-westward range expansion by M. al., 2002). Parthenogenetic reproduction and subsequent female coucha into the WC (Venturi et al., 2004; Avery et al., 2005). bias seems to be common among certain members of another Listropsylla agrippinae and H. tempori were the second and group of ectoparasites, the mammal-infesting ischnoceran lice third most numerous flea species, respectively, on R. pumilio. (Marshall, 1981). Female bias was also present in the mites and In addition to parasitizing R. pumilio, both species also infest in the tick /. bakeri in the present study. The female bias inOtomys species (O. irroratus by the former, and O. unisulcatus mites seems to be related to the specific genetic reproductive by the latter; Segerman, 1995). The presence of 3 female fleas system of the species. Haplodiploidy (males and females that belonging to the X. hirsuta group can be seen as an accidental are somatically haploid and diploid, respectively) and arrhe- infestation, and it is likely that these females belong to the notoky (a haplodiploid system in which males are produced hirsuta subgroup within the hirsuta group. The Cape gerbil (Ta- parthenogenetically but females are biparental) seem to be com- tera afra) has been listed as the only true host of fleas of the mon in laelapid mites, and both these systems are often accom- hirsuta subgroup (Segerman, 1995), which probably explains panied by a strong female bias (Norton et al., 1993). The female the low relative mean intensity of infestation and prevalence on bias in /. bakeri in this study is comparable with that in several R. pumilio in the present study. Although the flea species col- other members of this genus, and Fourie and Horak (1994) and lected in our study do not bite humans, they have the potential Horak and Boomker (1998) have recorded similar patterns for to act as enzootic rodent-to-rodent vectors of Y. pestis, the bac- /. rubicundus and Ixodes sp. (near /. pilosus), respectively. terium responsible for plague, and they thereby facilitate the Within Ixodes, there are nidicolous species that live in or close survival of foci of plague in nonanthropic areas (De Meillon et to caves, burrows, and the nests of their hosts (Sonenshine, al., 1961). Little, if anything, is known of the importance of the 1993). Male nidicolous ticks spend less time on the host, and flea species recovered in the present study as intermediate hosts it seems that, for several of these species, copulation takes place of cestodes and filarial worms in South Africa. Certain flea in or near the host nest (Sonenshine, 1993; Kiszewski et al., species (e.g., Ctenocephalides canis, Ctenocephalides felis, 2001). It would, however, seem that copulation also takes place Nosopsyllus fasciatus, and X. cheopis) can, however, act as in- off the host in some non-nidicolous species, such as /. rubicun- termediate hosts for some of the cestodes that infest dogs, cats, dus and that few males of such species attach to hosts (Fourie and rats (Roberts and Janovy, 2000). and Horak, 1994). The sucking louse, P. arvicanthis, was the only louse species Eight flea species representing 5 genera were recorded in the present on R. pumilio. It occurred at high intensities of infes- present study. These species are largely restricted to South Af- tation and was present on approximately 60% of mice exam- rica, and 7 of these species have previously been recorded in ined. Ledger (1980) records R. pumilio as the preferred host for the WC (Segerman, 1995). Two members of Chiastopsylla were this louse. Although lice have been collected from R. pumilio present, namely, C. numae and C. rossi. Chiastopsylla numae in the WC and at other localities by Horak et al. (1986, 2005), is host specific to Brants' whistling rat, Parotomys brantsii, and Horak and Boomker (1998), and Petney et al. (2004), their spe- its distribution coincides with this rat's distribution (mainly the cific identities were not recorded. The present survey is, there- Karoo area) in South Africa (Segerman, 1995). Its presence on fore, the first empirical study that provides data on the relative R. pumilio represents an accidental infestation. In contrast, C.mean intensity of infestation, prevalence, and temporal varia- rossi was present in large numbers and on more than 20% oftion of P. arvicanthis on R. pumilio in the WC. the host population. This flea is a generalist with a broad host Studies on the mite species that infest wild hosts in southern preference that includes R. pumilio; the vlei rat, Otomys irro- Africa are limited and several are mainly taxonomic in nature ratus; the bush karoo rat, Otomys unisulcatus; and the common (Tipton, 1960; Zumpt, 1961; Till, 1963; Louw et al., 1995; An- highveld gerbil, Tatera brantsii (Segerman, 1995). Three spe- derson and Kok, 2003). The study by Braack et al. (1996) in- cies of Dinopsyllus were recovered. Two of these species, D. cludes an extensive list of parasitic and phoretic-associated mite ellobius and D. tenax, have previously been recorded on R. species (>13 species) that occur on the red veld rat and the pumilio and in the WC (Segerman, 1995). In addition to para- bush veld gerbil (Tatera leucogaster) in the northeastern sum- sitizing R. pumilio, both fleas infest other small mammals such mer rainfall region of South Africa. The results of the latter as gerbils (Tatera sp.), vlei rats (Otomys sp.), and the Natal study and the present study are comparable in that host animals multimammate mouse (Mastomys natalensis). The third species were examined under a stereoscopic dissecting microscope, and in this genus, D. lypusus, is colloquially known as the tropical all the ectoparasites were collected. In the present study, 11 flea, mainly because of its preference for the more tropical areas mite species (including 2 nonparasitic species) were recovered. of southern Africa (Segerman, 1995). In South Africa, it is re- Although mites were collected from R. pumilio examined by stricted to the northern, more tropical, regions of the country Horak et al. (1986), Horak and Boomker (1998), Petney et al. with its most southern distribution recorded as KwaZulu-Natal (2004), and Horak et al. (2005), the species recovered were not (Segerman, 1995). This species seems to favor various small identified to species. mammal species, particularly M. natalensis and the red veld Mostrat of the mites recovered in the present study (A. dasymys, (Aethomys chrysophilus). Its low relative mean intensity A.of fahrenholzi,in- L. giganteus, L. paraspinosa, and O. bacoti) festation on R. pumilio indicates an accidental infestation, seem but to have wide host preferences that include rodents and the presence of both male and female fleas at 3 localities insectivores, (2-3 and also wide geographic distributions in southern individuals per locality) in the WC supports a new locality Africa rec- and Africa or beyond (e.g., A. fahrenholzi) (Tipton, ord for the species. The presence of D. lypusus in the WC 1960; may Zumpt, 1961; Till, 1963). In our study, A. fahrenholzi be due to host switching between sympatric host species was (M. the most numerous mite followed by L. giganteus. The

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latter species is a large mite (female length 1 ,274 ± 24. 1 (Schradin2 u,m) and Pillay, 2003, 2004). Larval stages of ticks are and is generally present posterodorsally near the base of morethe tail susceptible to desiccation than nymphs or adults (Short (Braack et al., 1996). The collection of a single L. paraspinosa et al., 1989a; Solomon and Kaaya, 1998), and the larvae of is probably due to accidental infestation. Nevertheless, someit seems species therefore may spend more of their time at ground as if this is the first record of this species on R. pumilio level as well or in the lower portion of the vegetation compared with as in the WC. Previous records list the vlei rat as the most the adults (Short et al., 1989b; Mejlon and Jeanson, 1997). This common host, and the most southern distribution is noted as behavior could facilitate a higher frequency of contact between the Eastern Cape Province (Tipton, 1960). Three undescribed the larvae and small mammal species such as R. pumilio. The species also were recovered, namely, Androlaelaps sp., Laelaps larvae of some species, however, may have a natural preference sp. near tillae, and a Laelaps sp. The tropical rat mite, O. bac- for rodents and hence quest for hosts from the soil surface or oti, that was also present, is an intermediate host of filarial from vegetation in its proximity. worms, Litomosoides carinii, in some New World rodents. Un- The single Amblyomma sylvaticum larva on R. pumilio can der laboratory conditions, it also can transmit Rickettsia typhi be regarded as an accidental infestation. Walker (1991) noted (murine typhus), R. akari (human rickettsial pox), Coxiella bur- that this tick is commonly associated with reptiles, and specif- netii (Q fever), Y. pestis (plague), Trypanosoma cruzi (Chagas' ically with tortoises and lizards. The 1 1 adult ticks collected at disease), and coxsackie virus (Baker, 1999), but it is not known 1 of the study sites (Table IV) were all present on an angulate whether this mite is a vector of any of these pathogens in na- tortoise (Chersina angulata). ture. The larvae of trombiculid mites (Trombiculidae) are par- Immature stages of H. aciculifer have been recorded previ- asitic and can cause chigger dermatitis, and they act as vectors ously on R. pumilio in the WC (Horak and Boomker, 1998), of the agent of scrub typhus in humans in some Old World and in the current study they were present in low-to-moderate tropical areas such as southeastern Asia and the Pacific region intensities, supporting the supposition that although H. acicu- (Roberts and Janovy, 2000). A recent case study of chigger lifer is widely distributed, it is never encountered in large num- dermatitis on dogs and a child in Free State Province seems to bers (Walker, 1991). Adult H. aciculifer parasitize domestic be the first formal report in South Africa (Heyne et al., 2001). livestock, various antelope, and carnivore species (Walker, Two nonparasitic mite species were collected, Macrocheles 1991). The immature stages of H. leachi also have previously sp. and P. u. kivuensis (Fain and Beaucournu, 1976). The for- been recorded in the WC as well as at other localities in South mer species is generally associated with decaying matter in soil, Africa (Horak and Boomker, 1998; Petney et al., 2004; Horak humus, forest litter, moss, dung, hay, rotting stumps, and also et al., 2005). Adult H leachi parasitize domestic and wild car- nests of rodents, birds, mammals, and bumblebees. The mites nivores (Horak et al., 2000; Horak and Matthee, 2003). Hae- are often phoretic on insects such as flies, beetles, and bees maphysalis leachi seems to be the only species within the genus (Krantz, 1962). Phoresy is a relationship between 2 species in that is economically important in the WC and South Africa, in which 1 species attaches itself to the other species, usually for that it is the vector of Babesia canis, the causative organism of the purpose of transport between hosts or nests (Askew, 1971). canine babesiosis in domestic dogs and of Rickettsia conori, the Phoretic associations seem to be common between heteromor- cause of human tick-bite fever (also known as boutoneusse fe- phic deutonymphs of certain mites and members of ver) the (Walker, Si- 1991). It also can harbor C. burnetii, the causative phonaptera, and they have been recorded in 76 species agent of fleasof Q fever in animals and humans (Walker, 1991). (Fain and Beaucournu, 1993). Hypopial nymphs of P. u. Hyalomma ki- truncatum was present in large numbers (> 1,500 vuensis, which were recovered in the present study, haveindividuals) been and on most R. pumilio at only 2 of the study associated with various flea species on several small localitiesmammal (Elandsberg Reserve and Elandsberg Agriculture). In species in 3 African countries, namely, Zaire, Gabon, a andprevious Ken- study on R. pumilio in the WC, 4 nymphs were ya (Fain and Beaucournu, 1993). The present study documents present on 2 of 25 R. pumilio examined (Horak and Boomker, the first record of a phoretic association between P. u. kivuensis1998), and in the Free State Province a single larva was col- and several flea species in South Africa. Moreover, it alsolected seems from 1 of 36 striped mice (Horak et al., 2005). Most H. that this is the first record of hypopial nymphs on C. truncatum rossi, H. larvae and nymphs were embedded in dermal pits temporis, and L. agrippinae. Interestingly, P. u. kivuensis on the wasanterodorsal part of the body, a finding similar to that only recorded at a locality that is generally wetter than made the otherfor this species on bushveld gerbils (Braack et al., 1996). localities (S. Matthee, unpubl. obs.). The largest proportion The only of adult tick collected from a four-striped mouse was hypopi (50%) was recorded on C. rossi, followed by from25% eachElandsberg Reserve (Table IV). Certain species of Hya- on L. agrippinae and H. temporis. Preference for female lomma fleas are vectors of the virus responsible for Crimean-Congo also was displayed (88% of the hypopi occurred on hemorrhagic female fever (CCHF) in humans (Shepherd et al., 1989; fleas). This finding may be attributed to the abdominal Swanepoel,segments 1998). Since 1982, more than 150 cases of CCHF of female fleas being freer to move than those of males, have whichbeen reported in South Africa, of which more than 50% could facilitate attachment of the hypopl. were associated with tick bites (Anonymous, 2000). Hyalomma Thirteen ixodid tick species, representing 5 genera, truncatum were re- is a vector of Babesia caballi, the causative agent of covered from R. pumilio in the WC. As expected, most equine of thebabesiosis, in South Africa (De Waal, 1990). It also ticks were larvae (Walker, 1991), which may partly beproduces attrib- dermotropic toxins that cause sweating sickness in uted to grooming by the host or to the height at which (Dolanthe and Newson, 1980) and necrotic lesions around various tick life stages quest for hosts (Gallivan and the Horak, bites of adult ticks on dogs (Burr, 1983). 1997). Grooming is more effective in removing the larger Four adult species of Ixodes were recovered. Ixodes bakeri and the stages, and allogrooming by R. pumilio has been immaturereported stages of an undescribed Ixodes sp. were the 2 most

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numerous ticks in this genus. Ixodes bakeri was the fourth most because of the small numbers recovered (1 nymph and 1 larva, numerous tick species and was present on 42.9% of R. pumilio. and 1 nymph, respectively). The large numbers of nymphs col- Walker (1991) noted that /. bakeri occurs throughout the WClected in the present study support the previous findings and and seems to prefer vlei rats (Otomys spp.) and shrews (Cro- indicate the possible importance of R. pumilio as a host for the cidura mariquensis and Myosorex varius) as hosts. As sug- immature stages. Adult R. lounsburyi were collected from the gested by Walker (1991), both adults and immature stages of environment at 2 of the study sites. Rhipicephalus simus is of this tick parasitize rodents. The immature stages of an unde- economic importance and can act as vector for Anaplasma mar- scribed Ixodes species were among the most numerous of the ginale and Anaplasma centrale, both of which cause anaplas- ticks collected and were prevalent in approximately one third mosis in cattle, , and goats (Potgieter and Van Rensburg, of the mice. This finding contrasts with their absence on R. 1987; Walker, 1991). In addition, R. simus can secrete toxins pumilio in all the previous studies (Horak et al., 1986, 2005; that cause paralysis in humans (Walker, 1991). Howell et al., 1989; Horak and Boomker, 1998; Petney et al., In general fleas, lice, and mites were more abundant during 2004). In addition to large numbers of larvae and nymphs of the cool wet months (predominantly June, followed by Septem- this tick, a single female Ixodes, seemingly belonging to an ber), whereas ticks generally preferred the warm dry months undescribed species, also was recovered. Some of the shared (December and February). High temperatures and low humidity taxonomic characters of the immature Ixodes sp. ticks and of may adversely affect the survival of fleas and lice (Askew, this female tick suggest that they may belong to the same spe- 1971; Cooke, 1984; Cooke and Skewes, 1988). Peaks in inten- cies. Both Ixodes alluaudi and /. rubicundus were present at sities during late winter and spring in both summer and winter low intensities. This finding may be explained by the fact that rainfall regions have been noted for the flea Ctenocephalides shrews are the preferred hosts of the former tick (Walker 1991), felis damarensis on scrub hares (Lepus saxatilis) at various lo- and rock elephant shrews (Elephantulus myurus) of the imma- calities in South Africa (Louw et al., 1993, 1995), and essen- ture stages of the latter tick (Fourie et al., 1992). Both ticks are tially during the same seasons for Xenopsylla brasiliensis and present at scattered localities in the WC (Walker, 1991). A sin- Xenopsylla frayi on red veld rats and bushveld gerbils, respec- gle adult /. alluaudi was recovered from a shrew at the Jon- tively, in Mpumalanga Province, a summer rainfall region kershoek study site, and 33 adult /. rubicundus at the Cordoba (Braack et al., 1996). Because the same pattern was recorded and Elandsberg study localities (Table IV). Ixodes rubicundus in both summer and winter rainfall regions, these authors sug- is an economically important tick in that feeding females se- gested that high temperature, rather than low humidity, may be crete a toxin that causes paralysis in domestic sheep, goats, and an important climatic factor in determining the intensity of in- calves as well as in some antelope species (Spickett and Heyne, festation. The predominance of lice in winter followed by 1988; Fourie et al., 1991). spring in the present study is supported by data from a different Rhipicephalus was represented by larvae and nymphs be- host species in a previous study in the WC (Horak et al., 1986). longing to the R. gertrudae group and nymphs of R. lounsburyi. In the latter study, both nymphs and adults of the chewing louse Although the majority of the larvae collected were R. gertru- Damalinia pelea peaked in intensity on grey rhebok (Pelea ca- dae, other larvae similar in appearance to R. gertrudae, namely, preolus) during winter (June), and they were almost completely Rhipicephalus capensis, Rhipicephalus follis, R. lounsburyi, and absent during the warm and dry midsummer months (Horak et Rhipicephalus simus, also were present. Because of the large al., 1986). The same pattern has been observed for lice in stud- numbers of larvae collected (> 13,000 individuals) and the dif- ies on several antelope species in the northeastern summer rain- ficulty in distinguishing between the immature stages of the fall region of South Africa (Horak et al., 1983, 2003; Matthee various species (Walker et al., 2000), the larval data for these et al., 1998). The decline in the relative mean intensity with 5 taxa were pooled. The presence on R. pumilio of immature lice during summer in our study may be related to high tem- ticks of the R. gertrudae group in the present study agrees with peratures during this period (Horak et al., 2003). previous studies on this mouse in the WC and in Free State According to Braack et al. (1996) little information is avail- Province (Horak and Boomker, 1998; Horak et al., 2005). The able on the temporal variation of mite species on wild hosts in immature stages also have been recorded from Namaqua rock southern Africa. Recently, Anderson and Kok (2003) provided mice (Aethomys namaquensis) in the Free State Province (Four- data on 2 mite species associated with the springhare {Pedetes ie et al., 1992). More than 900 adult R. gertrudae were collected capensis) and noted that the immature stages were prevalent at 6 of the 9 study localities (Table IV), implying that a large during the cooler yet dry months. This pattern is similar to that proportion of the questing immature ticks that infested the mice noted in the present study in that nymphs of the 3 Androlaelaps could have belonged to this species. Because murid rodents are species were only recorded in June and September. The 2 most the preferred hosts of the immature stages of R. gertrudae numerous mite species, A. fahrenholzi and L. giganteus in the (Walker et al., 2000), it is not unreasonable to assume that a present study, displayed contrasting seasonal patterns of occur- large proportion of the immature Rhipicephalus spp. collected rence during the cooler months. The mean abundance of the from R. pumilio belonged to this species. Several nymphs of formerR. species peaked in June, followed by a decrease in Sep- lounsburyi were recovered from R. pumilio. Walker (1991) not- tember, whereas the converse was true for the latter species. ed that the preferred hosts of the immature stages of this tick The higher mean abundances of tick larvae in the warmer were as yet unknown. Since then, authors of 1 study in the WC months in the present study are similar to those of several tick (Horak and Boomker, 1998) and another in Free State Province species on rock dassies (Procavia capensis) in the Eastern Cape (Horak et al., 2005) have reported immature stages on R. pum- Province (Horak and Fourie, 1986). Horak et al. (1986) also ilio. In both the latter studies, however, the presence of R. noted an increase in the intensities of infestation with larvae on lounsburyi could be interpreted as due to accidental infestations grey rhebok, bontebok (Damaliscus pygargus dorcas), and

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scrub hares in the WC during February; but in contrast to cation the guide and information source. The Natural History Museum, present study, peak intensities of infestation were recorded London, in U.K., 240 p. Beaucournu, J.-C, I. G. Horak, and L. J. Fourie. 2003. Fleas of April or June. Peak numbers of the immature stages of H. trun-elephant shrews (Mammalia, Macroscelididae), and a new host and catum were collected during the dry summer months (Decem- locality record for Macroscelidopsylla albertyni De Meillon & ber and February) in the present study. In studies on scrub Marcus, 1958 (Siphonaptera, Chimaeropsyllidae). Onderstepoort hares, red veld rats, and bushveld gerbils in a summer rainfall Journal of Veterinary Research 70: 251-253. Braack, L. E. O., I. G. Horak, L. C. Jordaan, J. Segerman, and J. P. region of South Africa, the immature stages were most numer- Louw. 1996. The comparative host status of red veld rats (Aetho- ous during the dry winter months from May to October (Horak mys chrysophilus) and bushveld gerbils (Tatera leucogaster) for et al., 1993; Braack et al., 1996). The absence of immature epifaunal arthropods in the southern Kruger National Park, South stages of H. truncatum on R. pumilio during the wet winter Africa. Onderstepoort Journal of Veterinary Research 63: 149-158. months in the present study could be due to a change in Burr, the E. W 1983. Tick toxicosis in a crossbred terrier caused by Hy- alomma truncatum. Veterinary Record 113: 260-261. seasonality of this tick, ensuring that all its developmental stag-Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Shostak. 1997. es are present during the warm dry summer months. Parasitology meets ecology on its own terms: Margolis et al. re- This study underlines high ectoparasite biodiversity on a visited. Journal of Parasitology 83: 575-583. small mammal host in the CFR of South Africa. Rhabdomys Cooke, B. D. 1984. Factors limiting the distribution of the rabbit flea, Spilopsyllus cuniculi (Dale) (Siphonaptera), in inland South Aus- pumilio is a habitat generalist and its consequent success in both tralia. Australian Journal of Zoology 32: 493-506. pristine natural areas and human-transformed landscapes ex- poses it to by a large number of species. The use of midity on the survival and development of the European rabbit flea, a generalist host species as a model organism in addition to aSpilopsyllus cuniculi (Dale). Australian Journal of Zoology 36: 649-659. relatively high sampling intensity provides us with an indication David, J. H. M., and J. U. M. Jarvis. 1985. Population fluctuations, of the potential parasite diversity that is present on mammals reproduction and survival in the striped fieldmouse Rhabdomys in the CFR. Based on the sampling approach used in this study, pumilio on the Cape Flats, South Africa. Journal of Zoology (Lon- it is evident that a spring-to-early summer sampling period will don) 207: 251-276. yield the broadest representation of ectoparasite species in De the Graaf, G. 1981. The rodents of southern Africa. Butterworths, Dur- ban, South Africa, 267 p. WC. A distinct on-host temporal pattern was evident between De Meillon, B., D. Davis, and F. Hardy. 1961. Plague in southern the fleas, lice, and mites on the 1 hand and the ticks on the Africa, vol. 1. The Siphonaptera (excluding Ischnopsyllidae). Gov- other hand. This study has highlighted the importance of R. ernment Printer, Pretoria, South Africa, 280 p. pumilio as a host for a number of ectoparasite species because De Waal, D. T. 1990. The transovarial transmission of Babesia caballi by Hyalomma truncatum. Onderstepoort Journal of Veterinary Re- of their high prevalence and large numbers. Several of the ec- search 57: 99-100. toparasites that it hosts are of medical and veterinary impor- Dolan, T. T, and R. M. Newson. 1980. Sweating sickness in adult tance in that they have the potential to act as vectors of various cattle. Tropical Animal Health and Production 12: 119-124. organisms that are pathogenic to animals and humans, such asFain, A., and J.-C. Beaucournu. 1976. Trois nouveaux hypopes du A. centrale, A. marginale, B. caballi, B. canis, Y. pestis, and genre Psylloglyphus Fain, phore*tique sur des puces et un Hemi- merus (Acarina: Sarcoptiformes). Revue de Zoologie Africaine 90: the virus that causes CCHF. In addition, adult H. truncatum also 181-187. produce toxins that cause sweating sickness in calves, and ne- crosis around their bites on dogs. Therefore, it is suggested that tiques sur les puces (Siphonaptera) de mammiferes et d'oiseaux. R. pumilio can contribute to a risk of disease especially at times Bulletin de l'lnstitut royal des Sciences Naturelles de Belgique, of high population numbers and when it is present in proximity Entomologie 63: 77-93. Feliu, C, F. Renaud, F. Catzeflis, J.-P. Hugot, P. Durand, and S. to anthropogenic areas. Morand. 1997. A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115: 453-466. ACKNOWLEDGMENTS Fourie, L. J., and I. G. Horak. 1994. The life cycle of Ixodes rubi- cundus (: Ixodidae) and its adaptation to a hot, dry environ- We thank Western Cape Nature Conservation for permits and assis- ment. Experimental and Applied Acarology 18: 23-35. tance with fieldwork and private land owners and managers for involve- ment in the project. We are grateful to A. Fain for identification of the hypopi (P. u. kivuensis) and M. van Rooyen, P. le Roux, C. Kassier, status C. of rock elephant shrews Elephantulus myurus and Namaqua A. Matthee, and C. Montgelard for field and technical assistance. rock The mice Aethomys namaquensis for economically important ticks. project was funded by the National Research Foundation (GUNSouth African Journal of Zoology 27: 108-114. 2053618 and a fellowship to S.M.), University of Stellenbosch, and BIOTA southern Africa. the Karoo paralysis tick Ixodes rubicundus (Acari: Ixodidae) within a false upper Karoo veld type. Experimental and Applied Acarol- ogy 11: 37-49. LITERATURE CITED Gallivan, G. J., and I. G. Horak. 1997. Body size and habitat as Anderson, P. C, and O. B. Kok. 2003. Ectoparasites of springhares determinants in of tick infestations of wild ungulates in South Africa. the Northern Cape Province, South Africa. South African Journal South African Journal of Wildlife Research 27: 63-70. of Wildlife Research 33: 23-32. Haeselbarth, E., J. Segerman, and F. Zumpt. 1966. The arthropod Anonymous. 2000. Crimean-Congo haemorrhagic fever. 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