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Ectoparasitic Community of the Mahali Mole-Rat, Cryptomys Hottentotus

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Ectoparasitic Community of the Mahali Mole-Rat, Cryptomys Hottentotus Fagir et al. Parasites Vectors (2021) 14:24 https://doi.org/10.1186/s13071-020-04537-w Parasites & Vectors SHORT REPORT Open Access Ectoparasitic community of the Mahali mole-rat, Cryptomys hottentotus mahali: potential host for vectors of medical importance in South Africa Dina M. Fagir1* , Nigel C. Bennett1†, Eddie A. Ueckermann2, Alexandra Howard1 and Daniel W. Hart1† Abstract Background: The endemic rodent family of Bathyergidae in Africa, particularly South Africa, are understudied as reservoirs of diseases of signifcant medical importance. Considering the diversity and wide distribution of African mole-rats in South Africa, many of these bathyergids could act as carriers of zoonoses. Methods: The present study assessed the ectoparasite community of the Mahali mole-rat (Cryptomys hottentotus mahali). We aimed to identify possible parasitic arthropods that may infest this mole-rat species and explore host preference, contributions of seasonality, host sex and body mass as well as social class and colony size on ectoparasite assemblage prevalence and abundance. Results: A limited number of ectoparasite species were found on C. h. mahali belonging to two signifcant taxa: mites (Acari) and feas, with mites being the most prevalent and abundant. We recorded the presence of X. philoxera, a fea well known as the principal reservoir of plague in the southern African region on the Mahali mole-rats. Only three mite species were collected: Androlaelaps scapularis, Androlaelaps capensis and Laelaps liberiensis. Seasonal peaks in prevalence and abundance of X. philoxera and A. scapularis were observed during summer. Xenopsylla philoxera abundance and A. scapularis loads signifcantly increased on reproductive mole-rat individuals in comparison to non- reproductive individuals. Conclusion: Despite the wide distribution of the subterranean African mole-rats, studies investigating their para- sitic fauna remain limited and scarce. This dearth in knowledge raises the concern regarding their potential role as an endemic reservoir for zoonotic diseases. Consequently, additional sampling of their ectoparasitic community throughout their distributional range and research addressing their role as a reservoir for zoonotic diseases in south- ern Africa are urgently needed. Keywords: Cryptomys, Mole-rats, Ectoparasites, Seasonality, Fleas, Xenopsylla, Androlaelapid mites, Zoonotic diseases Background Members of the Order Rodentia globally harbour dif- ferent ectoparasitic arthropods, of which many are vec- tors for diseases of medical and veterinary importance *Correspondence: [email protected] [1]. Factors driving parasite prevalence and abundance †Nigel C. Bennett and Daniel W. Hart contributed equally to this work 1 Department of Zoology and Entomology, University of Pretoria, Private patterns may be divided into two general categories, Bag X20, Hatfeld 0028, South Africa environmental factors (abiotic) and host-related factors Full list of author information is available at the end of the article (biotic) [2, 3]. Te diferences in parasite burdens may © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo- main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Fagir et al. Parasites Vectors (2021) 14:24 Page 2 of 9 result from a number of these factors (i.e. abiotic and knowledge and supply an inventory list of the ectopara- biotic) that are not always mutually exclusive, and their sites of the aseasonal breeding Mahali mole-rat. Also, the contributions may be difcult to disentangle [2, 4]. Sea- present study aimed to assess the contributions of host sonal patterns can be linked to the parasite life-cycle and sex, social class, group size and season on the ectopara- how, or to what degree, changes in temperature, rainfall sitic community in the cooperatively breeding Mahali and humidity may afect and/or determine the dura- mole-rat. tion of the developmental stages (i.e. eggs, larva/nymph, adult) in these parasites, as well as the periods, spent of-host by a particular ectoparasite [5–7]. Parasite bur- Methods dens often show a male-biased pattern with males being Te Mahali mole-rat (Cryptomys hottentotus mahali) was infested by more ectoparasites than females [8, 9]. Males captured on smallholdings and farms in and around the tend to be the larger of the sexes in the majority of mam- area of Patryshoek, Pretoria (25° 40′ S, 28° 2′ E), South mal species and to be able to sustain higher parasite num- Africa. Te region of Patryshoek comprises bushveld of bers as they represent more substantial resources [8]. Te South Africa, characterised by cold, dry winters and hot immunosuppressive properties of testosterone, associ- moist summers (South African Weather Bureau). Mahali ated with breeding, could also be a contributing factor mole-rats were caught every month between October to higher male infestation [9–12]. Another host-related 2016 and September 2017. A total of 31 colonies were factor afecting parasite burdens is linked to the degree captured using Hickman live-traps baited with sweet of sociality [13]. Many studies have reported an increase potatoes. Traps were placed at the entrance of excavated in parasite burdens with the increases in group size [14, burrows each month during the capture period and were 15]. In contrast, other studies failed to support this and checked every 2 h from dusk till dawn. Colonies were did not fnd a correlation between parasite burdens and caught in their entirety, and a colony was deemed to be group size [16]. A study by Bordes et al. [17] suggested entirely trapped if no trap activity was observed for 5 that a decrease in ectoparasite loads might be afected consecutive days. Once captured, colonies were trans- by diferent factors such as the host’s environment (e.g. ported back to the mole-rat laboratory at the University temperature, rainfall, number of potential hosts and the of Pretoria, Department of Zoology and Entomology. number of other ectoparasites) as well as increased host Captured animals were housed with their colony mates defence strategies against ectoparasite transmission in in plastic crates (49.5 × 28 cm) with wood shavings and social species [17–19]. Further research is required to paper towelling provided as nesting material. Te mole- disentangle the abiotic and biotic factors afecting dif- rats were fed fresh sweet potato and apples daily until ferences in parasite burdens; this is particularly true in assessed for ectoparasites. All water requirements of the social mammalian species. animals were satisfed in the provisioning of food. African mole-rats (family Bathyergidae) are subter- In the laboratory, animals were weighed and sexed, and ranean hystricomorph rodents with a wide distribu- their reproductive status was determined. Reproductive tional range throughout sub-Saharan Africa [20]. Many males (RMs) were distinguishable from non-reproductive African mole-rat species are deemed pests since they males (NRMs) by their large descended testes and yellow eat the roots of crops and cause property damage due staining around the mouth. Furthermore, the RM was to their tunnel systems. Te Mahali mole-rat, Crypto- the heaviest male within each colony, while NRMs were mys hottentotus mahali, lives in colonies with only one signifcantly lighter [20]. Reproductive females (queens, reproductive female (queen) and up to three potential RFs) were characterised by having prominent axillary reproductive males [20]. Te remaining members of the teats and perforated vaginas, which were not observed in colony are reproductively inactive, with decreased levels the non-reproductive females (NRFs) [32]. of reproductive hormones such as testosterone and per- Individual animals were examined for ectoparasites form alloparental care to the queen’s ofspring [21, 22]. within 5 days of capture, and a modifed wash technique Te members in the colony exhibit allogrooming, which was applied for the assessment of ectoparasite loads could reduce ectoparasite loads, and the movement of [32]. Mole-rats were anaesthetised (to be used in other animals is restricted mainly by rainfall [20, 23]. A large studies) with an overdose of isofurane; subsequently, number of studies have focused on the social system and each individual was washed thoroughly in 100 ml of reproductive physiology of mole-rats [21, 22, 24–26]. warm soapy water in a 22 × 7 × 5-cm tub to remove However, in the southern African region, particularly any ectoparasites. Te washing process was standard- South Africa, very few studies have been carried out on ised for all individuals and involved kneading through parasites of bathyergids with only a limited number of the fur with the fngertips all the way along and around hosts [2, 27–31]. Tus, we aimed to address this dearth of the body length three times before washing the head and Fagir et al. Parasites Vectors (2021) 14:24 Page 3 of 9 the posterior end. Subsequently, individuals were moved investigated using generalized linear models (GZLMs). A back and forth through the water (20 times each side), model with a binomial distribution with a logit-link func- to remove any ectoparasites that remained caught in the tion was selected for prevalence data and a negative-bino- fur.
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