Ectoparasitic community of the Mahali mole-rat, Cryptomys hottentotus mahali: potential host for vectors of medical importance in South Africa.

BACKGROUND: The endemic rodent family of Bathyergidae in Africa, particularly South Africa, are understudied as reservoirs of diseases of significant 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 significant taxa: mites (Acari) and fleas, with mites being the most prevalent and abundant. We recorded the presence of X. philoxera, a flea 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 significantly 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 parasitic 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 southern Africa are urgently needed.

Surveys and Literature Review of Parasites among African Mole-Rats: Proposing Hypotheses for the Roles of Geography, Ecology, and Host Phylogenetic Relatedness in Parasite Sharing.

Hosts that overlap geographically, are less phylogenetically divergent, and/or share similar ecological conditions (e.g., climate, habitat type) are also likely to share parasites. Here we assessed the ectoparasite communities sustained by 3 solitary species of Bathyergidae (Georychus capensis, Bathyergus suillus, and Bathyergus janetta) as well as the endoparasites exploiting G. capensis and compared them with those reported in the literature for other sympatric and parapatric African mole-rat species. In addition to 1 nematode ( Trichuris sp.) and 1 symbiotic ciliate (Meistoma georychi), we collected mites of the genera Androlaelaps and Bathyergolichus as well as unidentified trombiculids from these hosts. Host specificity was high at either the species, genus, or family level for Androlaelaps spp. and Bathyergolichus spp. irrespective of geographic proximity, host phylogeny, or ecological conditions. Host sharing was more limited for helminths but observed among sympatric host species. Our results suggest that ecological similarity and geographic proximity may be more important determinants of host sharing than phylogeny within Bathyergidae.

First Report of Gastrointestinal Parasites from Ansell's Mole-Rat ( Fukomys anselli) in Zambia.

The endoparasite fauna of Ansell's mole-rat, Fukomys anselli (Burda, Zima, Scharff, Macholán and Kawalika) (Rodentia, Bathyergidae), was studied for the first time near Lusaka, Zambia. We recovered 7 endoparasite taxa including 5 nematodes ( Hexametra sp.; Protospirura numidica Seurat, 1914; Protospirura muricola Gedoelst, 1916; Protospirura sp.; and Mammalakis zambiensis Junker, Lutermann and Mutafchiev, 2017 ); and 2 cestodes ( Inermicapsifer sp. and Rodentolepis cf. microstoma Dujardin, 1845) from 272 individuals sampled between February 2009 and February 2010. Species richness (0-2), prevalence (14.7%), and abundance (0.44 ± 0.10) were low, probably as a result of the subterranean lifestyle of the study species. Although effect of host sex on helminth burden was largely absent, helminth burden varied with season and breeding status of the host. This may be a result of seasonal variation in burrow size in response to rainfall, but also the division of labor present in the study species.

The Distribution of Gastrointestinal Parasites in Two Populations of Common Mole-Rats ( Cryptomys hottentotus hottentotus).

The spread of parasites through a host population is based on the variation in behavior and immune function between individuals and is rarely uniform. We studied the gastrointestinal parasites of common mole-rats ( Cryptomys hottentotus hottentotus, Lesson 1826) from 2 sites and assessed the levels of infection based on host sex, breeding status, and season. Only nematode species were found: Neoheligmonella sp. and Mammalakis macrospiculum (Ortlepp, 1939) and a single specimen of Trichuris sp., all of which have direct life cycles. Parasite burden and species richness was greater in the mesic habitat. The abundance of Neoheligmonella sp. differed significantly between seasons, and the season of peak abundance differed between sites, perhaps due to differences in host densities between sites. In addition, parasite burden did not differ between the sexes, but breeding animals had higher infections of Neoheligmonella sp. and M. macrospiculum than non-breeding animals. This and previous studies thus suggest that the subterranean environment is beneficial in reducing parasite diversity, although the restrictions on movement may lead to certain individuals suffering higher parasite burdens.

A new ascaridid nematode, Mammalakis zambiensis n. sp. (Heterakoidea: Kiwinematidae), from the mole rat Fukomys anselli (Burda, Zima, Scharff, Macholán & Kawalika) (Rodentia: Bathyergidae) in Zambia.

Mammalakis zambiensis n. sp. is described from the large intestine and caecum of Fukomys anselli (Burda, Zima, Scharff, Macholán & Kawalika), a bathyergid rodent endemic to Zambia. Morphological data for comparison with its three congeners, M. macrospiculum (Ortlepp, 1939), M. spalacis (Marcu, 1930) and M. spalaxi (Kozlov & Jangolenko, 1962) are provided. Based on studies of the type-material, observations of hitherto undescribed morphological characters of M. macrospiculum, a parasite of Bathyergus suillus (Schreber) (Hystricomorpha: Bathyergidae) in South Africa, are presented. To date, the generic diagnosis of Mammalakis Inglis, 1991 is based largely on characters of its type-species, M. macrospiculum. In having three rounded lips, not set-off from the body, a stout oesophagus with a flask-shaped posterior bulb, lateral alae that broaden on the level of the precloacal sucker and cloaca, and mature eggs with a smooth shell, M. zambienis n. sp. corresponds to the characters of the genus. However, the presence of lips with anterior flanges that were observed in M. zambiensis n. sp., and also for the first time in M. macrospiculum, are in contrast with the current diagnosis of Mammalakis. Further studies will be needed to determine if an amendment of the generic diagnosis is indicated.

Digging for answers: contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal.

Due to the density-dependent nature of parasite transmission parasites are generally assumed to constrain the evolution of sociality. However, evidence for a correlation between group size and parasite burden is equivocal, particularly for mammals. Host contact rates may be modified by mobility of the host and parasite as well as social barriers. In the current study, we used the common mole-rat (Cryptomys hottentotus hottentotus), a social subterranean rodent, as a model system to investigate the effect of host density and frequency of contact rates on ectoparasite burdens. To address these factors we used a study species that naturally varies in population densities and intergroup contact rates across its geographic range. We found that ectoparasite prevalence, abundance and species richness decreased with increasing host density at a regional scale. At the same time, measures of parasite burden increased with intergroup contact rates. Ectoparasite burdens decreased with colony size at the group level possibly as a result of increased grooming rates. Equating group size with population density might be too simplistic an approach when assessing parasite distributions in social mammals. Our data suggest that frequency-dependent mechanisms may play a much greater role at a population level than density-dependent mechanisms in determining parasite distributions in social species. We suggest that future studies should explicitly consider behavioural mechanisms that may affect parasite distribution.

Ectoparasite Burdens of the Damaraland Mole-Rat (Fukomys damarensis) from Southern Africa.

Damaraland mole-rats (Fukomys damarensis) of the family Bathyergidae are widely distributed subterranean rodents in sub-Saharan Africa. No parasites have ever been reported for this species and only 1 ectoparasite is described for the entire genus. In the current study ectoparasites were collected from individuals captured at 3 localities in South Africa and Namibia to document the ectoparasite community of F. damarensis, investigate their aggregation patterns, and evaluate the influence of season on ectoparasite burden. A total of 2,071 arthropods from 9 mite taxa and 1 louse species (Eulinognathus hilli) were collected from 293 hosts sampled. Of these, 5 mite species (Androlaelaps scapularis, Androlaelaps capensis, Androlaelaps tauffliebi, Radfordia sp., and unidentified chiggers) and the louse were parasites while the remainder was soil mites. All ectoparasites were highly aggregated and the species richness as well as the prevalence and abundance of 4 of them were significantly greater in summer compared to winter, possibly as a result of seasonal changes in rainfall patterns affecting the ectoparasites, host behavior, or both.

Ectoparasite burdens of the common mole-rat (Cryptomys hottentotus hottentotus) from the Cape Provinces of South Africa.

The members of the African mole-rat family Bathyergidae are widely distributed across sub-Saharan Africa. Despite their well-studied biology and reproductive physiology, the current knowledge of their ectoparasite fauna is limited and ambiguous due to recent revisions of the bathyergid taxonomy. The common mole-rat (Cryptomys hottentotus hottentotus) is 1 of the most widely distributed species of these subterranean rodents. Ectoparasites were collected from 268 common mole-rats at 2 localities (Western and Northern Cape provinces) in South Africa over the course of 18 mo with the aim to document species richness, prevalence, and abundance of these ectoparasites. The aggregation of parasite species, sex bias within a species, and seasonal variation in ectoparasite burdens were investigated. A total of 4,830 individual parasites from 4 mite species (Androlaelaps scapularis, Androlaelaps capensis, Radfordia ensifera, and 1 undetermined chigger [family Trombiculidae]), 1 flea species (Cryptopsylla ingrami), and 1 louse species (Eulinognathus hilli) were collected. With the exception of R. ensifera and the chigger, all of these ectoparasites appear to be host specific either for the host species or the Bathyergidae. Aggregation indices indicated that with the exception of E. hilli, the distribution of all parasite species was highly aggregated among hosts and sex biased. Seasonal variation in prevalence, abundance, and species richness was apparent, with greater burdens in the rainy winter season. This is likely related to seasonal variation in abiotic factors but may also be affected by the timing of host reproduction and dispersal behavior.

Energetic benefits of sociality offset the costs of parasitism in a cooperative mammal.

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.

Determinants of helminth infection in a subterranean rodent, the Cape dune mole-rat ( Bathyergus suillus ).

The helminth fauna of the largest bathyergid, the Cape mole-rat ( Bathyergus suillus ) was studied throughout an entire calendar year. The species richness encountered was low, with only 3 species of nematodes ( Longistriata bathyergi , Mammalakis macrospiculum, and Trichostrongylus sp.) and 2 species of cestodes ( Taenia sp. and Rodentolepis sp.). At less than 10%, the prevalence for all helminths species was similarly low and may be a result of the solitary lifestyle and the subterranean habitat exploited by this rodent. Clear seasonal patterns were apparent for the most common nematode ( L. bathyergi ), and prevalence and abundance were highest among non-pregnant females compared to males and pregnant females. Dispersal patterns associated with the mating system of the host could explain this pattern. In contrast, the prevalence of the most common cestode ( Taenia sp.) was neither determined by season nor host sex, suggesting that foraging habits may constantly expose B. suillus to this parasite.

Natural parasite infection affects the tolerance but not the response to a simulated secondary parasite infection.

Parasites deplete the resources of their host and can consequently affect the investment in competing traits (e.g. reproduction and immune defence). The immunocompetence handicap hypothesis posits that testosterone (T) mediates trade-offs between parasite defence and reproductive investment by suppressing immune function in male vertebrates while more recently a role for glucocorticoids (e.g. cortisol (C)) in resource allocation has been suggested. These hypotheses however, have not always found support in wild animals, possibly because most studies focus on a single parasite species, whereas infections with multiple parasites are the rule in nature. We measured body mass, T- and C-levels of wild male highveld mole-rats (Cryptomys hottentotus pretoriae) naturally uninfected or infected with a cestode (Mathevotaenia sp.) right after capture. Subsequently, we injected animals subcutaneously with a lipopolysaccharide (LPS) to simulate a bacterial infection and recorded changes in body mass, food intake, haematological parameters and hormone levels. As a control, animals were injected with saline. Natural infection neither affected initial body mass nor C-levels, whereas infected males had significantly reduced T-levels. We observed significant reductions in food intake, body mass and T in response to LPS but not saline while C increased. However, this response did not vary with infection status. In contrast, final body mass and some haematological parameters were significantly lowered in infected males. Our results suggest that naturally infected males are able to compensate for resource depletion by physiological adjustments. However, this leaves them less tolerant to the challenges of a secondary infection.

The role of host traits, season and group size on parasite burdens in a cooperative mammal.

The distribution of parasites among hosts is often characterised by a high degree of heterogeneity with a small number of hosts harbouring the majority of parasites. Such patterns of aggregation have been linked to variation in host exposure and susceptibility as well as parasite traits and environmental factors. Host exposure and susceptibility may differ with sexes, reproductive effort and group size. Furthermore, environmental factors may affect both the host and parasite directly and contribute to temporal heterogeneities in parasite loads. We investigated the contributions of host and parasite traits as well as season on parasite loads in highveld mole-rats (Cryptomys hottentotus pretoriae). This cooperative breeder exhibits a reproductive division of labour and animals live in colonies of varying sizes that procreate seasonally. Mole-rats were parasitised by lice, mites, cestodes and nematodes with mites (Androlaelaps sp.) and cestodes (Mathevotaenia sp.) being the dominant ecto- and endoparasites, respectively. Sex and reproductive status contributed little to the observed parasite prevalence and abundances possibly as a result of the shared burrow system. Clear seasonal patterns of parasite prevalence and abundance emerged with peaks in summer for mites and in winter for cestodes. Group size correlated negatively with mite abundance while it had no effect on cestode burdens and group membership affected infestation with both parasites. We propose that the mode of transmission as well as social factors constrain parasite propagation generating parasite patterns deviating from those commonly predicted.

Three new species of Eimeria (Apicomplexa: Eimeriidae) from the silvery mole rat Heliophobius argenteocinereus Peters, 1846 (Rodentia: Bathyergidae) from Malawi.

Three species of Eimeria Schneider are described from feces of the African bathyergid rodent, Heliophobius argenteocinereus, from Malawi. Oocysts of Eimeria heliophobii n. sp. are broadly ellipsoidal; 27.9 (22-31) x 22.3 (18-24.5) microm with a brownish, heavily pitted oocyst wall, and vacuolar oocyst residuum. Sporocysts are oval, 12.8 (12-14) x 8.4 (8-9) microm with Stieda and substieda bodies. Eimeria nafuko n. sp. has subspherical oocysts; 15.5 (15-16) x 12.8 (12-13) microm with a smooth, colorless oocyst wall. Sporocysts are oval, 9.2 (9-10) x 5.3 (5-6) microm, with a small Stieda body; the substieda body is not visible. Oocysts of Eimeria yamikamiae n. sp. are broadly ellipsoidal to subspherical; 20.8 (19-22) x 17.5 (15.5-19) microm, with slightly yellowish, very faintly pitted oocyst wall. The majority of oocysts contained a single spherical vesicular oocyst residuum and numerous very small granules. Sporocysts are oval, 10.7 (10-11) x 6.8. (6-7) microm, with a dome -like Stieda body and a subspherical to lentil-like substieda body. Typically, infected rodents shed oocysts of more than 1 species of Eimeria.

Patterns of MHC selection in African mole-rats, family Bathyergidae: the effects of sociality and habitat.

African mole-rats are a family of rodents exhibiting an eclectic range of social behaviour and occupying a variety of habitat types. These differences are likely to impact upon the risk of parasite transmission and virulence, with increasing sociality predicted to correspond to an increased risk of transmission. We investigate these factors by analysing the major histocompatibility complex (MHC), a set of genes responsible for encoding highly variable intermediaries of the vertebrate adaptive immune response. To this end we assessed selection at exons 2 and 3 of the MHC class II DQalpha1 gene of four African mole-rat species representing a range of social behaviours. We demonstrate that: (i) the overall pattern of selection at these exons differentiates according to the predicted function of different regions, with the presence of positive selection indicating the likely influence of host-parasite coevolution; and (ii) contrary to the often observed and predicted positive correspondence between sociality and the risk of parasite transmission, two highly social African mole-rat species in fact appear to have comparatively weak positive selection, suggesting diminished host immunity and thus a low overall risk of parasite transmission.

Eimeria burdai sp. n. (Apicomplexa: Eimeriidae), a new parasite species from subterranean African silvery mole-rat, Heliophobius argenteocinereus.

A new coccidian parasite of the genus Eimeria Schneider, 1875 is described from the subterranean African silvery mole-rat Heliophobius argenteocinereus Peters, 1846. Oocysts of Eimeria burdai sp. n. were subspherical to broadly ellipsoidal 17.8 (16-19) x 14.1 (12-15), with a shape index 1.2 (1.1-1.4). Oocyst wall was bilayered, smooth and colourless, approximately 1.0 thick. Outer layer was significantly thicker than inner one. A micropyle and oocyst residuum were absent. One or two ellipsoidal or spherical polar granules were present. Sporocysts were ellipsoidal, 10.8 (9-12) x 6.2 (5-8) with a shape index 1.7 (1.5-1.9). Sporocyst wall was single-layered, thin, smooth and colourless, with small Stieda body at the pointed end. In freshly sporulated oocysts, spherical sporocyst residuum was composed of small granules enclosed by a thin membrane. Sporozoites were elongate, lying length-wise in the long axis of the sporocyst, partially curled around each other, with single large refractile body located posteriorly. Faintly distinguishable nucleus was in the central part of the sporozoite. This eimerian represents the first coccidian species described from subterranean African silvery mole-rat (Rodentia: Bathyergidae).