Zoonotic Pathogens Associated with Pet and Feeder Murid Rodent Species: A Global Systematic Review.

Background: Pet and feeder rodents are one of the main sources of emerging infectious diseases. These rodents are purchased from pet shops, breeders, and online. Consequently, some of these rodents may subtly transmit diseases as they may be asymptomatic to certain pathogens. Materials and Methods: We systematically searched four academic databases viz. Google Scholar, PubMed, Web of Science, and Scopus to determine zoonotic pathogens associated with pet and feeder rodents globally. Our searches were performed in R statistical software using the packages "metagear" and "revtool". Results: We found 62 studies reporting on zoonotic pathogens between 1973 and 2022 from 16 countries representing 4 continents, namely Africa, Europe, Asia, and North America. The review identified 30 zoonotic pathogens isolated from pet and feeder rodents, including the African pygmy mouse (Mus minutoides), brown rat (Rattus norvegicus), and the house mouse (Mus musculus). The greatest number of pathogens was reported from the United States, followed by Togo and the United Kingdom. Bacterial pathogens were the most prevalent. However, the Seoul virus and rat bite fever (Streptobacillus moniliformis) were the most studied pathogens, found in more than one country, with reported outbreak cases. Most of the zoonotic pathogens were isolated from rodents acquired from pet shops. Conclusions: We recommend that pet and feeder rodents purchased from pet shops should be regularly screened for potential zoonotic pathogens as some of these animals may not show clinical signs of the illness. There is also a critical need to develop strict regulations and policies, especially in underdeveloped and developing regions for an effective surveillance process, which will include early detection, rapid response, and control of zoonotic diseases globally.

Haemoplasma Prevalence and Diversity in Three Invasive Rattus Species from Gauteng Province, South Africa.

Invasive Rattus species are carriers of haemotropic Mycoplasmas (haemoplasmas) globally, but data from Africa are lacking. Using a PCR-sequencing approach, we assessed haemoplasma prevalence and diversity in kidney and buccal swabs collected from three invasive Rattus species (Rattus rattus, R. norvegicus and R. tanezumi) in Gauteng Province, South Africa. Whilst the overall sequence-confirmed haemoplasma prevalence was 38.4%, infection rates in R. rattus (58.3%) were significantly higher (χ2 = 12.96; df = 2; n = 99 p < 0.05) than for R. tanezumi (14.3%). Differences between host sex (χ2 = 3.59 × 10−31; df = 1; n = 99; p = 1.00) and age (χ2 = 4.28; df = 2; n = 99; p = 0.12) were not significant. Whilst buccal (1.01%) and ectoparasite positivity (2.13%) were low, these results suggest that multiple transmission routes are possible. Three phylogenetically distinct lineages, consistent with global rat-associated strains described to date, were detected, namely, 'Candidatus Mycoplasma haemomuris subsp. Ratti', and two Rattus-specific haemoplasmas that are yet to be formally described. These results expand the known distribution of invasive rat-associated haemoplasmas and highlight the potential for pathogen co-invasion of new territories together with invading rodent hosts.

Prevalence and Diversity of the Streptobacillus Rat-bite Fever Agent, in Three Invasive, Commensal Rattus Species from South Africa.

Rat-bite fever is an over-looked, global zoonotic disease that has a mortality rate of up to 13%, if untreated. Historically, this rat-borne disease has been attributed to one of two causative agents, Streptobacillus moniliformis or Spirillum minus. Given the confirmed presence of multiple invasive Rattus host species, high rat densities in urban, informal human settlements and increasing reports of rat bites in South Africa, we undertook a retrospective assessment of Streptobacillus in rats sampled from 16 urban sites, in Gauteng, the smallest but most populous Province in South Africa. Using a multi-gene PCR-sequencing approach, we confirmed Streptobacillus presence in 50.9% of oral swabs from three rat species and the presence of two Streptobacillus species, viz.S. moniliformis and S. notomytis. The two members of the cryptic Rattus rattus species complex (R. rattus and R. tanezumi), which are morphologically indistinguishable from each other, had markedly different colonization rates. Whereas 48.6% of rats from this species complex were Streptobacillus-positive, only 32.3% of Rattus tanezumi were positive compared to 61.5% R. rattus. Rattus norvegicus had an intermediate prevalence of 55.6%. Phylogenetic analysis of four gene regions (16S rRNA, gyrB, groEL, recA) identified two discrete lineages; S. moniliformis occurred exclusively in R.norvegicus, and S. notomytis was restricted to the two members of the R. rattus species complex; this represents the first report of Streptobacillus in R. tanezumi. These results highlight a largely overlooked zoonotic threat posed by invasive rats and confirm the presence of two discrete and potentially host-specific Streptobacillus lineages in South Africa.

Geospatial Modelling and Univariate Analysis of Commensal Rodent-Borne Cestodoses: The Case of Invasive spp. of Rattus and Indigenous Mastomys coucha From South Africa.

Poor socio-economic and unsanitary conditions are conducive to commensal rodent infestations, and these conditions are widespread in South Africa. Cestode species of zoonotic interest are highly prevalent in commensal rodents, such as invasive Rattus norvegicus, Rattus rattus, Rattus tanezumi, and indigenous Mastomys coucha, and have been frequently recovered from human stool samples. These cestode species have similar transmission dynamics to traditional soil-transmitted helminths (STHs), which ties them to infections associated with poverty and poor sanitation. Univariate analysis was used in the present study to determine the association between rodent-related factors and cestode prevalence, while ecological niche modelling was used to infer the potential distribution of the cestode species in South Africa. Cestode prevalence was found to be associated with older rodents, but it was not significantly associated with sex, and ectoparasite presence. The predicted occurrence for rodent-borne cestodes predominantly coincided with large human settlements, typically associated with significant anthropogenic changes. In addition, cestode parasite occurrence was predicted to include areas both inland and along the coast. This is possibly related to the commensal behaviour of the rodent hosts. The study highlights the rodent-related factors associated with the prevalence of parasites in the host community, as well as the environmental variables associated with parasite infective stages that influence host exposure. The application of geospatial modelling together with univariate analysis to predict and explain rodent-borne parasite prevalence may be useful to inform management strategies for targeted interventions.

The influence of distance to perennial surface water on ant communities in Mopane woodlands, northern Botswana.

Studies of biodiversity along environmental gradients provide information on how ecological communities change in response to biotic and abiotic factors. For instance, distance to water is associated with several factors that shape the structure and the functioning of ecosystems at a range of spatial scales. We investigated the influence of distance to a perennial water source on ant communities in a semi-arid savanna in northern Botswana. Ant abundance, taxonomic richness, and both alpha and beta diversity were generally higher during the wet than the dry season. However, there were strong seasonal influences on the effects of distance to water, with more pronounced effects during the wet season. While both abundance and beta diversity declined with increasing distances to water during the wet season, there was a contrasting increase in alpha diversity. There was no major effect of distance to water on taxonomic richness during either season. Beta diversity was as high across as along gradients, and we found support for modular rather than nested community structures along gradients. Our study demonstrated that small-scale gradients in distance to water can influence several aspects of ant communities in semi-arid savannas. However, our results also point to strong effects of small-scale environmental variation, for instance associated with vegetation characteristics, soil properties, and plant community structure that are not directly linked to water access.

Analysis of gonadotrophin-releasing hormone-1 and kisspeptin neuronal systems in the nonphotoregulated seasonally breeding eastern rock elephant-shrew (Elephantulus myurus).

Of the 18 sub-Saharan elephant-shrew species, only eastern rock elephant-shrews reproduce seasonally throughout their distribution, a process seemingly independent of photoperiod. The present study characterizes gonadal status and location/intensity of gonadotrophin-releasing hormone-1 (GnRH-1) and kisspeptin immunoreactivities in this polyovulating species in the breeding and nonbreeding seasons. GnRH-1-immunoreactive (ir) cell bodies are predominantly in the medial septum, diagonal band, and medial preoptic area; processes are generally sparse except in the external median eminence. Kisspeptin-ir cell bodies are detected only within the arcuate nucleus; the density of processes is generally low, except in the septohypothalamic nucleus, ventromedial bed nucleus of the stria terminalis, arcuate nucleus, and internal and external median eminence. Kisspeptin-ir processes are negligible at locations containing GnRH-1-ir cell bodies. The external median eminence is the only site with conspicuously overlapping distributions of the respective immunoreactivities and, accordingly, a putative site for kisspeptin's regulation of GnRH-1 release in this species. In the nonbreeding season in males, there is an increase in the rostral population of GnRH-1-ir cell bodies and density of GnRH-1-ir processes in the median eminence. In both sexes, the breeding season is associated with increased kisspeptin-ir process density in the rostral periventricular area of the third ventricle and arcuate nucleus; at the latter site, this is positively correlated with gonadal mass. Cross-species comparisons lead us to hypothesize differential mechanisms within these peptidergic systems: that increased GnRH-1 immunoreactivity during the nonbreeding season reflects increased accumulation with reduced release; that increased kisspeptin immunoreactivity during the breeding season reflects increased synthesis with increased release.

Life on the rocks: Multilocus phylogeography of rock hyrax (Procavia capensis) from southern Africa.

Understanding the role of geography and climatic cycles in determining patterns of biodiversity is important in comparative and evolutionary biology and conservation. We studied the phylogeographic pattern and historical demography of a rock-dwelling small mammal species from southern Africa, the rock hyrax Procavia capensis capensis. Using a multilocus coalescent approach, we assessed the influence of strong habitat dependence and fluctuating regional climates on genetic diversity. We sequenced a mitochondrial gene (cytochrome b) and two nuclear introns (AP5, PRKC1) supplemented with microsatellite genotyping, in order to assess evolutionary processes over multiple temporal scales. In addition, distribution modelling was used to investigate the current and predicted distribution of the species under different climatic scenarios. Collectively, the data reveal a complex history of isolation followed by secondary contact shaping the current intraspecific diversity. The cyt b sequences confirmed the presence of two previously proposed geographically and genetically distinct lineages distributed across the southern African Great Escarpment and north-western mountain ranges. Molecular dating suggests Miocene divergence of the lineages, yet there are no discernible extrinsic barriers to gene flow. The nuclear markers reveal incomplete lineage sorting or ongoing mixing of the two lineages. Although the microsatellite data lend some support to the presence of two subpopulations, there is weak structuring within and between lineages. These data indicate the presence of gene flow from the northern into the southern parts of the southern African sub-region likely following the secondary contact. The distribution modelling predictably reveal the species' preference for rocky areas, with stable refugia through time in the northern mountain ranges, the Great Escarpment, as well as restricted areas of the Northern Cape Province and the Cape Fold Mountains of South Africa. Different microclimatic variables appear to determine the distributional range of the species. Despite strong habitat preference, the micro-habitat offered by rocky crevices and unique life history traits likely promoted the adaptability of P. capensis, resulting in the widespread distribution and persistence of the species over a long evolutionary period. Spatio-temporal comparison of the evolutionary histories of other co-distributed species across the rocky landscapes of southern Africa will improve our understanding of the regional patterns of biodiversity and local endemism.

Trophic overlap between fish and riparian spiders: potential impacts of an invasive fish on terrestrial consumers.

Studies on resource sharing and partitioning generally consider species that occur in the same habitat. However, subsidies between linked habitats, such as streams and riparian zones, create potential for competition between populations which never directly interact. Evidence suggests that the abundance of riparian consumers declines after fish invasion and a subsequent increase in resource sharing of emerging insects. However, diet overlap has not been investigated. Here, we examine the trophic niche of native fish, invasive fish, and native spiders in South Africa using stable isotope analysis. We compared spider abundance and diet at upstream fishless and downstream fish sites and quantified niche overlap with invasive and native fish. Spider abundance was consistently higher at upstream fishless sites compared with paired downstream fish sites, suggesting that the fish reduced aquatic resource availability to riparian consumers. Spiders incorporated more aquatic than terrestrial insects in their diet, with aquatic insects accounting for 45-90% of spider mass. In three of four invaded trout rivers, we found that the average proportion of aquatic resources in web-building spider diet was higher at fishless sites compared to fish sites. The probability of web-building and ground spiders overlapping into the trophic niche of invasive brown and rainbow trout was as high as 26 and 51%, respectively. In contrast, the probability of spiders overlapping into the trophic niche of native fish was always less than 5%. Our results suggest that spiders share resources with invasive fish. In contrast, spiders had a low probability of trophic overlap with native fish indicating that the traits of invaders may be important in determining their influence on ecosystem subsidies. We have added to the growing body of evidence that invaders can have cross-ecosystem impacts and demonstrated that this can be due to niche overlap.

Net effects of multiple stressors in freshwater ecosystems: a meta-analysis.

The accelerating rate of global change has focused attention on the cumulative impacts of novel and extreme environmental changes (i.e. stressors), especially in marine ecosystems. As integrators of local catchment and regional processes, freshwater ecosystems are also ranked highly sensitive to the net effects of multiple stressors, yet there has not been a large-scale quantitative synthesis. We analysed data from 88 papers including 286 responses of freshwater ecosystems to paired stressors and discovered that overall, their cumulative mean effect size was less than the sum of their single effects (i.e. an antagonistic interaction). Net effects of dual stressors on diversity and functional performance response metrics were additive and antagonistic, respectively. Across individual studies, a simple vote-counting method revealed that the net effects of stressor pairs were frequently more antagonistic (41%) than synergistic (28%), additive (16%) or reversed (15%). Here, we define a reversal as occurring when the net impact of two stressors is in the opposite direction (negative or positive) from that of the sum of their single effects. While warming paired with nutrification resulted in additive net effects, the overall mean net effect of warming combined with a second stressor was antagonistic. Most importantly, the mean net effects across all stressor pairs and response metrics were consistently antagonistic or additive, contrasting the greater prevalence of reported synergies in marine systems. Here, a possible explanation for more antagonistic responses by freshwater biota to stressors is that the inherent greater environmental variability of smaller aquatic ecosystems fosters greater potential for acclimation and co-adaptation to multiple stressors.

Partitioning of evaporative water loss into respiratory and cutaneous pathways in Wahlberg's epauletted fruit bats (Epomophorus wahlbergi).

The relative contributions of respiratory and cutaneous evaporation to total evaporative water loss (TEWL) and how the partitioning of these two avenues varies with environmental temperature has received little attention in bats. We trained Wahlberg's epauletted fruit bats (Epomophorus wahlbergi) captured in Pretoria, South Africa, to wear latex masks while hanging in respirometry chambers, and we measured respiratory evaporative water loss (REWL) and cutaneous evaporative water loss (CEWL) over air temperatures (Ta) from 10° to 40°C. The bats' normothermic body temperature (Tb) was approximately 36°C, which increased at higher Ta to 40.5° ± 1.0°C at Ta ≈ 40°C. Both TEWL and resting metabolic rate (RMR) increased sharply at Ta >35°C, with a mean TEWL at 40°C equivalent to 411% of that at 30°C. The increase in TEWL was driven by large increases in both CEWL and REWL. CEWL comprised more than 50% of TEWL over the entire Ta range, with the exception of Ta ≈ 40°C, where REWL accounted for 58% of evaporative water loss. Surface area-specific CEWL increased approximately sixfold with increasing Ta. Thermoregulation at Ta approaching or exceeding Tb involved a considerable energetic cost, with RMR at Ta ≈ 40°C exceeding by 24% that measured at Ta ≈ 10°C. Our data do not support recent arguments that respiratory gas exchange across the wing membranes represents 5%-10% of the total in E. wahlbergi.

Summit metabolism and metabolic expansibility in Wahlberg's epauletted fruit bats (Epomophorus wahlbergi): seasonal acclimatisation and effects of captivity.

Summit metabolism (M sum), the maximum rate of resting metabolic thermogenesis, has been found to be broadly correlated with climatic variables and the use of heterothermy in some endotherms. Far less is known about M sum and metabolic expansibility [ME, the ratio of M sum to basal metabolic rate (BMR)] in bats compared with many other endotherm taxa. We measured BMR and M sum during winter and summer in captive and wild populations of a pteropodid from the southern subtropics, Wahlberg's epauletted fruit bat (Epomophorus wahlbergi) in Pretoria, South Africa. The M sum of fruit bats ranged from 5.178 ± 0.611 W (captive, summer) to 6.006 ± 0.890 W (captive, winter), and did not vary significantly between seasons. In contrast, BMR decreased by 17-25% in winter. The combination of seasonally stable M sum but flexible BMR resulted in ME being significantly higher in winter than in summer, ranging from 7.24 ± 1.49 (wild, summer) to 13.11 ± 2.14 (captive, winter). The latter value is well above the typical mammalian range. Moreover, both M sum and ME were significantly higher in captive bats than in wild individuals; we speculate this represents a phenotypic response to a reduction in exercise-associated heat production while in captivity. Our data for E. wahlbergi, combined with those currently available for other chiropterans, reveal that M sum in bats is highly variable compared with allometrically expected values for other mammals.

The hippocampus of the eastern rock sengi: cytoarchitecture, markers of neuronal function, principal cell numbers, and adult neurogenesis.

The brains of sengis (elephant shrews, order Macroscelidae) have long been known to contain a hippocampus that in terms of allometric progression indices is larger than that of most primates and equal in size to that of humans. In this report, we provide descriptions of hippocampal cytoarchitecture in the eastern rock sengi (Elephantulus myurus), of the distributions of hippocampal calretinin, calbindin, parvalbumin, and somatostatin, of principal neuron numbers, and of cell numbers related to proliferation and neuronal differentiation in adult hippocampal neurogenesis. Sengi hippocampal cytoarchitecture is an amalgamation of characters that are found in CA1 of, e.g., guinea pig and rabbits and in CA3 and dentate gyrus of primates. Correspondence analysis of total cell numbers and quantitative relations between principal cell populations relate this sengi to macaque monkeys and domestic pigs, and distinguish the sengi from distinct patterns of relations found in humans, dogs, and murine rodents. Calretinin and calbindin are present in some cell populations that also express these proteins in other species, e.g., interneurons at the stratum oriens/alveus border or temporal hilar mossy cells, but neurons expressing these markers are often scarce or absent in other layers. The distributions of parvalbumin and somatostatin resemble those in other species. Normalized numbers of PCNA+ proliferating cells and doublecortin-positive (DCX+) differentiating cells of neuronal lineage fall within the overall ranges of murid rodents, but differed from three murid species captured in the same habitat in that fewer DCX+ cells relative to PCNA+ were observed. The large and well-differentiated sengi hippocampus is not accompanied by correspondingly sized cortical and subcortical limbic areas that are the main hippocampal sources of afferents and targets of efferents. This points to intrinsic hippocampal information processing as the selective advantage of the large sengi hippocampus.

Habitat-specific shaping of proliferation and neuronal differentiation in adult hippocampal neurogenesis of wild rodents.

Daily life of wild mammals is characterized by a multitude of attractive and aversive stimuli. The hippocampus processes complex polymodal information associated with such stimuli and mediates adequate behavioral responses. How newly generated hippocampal neurons in wild animals contribute to hippocampal function is still a subject of debate. Here, we test the relationship between adult hippocampal neurogenesis (AHN) and habitat types. To this end, we compare wild Muridae species of southern Africa [Namaqua rock mouse (Micaelamys namaquensis), red veld rat (Aethomys chrysophilus), highveld gerbil (Tatera brantsii), and spiny mouse (Acomys spinosissimus)] with data from wild European Muridae [long-tailed wood mice (Apodemus sylvaticus), pygmy field mice (Apodemus microps), yellow-necked wood mice (Apodemus flavicollis), and house mice (Mus musculus domesticus)] from previous studies. The pattern of neurogenesis, expressed in normalized numbers of Ki67- and Doublecortin(DCX)-positive cells to total granule cells (GCs), is similar for the species from a southern African habitat. However, we found low proliferation, but high neuronal differentiation in rodents from the southern African habitat compared to rodents from the European environment. Within the African rodents, we observe additional regulatory and morphological traits in the hippocampus. Namaqua rock mice with previous pregnancies showed lower AHN compared to males and nulliparous females. The phylogenetically closely related species (Namaqua rock mouse and red veld rat) show a CA4, which is not usually observed in murine rodents. The specific features of the southern environment that may be associated with the high number of young neurons in African rodents still remain to be elucidated. This study provides the first evidence that a habitat can shape adult neurogenesis in rodents across phylogenetic groups.

Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa.

BACKGROUND: South Africa's long and extensive trade activity has ensured ample opportunities for exotic species introduction. Whereas the rich biodiversity of endemic southern African fauna has been the focus of many studies, invasive vertebrates are generally overlooked despite potential impacts on biodiversity, health and agriculture. Genetic monitoring of commensal rodents in South Africa which uncovered the presence of Rattus tanezumi, a South-East Asian endemic not previously known to occur in Africa, provided the impetus for expanded studies on all invasive Rattus species present. RESULTS: To this end, intensified sampling at 28 South African localities and at one site in Swaziland, identified 149 Rattus specimens. Cytochrome b gene sequencing revealed the presence of two R. tanezumi, seven Rattus rattus and five Rattus norvegicus haplotypes in south Africa. Phylogenetic results were consistent with a single, recent R. tanezumi introduction and indicated that R. norvegicus and R. rattus probably became established following at least two and three independent introductions, respectively. Intra- and inter-specific diversity was highest in informal human settlements, with all three species occurring at a single metropolitan township site. Rattus norvegicus and R. rattus each occurred sympatrically with Rattus tanezumi at one and five sites, respectively. Karyotyping of selected R. rattus and R. tanezumi individuals identified diploid numbers consistent with those reported previously for these cryptic species. Ordination of bioclimatic variables and MaxEnt ecological niche modelling confirmed that the bioclimatic niche occupied by R. tanezumi in south Africa was distinct from that occupied in its naturalised range in south-east Asia suggesting that factors other than climate may influence the distribution of this species. CONCLUSIONS: This study has highlighted the value of genetic typing for detecting cryptic invasive species, providing historical insights into introductions and for directing future sampling. The apparent ease with which a cryptic species can become established signals the need for broader implementation of genetic monitoring programmes. In addition to providing baseline data and potentially identifying high-risk introduction routes, the predictive power of ecological niche modelling is enhanced when species records are genetically verified.

Bioregion heterogeneity correlates with extensive mitochondrial DNA diversity in the Namaqua rock mouse, Micaelamys namaquensis (Rodentia: Muridae) from southern Africa--evidence for a species complex.

BACKGROUND: Intraspecific variation within the diverse southern African murine rodents has not been extensively investigated, yet cryptic diversity is evident in several taxa studied to date. The Namaqua rock mouse, Micaelamys namaquensis Smith, 1834 is a widespread endemic murine rodent from the subregion. Currently, a single species with four subspecies is recognised, but in the past up to 16 subspecies were described. Thus, this species is a good candidate for the investigation of patterns and processes of diversification in a diverse but under-studied mammalian subfamily and geographic region. Here, we report genetic differentiation based on mitochondrial DNA (mtDNA) cytochrome b (cyt b) sequences among samples collected over an extensive coverage of the species' range. RESULTS: Cytochrome b sequences of 360 widely sampled individuals identified 137 unique maternal alleles. Gene tree and phylogeographic analyses of these alleles suggest the presence of at least eight lineages or haplogroups (A-H), with varying degrees of intra-lineage diversity. This differentiation is in contrast with the most recent taxonomic treatment based on cranial morphometrics which only recognised four subspecies. The mtDNA diversity strongly supports earlier views that this taxon may represent a species complex. We further show statistical support for the association of several of these lineages with particular vegetation biomes of southern Africa. The time to the most recent common ancestor (TMRCA) dates to the Pliocene (~5 Mya) whereas coalescent-based divergence time estimates between lineages vary between 813 Kya [0.22-1.36] and 4.06 Mya [1.21-4.47]. The major diversification within lineages occurred during the Pleistocene. The identification of several regions of sympatry of distinct lineages offers future opportunities for the elucidation of the underlying speciation processes in the suggested species complex. CONCLUSIONS: Similar to other African murine rodents, M. namaquensis radiated during the Pliocene and Pleistocene coinciding with major periods of aridification and the expansion of savanna habitats. The suggested species complex is represented by at least eight lineages of which the majority are confined to only one or a few neighbouring biomes/bioregions. Contrasting intra-lineage phylogeographic patterns suggest differences in adaptation and responses to Plio-Pleistocene climatic and vegetation changes. The role of ecological factors in driving speciation in the group needs further investigation.