Eimeria and Klossia spp. (Protozoa: Sporozoa) from Wild Mammals in Borneo*

SYNOPSIS. During a survey of parasites of Sabah mammals, coccidia oocysts were found in 9 of 22 host species examined. Sporulated oocysts of Klossia sp. from Rattus whiteheadi are described. New geographic records are reported for Eimeria callosciuri, Eimeria sabani, and Eimeria tupaiae. New host and geographic records are reported for Eimeria separata from Rattus cremoriventer, for E. tupaiae and Eimeria ferruginea from Tupaia tana, for Eimeria nieschulzi from Rattus muelleri, and for E. sabani and Klossia sp. from R. whiteheadi.     

New microsatellite markers for the bush rat,Rattus fuscipes greyii: characterization and cross‐species amplification

We describe here 16 new microsatellite markers for the bush rat, Rattus fuscipes greyii, and characterize their cross‐species amplification within the Australian Rattus and at a greater level of divergence in Rattus rattus and Rattus norvegicus. Within R. f. greyii, all of the loci are highly polymorphic, with six to 24 alleles per locus across the species range and expected heterozygosity ranging from 0.48 to 0.90 per locus within a sample of 24 rats from a large population on Kangaroo Island. Cross‐species amplification rates were approximately 87% within the Australian Rattus and approximately 50% within R. rattus and R. norvegicus. These loci are highly polymorphic with a high success rate of cross‐species amplification, making them potentially useful for a wide range of genetic studies.     

Invasion by Rattus rattus into native coastal forests of south‐eastern Australia: are native small mammals at risk?

The black rat, Rattus rattus, is an alien rodent in Australian ecosystems where niche overlap with native small mammals may lead to competition for resources and displacement of native species. In coastal habitats surrounding Jervis Bay in south‐eastern Australia, R. rattus co‐occurs with the native bush rat, Rattus fuscipes, and brown antechinus, Antechinus stuartii. Relative distributions and abundances, and fine‐scale space use suggest invasive and native rodents compete for use of space and habitat. Such competitive interactions were not evident between R. rattus and native A. stuartii, which was negatively influenced more by disturbance to habitat. Differences in rodent communities between spatially separate forests forming the northern and southern peninsulas of Jervis Bay potentially reflect symmetrical competition and differences in competitive outcomes. In southern forests, R. rattus was largely restricted to patches of disturbed forest associated with campgrounds. Competitive interference by native rodent populations inhabiting surrounding intact forests may have so far limited R. rattus colonization of these areas. In northern forests, R. rattus was the predominant rodent irrespective of disturbance, while populations of R. fuscipes were unusually low seemingly due to poor juvenile recruitment. Native individuals avoided areas frequented by adult R. rattus and given that species did not partition use of microhabitats, R. rattus most likely precluded R. fuscipes from suitable habitat and in doing so limited native populations. We discuss how natural disturbance of habitat and human activity have potentially facilitated successful invasion by R. rattus of the northern forests. Studies that manipulate rodent populations are required to support these interpretations of observed patterns.     

The use of habitat components by small mammals in eastern Australia

The effect of habitat components (vegetation density at two levels, litter, logs and roads) on the distribution of small mammals was assessed in adjacent areas of native forest and Pinus taeda plantation in north-eastern New South Wales. Rattus fuscipes was associated with structural complexity in native forest but not in pine plantation where it was found on downslope areas. R. rattus was associated with windrows in the pine plantation, R. lutreolus with areas devoid of a shrub layer in the pine plantation, Antechinus stuartii with logs and Melomys cervinipes with habitat components associated with rainforest areas. Road crossing by small mammals was inversely related to road width; roads severely restricted or stopped the movement of small mammals even when the road consisted of a long-unused and partly overgrown track.     

Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)

Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This species complex is native to India and Southeast Asia. According to current taxonomic classification, there are three taxa living in sympatry in several parts of Thailand, Cambodia and Lao People's Democratic Republic, where this study was conducted: two accepted species (Rattus tanezumi, Rattus sakeratensis) and an additional mitochondrial lineage of unclear taxonomic status referred to here as ‘Rattus R3’. We used extensive sampling, morphological data and diverse genetic markers differing in rates of evolution and parental inheritance (two mitochondrial DNA genes, one nuclear gene and eight microsatellite loci) to assess the reproductive isolation of these three taxa. Two close Asian relatives, Rattus argentiventer and Rattus exulans, were also included in the genetic analyses. Genetic analyses revealed discordance between the mitochondrial and nuclear data. Mitochondrial phylogeny studies identified three reciprocally monophyletic clades in the black rat complex. However, studies of the phylogeny of the nuclear exon interphotoreceptor retinoid‐binding protein gene and clustering and assignation analyses with eight microsatellites failed to separate R. tanezumi and R3. Morphometric analyses were consistent with nuclear data. The incongruence between mitochondrial and nuclear (and morphological) data rendered R. tanezumi/R3 paraphyletic for mitochondrial lineages with respect to R. sakeratensis. Various evolutionary processes, such as shared ancestral polymorphism and incomplete lineage sorting or hybridization with massive mitochondrial introgression between species, may account for this unusual genetic pattern in mammals.     

Role of movement,interremnant dispersal and edge effects in determining sensitivity to habitat fragmentation in two forest‐dependent rodents

Abstract Habitat fragmentation and disturbance affect patterns of habitat use, animal movement and spatial behaviour and might have significant effects upon population dynamics and trends, and ultimately population persistence. Previous studies have suggested that the ability to disperse between remnants and a positive or neutral response to edges should be associated with species capable of persisting in remnant habitat. Using both radiotracking and trapping data, movement patterns, dispersal and response to habitat edges of Rattus fuscipes were examined within forests, corridors, remnants and pastures in south‐east Queensland, Australia. Rattus fuscipes has previously been shown to be robust to the effects of habitat fragmentation; however, contrary to expectations, R. fuscipes was found to be sensitive to edges, and no evidence of interremnant dispersal was detected, despite interremnant distances that were substantially smaller than the distances R. fuscipes was found to move in continuous habitat. Using only trapping data, the same factors were examined in relation to Melomys cervinipes, a species sensitive to fragmentation. Melomys cervinipes was found to utilize edge habitat, but no evidence of interremnant dispersal was detected, although the capacity to detect such movement was limited by low abundance in remnants where M. cervinipes was extant, and the species absence from many remnants. Movement patterns, interremnant dispersal capacity, and sensitivity to edges did not prove to be good predictors of these species responses to habitat fragmentation. Alternative explanations, such as population fluctuation and the capacity for rapid population growth in remnants for these two species, and the influence habitat quality has on these parameters should be investigated.     

Herbivory in invasive rats: criteria for food selection

Three species of rats (Rattus exulans, R. rattus, R. norvegicus) are widely invasive, having established populations in terrestrial habitats worldwide. These species exploit a wide variety of foods and can devastate native flora and fauna. Rats can consume a variety of plant parts, but may have the most dramatic effects on plant populations through consumption and destruction of seeds. The vulnerability of vegetation to rat consumption is influenced by many factors including size of plant part, and mechanical and chemical defenses. We reviewed the literature to find out what plant species and plant parts invasive rats are consuming and what characteristics these sources share that may influence selection by rats. Many of the studies we found were preformed in New Zealand and our analyses are, therefore, focused on this location. We also performed feeding trials in the laboratory with R. norvegicus to determine if seed hardness and palatability would influence rat consumptive choices. We found more reports of rat consumption of fruits and seeds versus vegetative plant parts, and smaller fruits and seeds versus larger. R. norvegicus are reported to consume proportionally more vegetative plant parts than either R. exulans or R. rattus, possibly due to their more ground dwelling habits. Large size and hard seed coats may deter rat feeding, but unpalatable chemicals may be even more effective deterrents to rats. Scientists and managers can better manage vegetation in rat invaded areas by understanding the criteria rats use to select food.     

Dual exposure of Rickettsia typhi and Orientia tsutsugamushi in the field‐collected Rattus rodents from Thailand

Field‐collected rodents and fleas from ten provinces covering four regions of Thailand were investigated for possible rickettsial pathogen infections. The 257 trapped‐rodents belonged to 12 species. Five species of Genus Rattus accounted for 93% of the total capture, of which Rattus exulans and Rattus norvegicus were the two major species caught. All flea specimens, removed from trapped rodents, were identified as Xenopsylla cheopis. The PCR technique was performed on ectoparasite specimens to detect the presence of murine typhus pathogen (Rickettsia typhi) and scrub typhus pathogen (Orientia tsutsugamushi). Thirteen flea specimens (2.6 %) were found to be positive for R. typhi but none for O. tsutsugamushi. An ELISA technique was used to detect the rodent's antibodies against R. typhi and O. tsutsugamushi. Sixty‐one rodent serum samples (23.7%) were positive for R. typhi specific IgM, IgG, or both, while 47 of the samples (18.3%) were positive for O. tsutsugamushi. Twenty serum samples from R. norvegicus (7.8%) had detectable antibodies against both R. typhi and O. tsutsugamushi. Our findings revealed the existence of the dual infection of rickettsial pathogens in the same natural hosts.     

A mathematical epidemiological model of gram-negative Bartonella bacteria: does differential ectoparasite load fully explain the differences in infection prevalence of Rattus rattus and Rattus norvegicus?

We postulate that the large difference in infection prevalence, 24% versus 5%, in R. norvegicus and R. rattus, respectively, between these two co-occurring host species may be due to differences in ectoparasite and potential vector infestation rates. A compartmental model, representative of an infectious system containing these two Rattus species and two ectoparasite vectors, was constructed and the coefficients of the forces of infection determined mathematically. The maximum difference obtained by the model in the prevalence of Bartonella in the two Rattus species amounts to 4.6%, compared to the observed mean difference of 19%. Results suggest the observed higher Bartonella infection prevalence in Rattus norvegicus compared to Rattus rattus, cannot be explained solely by higher ectoparasite load. The model also highlights the need for more detailed biological research on Bartonella infections in Rattus and the importance of the flea vector in the spread of this disease.     

Invasion facilitates hybridization with introgression in the Rattus rattus species complex

Biological invasions result in novel species interactions, which can have significant evolutionary impacts on both native and invading taxa. One evolutionary concern with invasions is hybridization among lineages that were previously isolated, but make secondary contact in their invaded range(s). Black rats, consisting of several morphologically very similar but genetically distinct taxa that collectively have invaded six continents, are arguably the most successful mammalian invaders on the planet. We used mitochondrial cytochrome b sequences, two nuclear gene sequences (Atp5a1 and DHFR) and nine microsatellite loci to examine the distribution of three invasive black rat lineages (Rattus tanezumi, Rattus rattus I and R. rattus IV) in the United States and Asia and to determine the extent of hybridization among these taxa. Our analyses revealed two mitochondrial lineages that have spread to multiple continents, including a previously undiscovered population of R. tanezumi in the south‐eastern United States, whereas the third lineage (R. rattus IV) appears to be confined to Southeast Asia. Analyses of nuclear DNA (both sequences and microsatellites) suggested significant hybridization is occurring among R. tanezumi and R. rattus I in the United States and also suggest hybridization between R. tanezumi and R. rattus IV in Asia, although further sampling of the latter species pair in Asia is required. Furthermore, microsatellite analyses suggest unidirectional introgression from both R. rattus I and R. rattus IV into R. tanezumi. Within the United States, introgression appears to be occurring to such a pronounced extent that we were unable to detect any nuclear genetic signal for R. tanezumi, and a similar pattern was detected in Asia.     

Black rat (Rattus rattus) genomic variability characterized by chromosome painting

Black rats are of outstanding interest in parasitology and infective disease analysis. We used chromosome paints from both the mouse(Mus musculus) and the Norway rat(Rattus norvegicus) to characterize the genome of two Black rat subspecies from Italy. Both subspecies have two large metacentrics (n. 1, 4) not present in the Norway rat (2n = 42).Rattus rattus rattus has a diploid number of 2n = 38, whileRattus rattus frugivorous has two small metacentric “supernumerary” or B chromosomes for a diploid number of 2n = 38 + 2B. The 21 mouse paints gave 38 signals on theR. r. rattus karyotype and 39 signals in theR. r. frugivorous karyotype. The two metacentrics, not present inR. norvegicus, were hybridized by mouse 16/1/17 and mouse 4/10/15. These chromosomes are homologous to: RRA1 = RNO 5/7, and RRA4 = RNO 9/11 and not “4/7” and “11/12” as previously reported. Furthermore, the synteny of Chr 13 of theR. r. frugivorous withR. norvegicus Chr 16 and mouse Chrs 8/14 is not complete, because there is a small pericentromeric insertion of RNO Chr 18 (mouse Chr 18). If we consider only the two metacentrics, RRA1 and RRA4, the principal differences betweenR. norvegicus andR. rattus, then we can propose the derived synteny of 124 genes in the black rat. A comparison of the Z index between rats and mice shows an acceleration of genomic evolution among genus, species, and subspecies. The chromosomal differences betweenR. r. rattus xR. r. frugivorous suggest that they may be classified as different species because hybrids would produce 50% unbalanced gametes.     

Gut microflora may facilitate adaptation to anthropic habitat: A comparative study in Rattus

Anthropophilic species (“commensal” species) that are completely dependent upon anthropic habitats experience different selective pressures particularly in terms of food than their noncommensal counterparts. Using a next‐generation sequencing approach, we characterized and compared the gut microflora community of 53 commensal Rattus rattus and 59 noncommensal Rattus satarae captured in 10 locations in the Western Ghats, India. We observed that, while species identity was important in characterizing the microflora communities of the two Rattus hosts, environmental factors also had a significant effect. While there was significant geographic variation in the microflora of the noncommensal R. satarae, there was no effect of geographic distance on gut microflora of the commensal R. rattus. Interestingly, host genetic distance did not significantly influence the community in either Rattus hosts. Collectively, these results indicate that a shift in habitat is likely to result in a change in the gut microflora community and imply that the gut microflora is a complex trait, influenced by various parameters in different habitats.     

Is it worth eradicating the invasive pest Rattus norvegicus from Molène archipelago? Genetic structure as a decision-making tool

Genetic variability and structure were estimated by microsatellite analysis at 7 loci in brown rat populations (Rattus norvegicus) from the Iroise insular complex and neighbouring mainland (Brittany, France). Island genetic diversity is lower than on the mainland and a highly significant positive correlation was found between mean heterozygosity and the logarithm of island area, which is consistent with theoretical expectations. Rattus norvegicus populations are substructured at a kilometric scale, both on the islands and on the mainland. Intra-island structuration is extremely high, suggesting that no effective migration occurs between islands or with the mainland. Historical and genetical evidence suggest that R. norvegicus was introduced independently on Ouessant and Molène archipelago, with a low and a high founder effect respectively. These results are discussed in terms of recolonization probability of islands that have been cleared of R. norvegicus, which illustrates the usefulness of genetic markers in determining parameters of interest to the conservation biologist.     

Trypomastigotes and potential flea vectors of the endemic rodents and the introduced Rattus rattus in the rainforests of Madagascar

Transmission of parasites and diseases may be one of the mechanisms for the displacement of native and endemic rodents of Madagascar (subfamily Nesomyinae) by the introduced Rattus rattus (subfamily Murinae). We studied the occurrence of trypomastigotes in rodents at several rainforest sites on the island. Examination of blood smears showed Trypanosoma lewisi-like trypomastigotes in 11.5% of the R. rattus (n = 52). Trypomastigotes differing in morphology from those of T. lewisi were detected in 4% of the endemic rodent Nesomys rufus (n = 23). In contrast to the relatively heavy infections found in R. rattus, only a few trypomastigotes were found in the infected N. rufus. Trypomastigotes were not found in other nesomyine rodents including Eliurus minor (n = 18), E. tanala (n = 15), E. grandidieri (n = 12), E. majori (n = 9) or E. webbi (n = 9). Of potential vectors of trypomastigotes, six endemic species of fleas were identified from the rodents.     

Rodent Diversity in a Highly Degraded Tropical Landscape: Hong Kong, South China

The diverse ecological roles played by different rodent species mean that the loss of some species and superabundance of others could potentially influence a wide range of ecological processes. Hong Kong (22° N, 114° E), with seven million people in a land area of 1100 km², could be considered a `worst case scenario' for the survival of mammalian diversity. Existing information on rodents in Hong Kong was compiled from previous published and unpublished studies, and additional trapping was conducted at 17 non-urban sites. The rodent fauna of modern Hong Kong consists of eight species of rats and mice (Bandicota indica, Mus caroli, M. musculus, Niviventer fulvescens, Rattus norvegicus, R. rattus, R. tanezumi, R. sikkimensis: Muridae), one porcupine (Hystrix brachyura: Hystricidae), and one recently introduced tree squirrel (Callosciurus erythraeus: Sciuridae). Six of the murids are urban or agricultural commensals, so only the porcupine and two murids, N. fulvescens and R. sikkimensis, are likely survivors of Hong Kong's pre-deforestation native rodent fauna. The two murids co-dominate in forest and shrubland, but can also move through grassland, which has probably enabled their survival through repeated cycles of fragmentation and regrowth. Additional forest rodents that may have inhabited Hong Kong in the past are tentatively identified from information on their recent distributions in the region. One possible ecological consequence of Hong Kong's depleted rodent fauna is a shift in the balance between seed predation and seed dispersal, in favor of the former.     

Review of negative effects of introduced rodents on small mammals on islands

In this first comprehensive review of negative effects of introduced rodents on insular small mammals, the focal species Rattus rattus, R. norvegicus, R. exulans and Mus musculus are implicated in at least 11 extinctions. Furthermore, removal experiments, eradication campaigns and control programmes provide evidence for negative effects on extant populations. While data are currently insufficient for meaningful generalisation with regard to the most threatening rodents, the most threatened small mammals, and the true extent of the problem, it is interesting that R. rattus is implicated in the majority of impacts. This may be explained by its extensive distribution and ecological plasticity. I conclude with methodological recommendations to guide data collection for impact quantification and the study of impact mechanism. This information should facilitate the prioritisation and justification of eradication campaigns, control programmes and biosecurity measures while ensuring that much-needed attention is paid to the conservation of insular small mammals.     

Duplication of J κ genes within genus Rattus

We have isolated a region containing the immunoglobulin kappa chain joining segments from a liver DNA library of the Australian rat Rattus villosissimus, and determined its nucleotide sequence. While the laboratory rat (Rattus norvegicus) had previously been shown to contain three recently duplicated copies of J 2, R. villosissimus has only two. Furthermore, all three copies of J 2 in R. norvegicus share an 11 by deletion in their 5 flanking regions which is not evident in either copy of J 2 in R. villosissimus. This suggests that the initial duplication events occurred separately in the two lineages, and were followed by a second duplication in R. norvegicus, all three duplications having occurred within the last 6–12 million years (although more complicated schemes involving gene conversion events cannot be excluded). These results indicate that there is a high degree of plasticity in this region of the genome, and that selective forces must exist which have maintained the number of expressible J segments in humans (5) and rodents (4–6) within their narrow range.     

Commensal Rats and Humans: Integrating Rodent Phylogeography and Zooarchaeology to Highlight Connections between Human Societies

Phylogeography and zooarchaeology are largely separate disciplines, yet each interrogates relationships between humans and commensal species. Knowledge gained about human history from studies of four commensal rats (Rattus rattus, R. tanezumi, R. exulans, and R. norvegicus) is outlined, and open questions about their spread alongside humans are identified. Limitations of phylogeographic and zooarchaeological studies are highlighted, then how integration would increase understanding of species’ demographic histories and resultant inferences about human societies is discussed. How rat expansions have informed the understanding of human migration, urban settlements, trade networks, and intra- and interspecific competition is reviewed. Since each rat species is associated with different human societies, they identify unique ecological and historical/cultural conditions that influenced their expansion. Finally, priority research areas including nuclear genome based phylogeographies are identified using archaeological evidence to understand R. norvegicus expansion across China, multi-wave colonization of R. rattus across Europe, and competition between R. rattus and R. norvegicus.     

Mammals,reptiles and crabs on the Krakatau Islands: Their roles in the ecosystem

In 1982 I studied the changes which had taken place in the fauna of the Krakatau Islands over the last fifty years, and elucidated the roles of terrestrial consumers and reducers in the developing ecosystems of these islands. Only two species of rat were found (Rattus rattus andR. tiomanicus) as observed by Dammerman (1948) in 1933, butR. tiomanicus had newly established its population on Sertung. No rats were found on Anak Krakatau. Although many skinks (Mabuya multifasciata) were observed on R. Besar, this species was not found on the other islands. The rat and skink are considered strong competitors to the sand crab (Ocypode kuhli), because while the crab was restricted to the sandy beach on the three islands where rat and skink live it had expanded inland on Anak Krakatau where there are no rats and skinks. The two banded monitor (Varanus sarvator) was found on every island and it mainly fed on crabs (Gecarcoidea natalis andMetasesarma aubryi). Thus it is suggested that the crab plays an important role in the process of faunal succession on the Krakatau Islands.     

Rat kappa-chain allotypes

The distribution of rat kappa-chain allotype specificities (RI-1a and 1b) was studied amongRattus rattus and a variety of other Asian rodents. No sera other than those ofRattus norvegicus showed the presence of RI-1a (DA type), whereas many cross-reacted with RI-1b (LEW-type). While manyR. rattus showedtotal cross-reactivity with RI-1b, various sera from the generaRattus, Bandicota, andTokudaia showed different levels ofpartial cross-reactivity. These results indicate that (1) anti-RI-1b reagents can detectmultiple specificities on LEW-type kappa chains, and (2) these RI-1b specificities, butnot RI-1a, are widely distributed among murid rodents, in seeming contradiction to amino acid sequence data suggesting that RI-1b is more closely related to ancestral rat kappa chains.