Phylogeography of the introduced species Rattus rattus in the western Indian Ocean,with special emphasis on the colonization history of Madagascar

Aim To describe the phylogeographic patterns of the black rat, Rattus rattus, from islands in the western Indian Ocean where the species has been introduced (Madagascar and the neighbouring islands of Réunion, Mayotte and Grande Comore), in comparison with the postulated source area (India). Location Western Indian Ocean: India, Arabian Peninsula, East Africa and the islands of Madagascar, Réunion, Grande Comore and Mayotte. Methods Mitochondrial DNA (cytochrome b, tRNA and D‐loop, 1762 bp) was sequenced for 71 individuals from 11 countries in the western Indian Ocean. A partial D‐loop (419 bp) was also sequenced for eight populations from Madagascar (97 individuals), which were analysed in addition to six previously published populations from southern Madagascar. Results Haplotypes from India and the Arabian Peninsula occupied a basal position in the phylogenetic tree, whereas those from islands were distributed in different monophyletic clusters: Madagascar grouped with Mayotte, while Réunion and Grand Comore were present in two other separate groups. The only exception was one individual from Madagascar (out of 190) carrying a haplotype that clustered with those from Réunion and South Africa. ‘Isolation with migration’ simulations favoured a model with no recurrent migration between Oman and Madagascar. Mismatch distribution analyses dated the expansion of Malagasy populations on a time‐scale compatible with human colonization history. Higher haplotype diversity and older expansion times were found on the east coast of Madagascar compared with the central highlands. Main conclusions Phylogeographic patterns supported the hypothesis of human‐mediated colonization of R. rattus from source populations in either the native area (India) or anciently colonized regions (the Arabian Peninsula) to islands of the western Indian Ocean. Despite their proximity, each island has a distinct colonization history. Independent colonization events may have occurred simultaneously in Madagascar and Grande Comore, whereas Mayotte would have been colonized from Madagascar. Réunion was colonized independently, presumably from Europe. Malagasy populations may have originated from a single successful colonization event, followed by rapid expansion, first in coastal zones and then in the central highlands. The congruence of the observed phylogeographic pattern with human colonization events and pathways supports the potential relevance of the black rat in tracing human history.     

Isolation and characterization of microsatellites in Rattus rattus

We isolated and characterized 10 microsatellite loci in the black rat Rattus rattus (Muridae, Rodentia), a widespread invasive species largely known to cause serious problems in agriculture and human health. Polymorphism was studied in two populations, one from Madagascar and one from Senegal. It ranged from three to 12 alleles in Madagascar, and from two to five alleles in Senegal. Together with the loci previously adapted from Rattus norvegicus, this set of markers should allow the conduct of thorough studies on the genetic structure of natural populations of R. rattus.     

Beyond an AFLP genome scan towards the identification of immune genes involved in plague resistance in Rattus rattus from Madagascar

Genome scans using amplified fragment length polymorphism (AFLP) markers became popular in nonmodel species within the last 10 years, but few studies have tried to characterize the anonymous outliers identified. This study follows on from an AFLP genome scan in the black rat (Rattus rattus), the reservoir of plague (Yersinia pestis infection) in Madagascar. We successfully sequenced 17 of the 22 markers previously shown to be potentially affected by plague‐mediated selection and associated with a plague resistance phenotype. Searching these sequences in the genome of the closely related species Rattus norvegicus assigned them to 14 genomic regions, revealing a random distribution of outliers in the genome (no clustering). We compared these results with those of an in silico AFLP study of the R. norvegicus genome, which showed that outlier sequences could not have been inferred by this method in R. rattus (only four of the 15 sequences were predicted). However, in silico analysis allowed the prediction of AFLP markers distribution and the estimation of homoplasy rates, confirming its potential utility for designing AFLP studies in nonmodel species. The 14 genomic regions surrounding AFLP outliers (less than 300 kb from the marker) contained 75 genes encoding proteins of known function, including nine involved in immune function and pathogen defence. We identified the two interleukin 1 genes (Il1a and Il1b) that share homology with an antigen of Y. pestis, as the best candidates for genes subject to plague‐mediated natural selection. At least six other genes known to be involved in proinflammatory pathways may also be affected by plague‐mediated selection.     

Systematics of the black rat in Madagascar: consequences for the transmission and distribution of plague

The plague has been present for a century in Madagascar; the only known reservoir is the black rat, which is also the main victim of this disease. Whereas the two plague foci are restricted to an altitude above 800 m, the black rat is distributed over the whole island, the only morphological variation being a within-site variability in belly colour. To resolve these apparent contradictions, an analysis of the different belly colour morphs and of populations living in different habitats and altitudes was undertaken. An allozymic study demonstrated that sympatric white- and grey-bellied rats ( N  = 26) living within the plague foci, all belonged to the same species: Rattus rattus . This specific assignment was confirmed by a chromosomal analysis which showed that all 90 individuals studied presented the same diploid number, 2 n  = 38, whatever the habitat and altitude. This study indicates that all specimens investigated in Madagascar could be referred to the same black rat species. Survival of rat populations, despite a century of coexistence with the plague, is most likely related to their high reproductive and recolonization potential, as well as selection of plague resistant genotypes. As the altitudinal limit of the plague foci does not seem to be related to characteristics of the rodent reservoir, investigations concerning the vectors are now essential.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 335–341.     

Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus)

The stepwise colonization of islands within an archipelago is typically punctuated by successive founder effects, with each newly founded population being a subsample of the gene pool of the source island. Thus, the genetic signature of successive bottlenecks should be detected when analysing the genetic structure between islands of an archipelago. To test this prediction, we investigated introduced ship rat populations, Rattus rattus (Linnaeus, 1758), in the Guadeloupe Archipelago. Three different methods, commonly named the heterozygosity excess, the mode-shift indicator and the M ratio method, were used to detect bottlenecks from genetic data obtained with eight microsatellite markers on Guadeloupe and two neighbouring islands, Petite-Terre and Fajou. Moreover, a recent eradication failure on Fajou allowed us to test the accuracy of the methods in an 'experimental-like' situation. The results indicate that rats were introduced on Guadeloupe first, which then became the source population for independent secondary colonization of Fajou and Petite-Terre. Moreover, the heterozygosity excess and the mode-shift indicator only detected bottlenecks for the recent colonization of Petite-Terre and the eradication failure on Fajou. However, bottlenecks were detected for all the populations using the M ratio method. This could be interpreted as the remaining signature of the early introduction of the ship rat in the archipelago.     

Disease and competition,not just predation,as drivers of impacts of the black rat (Rattus rattus) on island mammals

Hanna & Cardillo (2014) report an association between the presence of black rats (Rattus rattus) and extinctions of endemic mammals on Australian islands. Although we agree that introductions of the black rat are likely to have had a significant impact on island ecosystems, we suggest that there is little empirical support for their main conclusion, that predation (and thus mesopredator processes) is the causal mechanism driving the association between the presence of black rats and extinctions of native mammals on Australian islands. We present a brief literature review of evidence for two alternative mechanisms – introduction of novel diseases and competition – which suggest there are multiple explanations for how native mammal extinctions on Australian islands may have occurred. The potential impact of these processes interacting across different trophic levels is rarely considered, but is applicable across many different ecosystems world‐wide.     

Denning behaviour of ship rats (Rattus rattus) on Taukihepa,a seabird breeding island

Abstract

Den sites of 14 ship rats (Rattus rattus) were located daily during the rat breeding season on Taukihepa (Big South Cape), a seabird island southwest of Rakiura (Stewart Island). In contrast to other New Zealand studies, no arboreal dens were found. Den sites on Taukihepa were in ferns, under logs, in woodpiles, or underground in sooty shearwater (Puffinusgriseus) breeding burrows. The number of times known den sites used was positively related to the amount of leaf litter and woodpiles near the den sites. Overall, 24% of radio‐tagged rats were sharing den sites on any given day. While there was considerable individual variation in the number of times den sites were used, female rats tended to reuse den sites more than males. Many rats were found in dens alone, but frequently males and females shared. Occasionally two females and one male denned together, as did two females, whereas males never denned with another male.     

The home range of ship rats (Rattus rattus) in beech forest in the Eglinton Valley,Fiordland, New Zealand: A pilot study

Abstract

Three male and two female ship rats (Rattus rattus) were radio‐tagged and tracked in beech (Nothofagus) forest in the Eglinton Valley, Fiordland, New Zealand over two field periods in 1996 and 2000. The home range of each animal was calculated using the minimum convex polygon method. Ranges of three male rats were 7.5, 9.1, and 11.4 ha whereas those of the female rats were 0.89 and 0.27 ha. The home ranges recorded for male rats were considerably larger than those reported from other studies in non‐beech forest. Ship rats are important predators of forest birds, and home range information could be used to provide a guide for trap or bait station spacing in beech forests. To carry out rat control in beech forests effectively, further studies are needed to determine if the results of this pilot study are typical, and if home ranges of ship rats change with season, or at various stages of the beech mast cycle.     

Use of habitat by the black rat (Rattus rattus) at North Head,New South Wales: an observational and experimental study

This study investigated the habitats used by an introduced species of rodent, the black rat Rattus rattus (Linnaeus), at North Head in New South Wales, Australia. At a coarse scale, combined live‐trapping and radio‐tracking indicated that animals used forest proportionately more than open, heath or scrub macrohabitats that were available. To identify the components contributing to this pattern, microhabitat use was assessed by scoring vegetative and structural features around trap stations, and by using spool‐and‐line tracking. The results indicated that rats preferred microhabitats providing a deep cover of leaf litter and dense understorey with numerous vertical stems. As statistical analysis did not distinguish which of these components was more important in determining habitat use, we designed an experiment to test the importance of a single component: leaf litter. Cover of litter was enhanced experimentally at 75 trap stations and reduced at 75 others, and the response of rats monitored by live‐trapping on two occasions. Although no clear response was found in the first run of the experiment, due to low numbers, rats strongly selected trap stations with enhanced leaf litter in the second run. These results indicate that litter cover affects use of habitat by the black rat. Access to food resources and avoidance of predators may contribute to the observed local patterns of abundance.     

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.     

Hair type,intake, and detection method influence Rhodamine B detectability

Rhodamine B (RB) is a popular bait-marking tool in wildlife research, although its use has required many assumptions about marking reliability. These assumptions have limited dosage ranges and detection methods in research applications. Identification of alternate detection methods, hair types, and dosage rates could create new opportunities for RB use and potentially reduce adverse effects on target animals. We examined the relationship between hair types, dosage rate, and detection method for RB applications using black rats (Rattus rattus) in laboratory settings. We gave study animals varying doses of RB, and examined vibrissae and guard hairs for the detection of RB bands using ambient light, ultraviolet (UV) light, and fluorescence microscopy techniques. Fluorescence microscopy detected more RB marked hairs than UV light or ambient light. Fluorescence microscopy was more sensitive to RB dose rate detection; with receiver operating characteristic curves suggesting that the minimum dose rates at which RB intake can be correctly detected are 3.9 and 33 mg/kg for vibrissae and guard hairs, respectively. Guard hair RB detection was less reliable under ambient light and UV lamps, but equally detectable as vibrissae under fluorescence microscopy. Our results confirmed the interrelationship between dosage and detection methods in the efficacy of bait markers. We demonstrated that guard hairs can be a reliable hair type for the detection of RB. This application is less invasive than sampling animal tissues to detect bait uptake. © 2012 The Wildlife Society.     

Invasion genetics of a human commensal rodent: the black rat Rattus rattus in Madagascar

Studies focusing on geographical genetic patterns of commensal species and on human history complement each other and provide proxies to trace common colonization events. On Madagascar, the unintentional introduction and spread of the commensal species Rattus rattus by people may have left a living clue of human colonization patterns and history. In this study, we addressed this question by characterizing the genetic structure of natural populations of R. rattus using both microsatellites and mitochondrial sequences, on an extensive sampling across the island. Such data sets were analysed by a combination of methods using population genetics, phylogeography and approximate Bayesian computation. Our results indicated two introduction events to Madagascar from the same ancestral source of R. rattus, one in the extreme north of the island and the other further south. The latter was the source of a large spatial expansion, which may have initially started from an original point located on the southern coast. The inferred timing of introduction events—several centuries ago—is temporally congruent with the Arabian trade network in the Indian Ocean, which was flourishing from the middle of the first millennium.     

Tooth wear patterns in black rats (Rattus rattus) of Madagascar differ more in relation to human impact than to differences in natural habitats

Dietary characteristics and environmental variables are important selective factors directing ecological diversification in rodents. On Madagascar, the introductions and spread of the commensal black rat (Rattus rattus) can be seen as example cases to study dietary niche occupation and dietary adaptation in an insular environment. We investigate how tooth wear as a measure of dietary adaptation of black rats differs between four distinct habitats (village, manioc fields, spiny forest, and rainforest) with different dietary resources. We use the 3D surface texture analysis (3DST, using 30 parameters according to ISO 25178) as a measure of dietary abrasiveness. 3DST is applied on the occlusal surface of the upper first molar of 37 black rat specimens. The rainforest sample displays less rough and less voluminous surface textures compared to the village samples as indicated by smaller values for height parameters (Sa, Sp, Sq), inverse areal material ratio (Smc), and volume parameters (Vm, Vmc, Vmp, Vv, and Vvc). We therefore rank sampling areas from highest to lowest abrasiveness (village>manioc fields/spiny forest>rainforest). The rats from villages and rainforest differ to such an extent that one could have interpreted them to belong to different species. This indicates a high degree of variability in terms of ingesta abrasiveness. Furthermore, the pronounced difference between rats from human habitations compared to rats from associated fields or natural vegetation is interpreted to clearly indicate shifts in dietary niche occupation in relation to human impact.     

Seasonal patterns of rodents, fleas and plague status in the Western Usambara Mountains, Tanzania

Field and commensal rodents were live-trapped at three villages in an active focus of plague (Yersinia pseudotuberculosis pestis) in Lushoto District, Western Usambara Mountains, Tanga Region, Tanzania, from December 1983 to November 1984. Their flea ectoparasites were collected, identified and counted. The rodent carcasses were serologically examined for specific plague antibodies and antigens, and bacteriologically examined for bipolar staining bacilli. A total of 1758 traps were set during the 12-month period and 924 animals were caught. From these, 1037 fleas were collected. Rattus rattus (L.), Praomys natalensis (Smith) and Lophuromys flavopunctatus Thomas comprised the largest proportions of the rodent population, while Dinopsyllus lypusus Jordan & Rothschild, Ctenophthalmus calceatus Waterston and Xenopsylla brasiliensis (Baker) were the dominant flea species. Rodents were most abundantly trapped during December and January. Flea indices were highest from December to May. Human plague was most active from November to March. Rodents contained plague antibodies every month except May and July, with a peak in September. Plague antigens and bipolar bacilli were detected in rodent organs during January-April. From the product of abundance and infection rate, the most prevalent rodent hosts of plague appeared to be R. rattus, Otomys angoniensis Wroughton, P. natalensis and Pelomys fallax (Peters). Continuous integrated control of rodents and fleas was recommended, reinforced by quarantine and maintenance of a surveillance service for clinical detection, diagnosis and treatment of patients in the plague endemic area.     

Madagascar Fish Eagle productivity in the Tsimembo-Manambolomaty Protected Area and surrounding habitat of western Madagascar

We monitored the productivity of the critically endangered Madagascar Fish Eagle Haliaeetus vociferoides inside and outside of the Tsimembo-Manambolomaty Protected Area (T-M PA), western Madagascar from 2010 to 2015. We recorded 14 breeding pairs inside and 13 outside T-M PA. The T-M PA and surrounding habitat hosted respectively 10 and six breeding polyandrous pairs, composed of one adult female and two adult males. During the six-year study period, 101 eggs were laid in nests in T-M PA of which 60 hatched and 58 young fledged. We recorded 62 eggs laid in nests outside the T-M PA of which 39 hatched and 36 young fledged. Productivity was similar at both sites, inside and outside T-M PA, with 0.84 (58/69) and 0.76 (36/47) fledgling per nesting attempt and 0.69 (58/84) and 0.5 (36/72) fledglings per territorial pair, respectively. Polyandrous pairs have higher productivity compared with normal pairs. Threats to Madagascar Fish Eagles and their habitat were low due to the existence of a community-based resource management system called the Local Management Secured System (GELOSE) inside and outside the T-M PA. This system is based on strengthening local traditional customs and rules, and involving local people in managing their natural resources sustainably along with biodiversity conservation.     

Genotyping of Toxoplasma gondii from Rats (Rattus rattus) in Riyadh,Saudi Arabia

Toxoplasma 3 main clonal lineages are designated as type I, II, and III; however, atypical and mixed genotypes were also reported. This study was conducted for detection of Toxoplasma gondii genotypes in rats (Rattus rattus) in Riyadh region, Saudi Arabia. PCR test on T. gondii B1 gene was conducted on ELISA IgM positive samples for confirmation of the infection. However, genetic analysis of the SAG2 locus was performed to determine T. gondii genotypes using PCR-RFLP technique. PCR test on T. gondii B1gene showed that 22 (81.5%) out of the 27 ELISA IgM positive samples have T. gondii DNA. Genotypic analysis shows that, of the total 22 PCR positive samples, only 13 (59.1%) were of type II, 7 (31.8%) were of type III, and 2 (9.1%) were of an unknown genotype. It is obvious that the prevalence of both type II and III is high in rats. No reports have been available on T. gondii genotypes among rats in Riyadh region, and only little is known about its seroprevalence in rats. Future studies on T. gondii genotypes in rats using multi-locus markers is needed in Riyadh region, Saudi Arabia for better understanding of T. gondii pathogenesis and treatment in humans and animals.