Publications by authors named "Steven M Goodman"

95 Publications

Diversity, distribution, and drivers of Polychromophilus infection in Malagasy bats.

Malar J 2021 03 20;20(1):157. Epub 2021 Mar 20.

Institut Pasteur de Madagascar, Antananarivo 101, BP 1274, Ambatofotsikely, Madagascar.

Background: Numerous studies have been undertaken to advance knowledge of apicomplexan parasites infecting vertebrates, including humans. Of these parasites, the genus Plasmodium has been most extensively studied because of the socio-economic and public health impacts of malaria. In non-human vertebrates, studies on malaria or malaria-like parasite groups have been conducted but information is far from complete. In Madagascar, recent studies on bat blood parasites indicate that three chiropteran families (Miniopteridae, Rhinonycteridae, and Vespertilionidae) are infected by the genus Polychromophilus with pronounced host specificity: Miniopterus spp. (Miniopteridae) harbour Polychromophilus melanipherus and Myotis goudoti (Vespertilionidae) is infected by Polychromophilus murinus. However, most of the individuals analysed in previous studies were sampled on the western and central portions of the island. The aims of this study are (1) to add new information on bat blood parasites in eastern Madagascar, and (2) to highlight biotic and abiotic variables driving prevalence across the island.

Methods: Fieldworks were undertaken from 2014 to 2016 in four sites in the eastern portion of Madagascar to capture bats and collect biological samples. Morphological and molecular techniques were used to identify the presence of haemosporidian parasites. Further, a MaxEnt modelling was undertaken using data from Polychromophilus melanipherus to identify variables influencing the presence of this parasite RESULTS: In total, 222 individual bats belonging to 17 species and seven families were analysed. Polychromophilus infections were identified in two families: Miniopteridae and Vespertilionidae. Molecular data showed that Polychromophilus spp. parasitizing Malagasy bats form a monophyletic group composed of three distinct clades displaying marked host specificity. In addition to P. melanipherus and P. murinus, hosted by Miniopterus spp. and Myotis goudoti, respectively, a novel Polychromophilus lineage was identified from a single individual of Scotophilus robustus. Based on the present study and the literature, different biotic and abiotic factors are shown to influence Polychromophilus infection in bats, which are correlated based on MaxEnt modelling.

Conclusions: The present study improves current knowledge on Polychromophilus blood parasites infecting Malagasy bats and confirms the existence of a novel Polychromophilus lineage in Scotophilus bats. Additional studies are needed to obtain additional material of this novel lineage to resolve its taxonomic relationship with known members of the genus. Further, the transmission mode of Polychromophilus in bats as well as its potential effect on bat populations should be investigated to complement the results provided by MaxEnt modelling and eventually provide a comprehensive picture of the biology of host-parasite interactions.
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http://dx.doi.org/10.1186/s12936-021-03696-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7980569PMC
March 2021

Evolutionary history of Carnivora (Mammalia, Laurasiatheria) inferred from mitochondrial genomes.

PLoS One 2021 16;16(2):e0240770. Epub 2021 Feb 16.

Institut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, MNHN, CNRS, EPHE, UA, Paris, France.

The order Carnivora, which currently includes 296 species classified into 16 families, is distributed across all continents. The phylogeny and the timing of diversification of members of the order are still a matter of debate. Here, complete mitochondrial genomes were analysed to reconstruct the phylogenetic relationships and to estimate divergence times among species of Carnivora. We assembled 51 new mitogenomes from 13 families, and aligned them with available mitogenomes by selecting only those showing more than 1% of nucleotide divergence and excluding those suspected to be of low-quality or from misidentified taxa. Our final alignment included 220 taxa representing 2,442 mitogenomes. Our analyses led to a robust resolution of suprafamilial and intrafamilial relationships. We identified 21 fossil calibration points to estimate a molecular timescale for carnivorans. According to our divergence time estimates, crown carnivorans appeared during or just after the Early Eocene Climatic Optimum; all major groups of Caniformia (Cynoidea/Arctoidea; Ursidae; Musteloidea/Pinnipedia) diverged from each other during the Eocene, while all major groups of Feliformia (Nandiniidae; Feloidea; Viverroidea) diversified more recently during the Oligocene, with a basal divergence of Nandinia at the Eocene/Oligocene transition; intrafamilial divergences occurred during the Miocene, except for the Procyonidae, as Potos separated from other genera during the Oligocene.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0240770PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7886153PMC
July 2021

Effects of land use, habitat characteristics, and small mammal community composition on Leptospira prevalence in northeast Madagascar.

PLoS Negl Trop Dis 2020 12 31;14(12):e0008946. Epub 2020 Dec 31.

Evolutionary Anthropology, Duke University, Durham North Carolina, United States of America.

Human activities can increase or decrease risks of acquiring a zoonotic disease, notably by affecting the composition and abundance of hosts. This study investigated the links between land use and infectious disease risk in northeast Madagascar, where human subsistence activities and population growth are encroaching on native habitats and the associated biota. We collected new data on pathogenic Leptospira, which are bacteria maintained in small mammal reservoirs. Transmission can occur through close contact, but most frequently through indirect contact with water contaminated by the urine of infected hosts. The probability of infection and prevalence was compared across a gradient of natural moist evergreen forest, nearby forest fragments, flooded rice and other types of agricultural fields, and in homes in a rural village. Using these data, we tested specific hypotheses for how land use alters ecological communities and influences disease transmission. The relative abundance and proportion of exotic species was highest in the anthropogenic habitats, while the relative abundance of native species was highest in the forested habitats. Prevalence of Leptospira was significantly higher in introduced compared to endemic species. Lastly, the probability of infection with Leptospira was highest in introduced small mammal species, and lower in forest fragments compared to other habitat types. Our results highlight how human land use affects the small mammal community composition and in turn disease dynamics. Introduced species likely transmit Leptospira to native species where they co-occur, and may displace the Leptospira species naturally occurring in Madagascar. The frequent spatial overlap of people and introduced species likely also has consequences for public health.
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http://dx.doi.org/10.1371/journal.pntd.0008946DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7774828PMC
December 2020

Genetic origins and diversity of bushpigs from Madagascar (Potamochoerus larvatus, family Suidae).

Sci Rep 2020 11 26;10(1):20629. Epub 2020 Nov 26.

Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Sydney, NSW, 2006, Australia.

The island of Madagascar, situated off the southeast coast of Africa, shows the first evidence of human presence ~ 10,000 years ago; however, other archaeological data indicates a settlement of the modern peoples of the island distinctly more recent, perhaps > 1500 years ago. Bushpigs of the genus Potamochoerus (family Suidae), are today widely distributed in Madagascar and presumed to have been introduced from Africa at some stage by human immigrants to the island. However, disparities about their origins in Madagascar have been presented in the literature, including the possibility of endemic subspecies, and few empirical data are available. Furthermore, the separation of bushpigs in Madagascar from their mainland relatives may have favoured the evolution of a different repertoire of immune genes first due to a founder effect and then as a response to distinct pathogens compared to their ancestors. Molecular analysis confirmed the species status of the bushpig in Madagascar as P. larvatus, likely introduced from the central region of southern Africa, with no genetic evidence for the recognition of eastern and western subspecies as suggested from previous cranial morphology examination. Investigation of the immunologically important SLA-DQB1 peptide-binding region showed a different immune repertoire of bushpigs in Madagascar compared to those on the African mainland, with seventeen exon-2 haplotypes unique to bushpigs in Madagascar (2/28 haplotypes shared). This suggests that the MHC diversity of the Madagascar populations may have enabled Malagasy bushpigs to adapt to new environments.
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http://dx.doi.org/10.1038/s41598-020-77279-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693328PMC
November 2020

Description of three new species of Ixodes Latreille, 1795 (Acari: Ixodidae), parasites of tenrecs (Afrotheria: Tenrecidae) on Madagascar.

Syst Parasitol 2020 12 5;97(6):623-637. Epub 2020 Nov 5.

Integrative Research Center, Field Museum of Natural History, Chicago, IL, 60605, USA.

Ixodes soarimalalae n. sp., Ixodes uilenbergi n. sp. and Ixodes uncus n. sp. (Acari: Ixodidae), are described based on females ex various species of tenrecs (Afrosoricida: Tenrecidae) from Madagascar. Females of all of these new species are similar to those of other species of the subgenus Afrixodes Morel, 1966 known from Madagascar, from which they can be distinguished and from one other by the size of scutum, size of scutal setae, shape of alloscutal setae, shape of genital aperture, development of genital apron, size of auriculae, size of anterior angle of basis capituli, size of palpi, dental formula on hypostome and size and development of spurs on coxa I.
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http://dx.doi.org/10.1007/s11230-020-09944-2DOI Listing
December 2020

Description of a new species of Haemaphysalis Koch, 1844 (Acari: Ixodidae) from the H. (Rhipistoma) asiatica subgroup, parasite of an endemic Malagasy carnivoran (Carnivora: Eupleridae).

Syst Parasitol 2020 12 15;97(6):591-599. Epub 2020 Oct 15.

Integrative Research Center, Field Museum of Natural History, Chicago, Illinois, 60605, USA.

Haemaphysalis (Rhipistoma) galidiae n. sp. (Acari: Ixodidae) is described herein based on males and a single female. Adults of H. galidiae n. sp. were collected from the ring-tailed vontsira, Galidia elegans Geoffroy Saint-Hilaire (Carnivora: Eupleridae) on Madagascar. Males and the single female of this new species morphologically are most close to H. obtusa Dönitz, 1910, known from various Malagasy euplerid carnivorans, including G. elegans, as well as introduced carnivorans, but can be differentiated from it by the shape of the female genital aperture, shape of posterolateral margin of palpal segment II ventrally in both male and female and shape and size of spurs on palpal segment II, coxa I and trochanter I in both sexes.
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http://dx.doi.org/10.1007/s11230-020-09943-3DOI Listing
December 2020

Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (Chiroptera, Hipposideridae).

Zookeys 2020 22;929:117-161. Epub 2020 Apr 22.

Negaunee Integrative Research Center, Field Museum of Natural History, Chicago IL 60605, USA Field Museum of Natural History Chicago United States of America.

The Old World leaf-nosed bats (Hipposideridae) are aerial and gleaning insectivores that occur throughout the Paleotropics. Both their taxonomic and phylogenetic histories are confused. Until recently, the family included genera now allocated to the Rhinonycteridae and was recognized as a subfamily of Rhinolophidae. Evidence that Hipposideridae diverged from both Rhinolophidae and Rhinonycteridae in the Eocene confirmed their family rank, but their intrafamilial relationships remain poorly resolved. We examined genetic variation in the Afrotropical hipposiderids , , and using relatively dense taxon-sampling throughout East Africa and neighboring regions. Variation in both mitochondrial (cyt-b) and four nuclear intron sequences (ACOX2, COPS, ROGDI, STAT5) were analyzed using both maximum likelihood and Bayesian inference methods. We used intron sequences and the lineage delimitation method BPP-a multilocus, multi-species coalescent approach-on supported mitochondrial clades to identify those acting as independent evolutionary lineages. The program StarBEAST was used on the intron sequences to produce a species tree of the sampled Afrotropical hipposiderids. All genetic analyses strongly support generic monophyly, with and as Afrotropical sister genera distinct from a Paleotropical ; mitochondrial analyses interpose the genera , , and between these clades. Mitochondrial analyses also suggest at least two separate colonizations of Africa by Asian groups of , but the actual number and direction of faunal interchanges will hinge on placement of the unsampled African-Arabian species . Mitochondrial sequences further identify a large number of geographically structured clades within species of all three genera. However, in sharp contrast to this pattern, the four nuclear introns fail to distinguish many of these groups and their geographic structuring disappears. Various distinctive mitochondrial clades are consolidated in the intron-based gene trees and delimitation analyses, calling into question their evolutionary independence or else indicating their very recent divergence. At the same time, there is now compelling genetic evidence in both mitochondrial and nuclear sequences for several additional unnamed species among the Afrotropical . Conflicting appraisals of differentiation among the Afrotropical hipposiderids based on mitochondrial and nuclear loci must be adjudicated by large-scale integrative analyses of echolocation calls, quantitative morphology, and geometric morphometrics. Integrative analyses will also help to resolve the challenging taxonomic issues posed by the diversification of the many lineages associated with and .
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http://dx.doi.org/10.3897/zookeys.929.50240DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197329PMC
April 2020

Comparative assessment on rodent impacts and cultural perceptions of ecologically based rodent management in 3 Afro-Malagasy farming regions.

Integr Zool 2020 Nov 25;15(6):578-594. Epub 2020 Jun 25.

Natural Resources Institute, University of Greenwich, Kent, UK.

Rodents generate negative consequences for smallholder farmers in Africa that directly impact household and livestock damage, food security, and public health. Ecologically Based Rodent Management (EBRM) seeks sustainable solutions for the mitigation of rodent damage through assessments of rodent population dynamics, agro-ecosystems, and socio-cultural contexts. We adopt a comparative approach across 3 rural Afro-Malagasy smallholder farming regions in South Africa, Tanzania, and Madagascar to assess the household impacts of rodent pests and current perceptions and preferences associated with several rodent control measures. We conducted focus group questionnaires and interviews in different study site locations. Rodents assert multiple impacts on Afro-Malagasy farmers demonstrating recurrent and emerging agricultural and household costs, and public health impacts. We identify a significant knowledge gap in educating communities about the application of different EBRM approaches in favor of acute poisons that are perceived to be more effective. Cultural issues and taboos also have a significant impact on the social acceptance of rodent hunting as well as biological control using indigenous predators. We advocate for an enhanced investigation of the socio-cultural beliefs associated with different rodent practices to understand the factors underlying social acceptance. A collaborative approach that integrates the perspectives of target communities to inform the design of EBRM initiatives according to the specific agro-ecosystem and socio-cultural context is necessary to ensure programmatic success.
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http://dx.doi.org/10.1111/1749-4877.12447DOI Listing
November 2020

Bat coronavirus phylogeography in the Western Indian Ocean.

Sci Rep 2020 04 23;10(1):6873. Epub 2020 Apr 23.

Université de La Réunion, UMR Processus Infectieux en Milieu Insulaire Tropical (PIMIT), INSERM 1187, CNRS 9192, IRD 249, Sainte-Clotilde, La Réunion, France.

Bats provide key ecosystem services such as crop pest regulation, pollination, seed dispersal, and soil fertilization. Bats are also major hosts for biological agents responsible for zoonoses, such as coronaviruses (CoVs). The islands of the Western Indian Ocean are identified as a major biodiversity hotspot, with more than 50 bat species. In this study, we tested 1,013 bats belonging to 36 species from Mozambique, Madagascar, Mauritius, Mayotte, Reunion Island and Seychelles, based on molecular screening and partial sequencing of the RNA-dependent RNA polymerase gene. In total, 88 bats (8.7%) tested positive for coronaviruses, with higher prevalence in Mozambican bats (20.5% ± 4.9%) as compared to those sampled on islands (4.5% ± 1.5%). Phylogenetic analyses revealed a large diversity of α- and β-CoVs and a strong signal of co-evolution between CoVs and their bat host species, with limited evidence for host-switching, except for bat species sharing day roost sites. These results highlight that strong variation between islands does exist and is associated with the composition of the bat species community on each island. Future studies should investigate whether CoVs detected in these bats have a potential for spillover in other hosts.
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http://dx.doi.org/10.1038/s41598-020-63799-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7181612PMC
April 2020

Speciation and gene flow in two sympatric small mammals from Madagascar, Microgale fotsifotsy and M. soricoides (Mammalia: Tenrecidae).

Mol Ecol 2020 05 11;29(9):1717-1729. Epub 2020 May 11.

University of Alaska Museum, Fairbanks, AK, USA.

Madagascar's shrew tenrecs (Mammalia: Tenrecidae; Microgale, Nesogale) represent an excellent system for studying speciation. Most species are endemic to the island's eastern humid forests, a region renowned for high levels of biodiversity and a high rate of in situ diversification. We set out to understand the speciation dynamics in a clade of recently described taxa: Microgale fotsifotsy and M. soricoides, which have nearly identical distributions in the moist evergreen forest, and M. nasoloi, which occurs in the western dry deciduous forest. A phylogenetic analysis using mitochondrial DNA data recovered two distinct clades of M. fotsifotsy: a south clade that is sister to, and broadly sympatric with, M. soricoides, and a north clade that is sister to the dry-forest and distantly allopatric species M. nasoloi. To better understand this result, we analysed cranioskeletal measurements and performed demographic analyses using nuclear sequence data from ultraconserved elements. Nuclear data did not support a sister relationship between M. soricoides and the south clade of M. fotsifotsy but did demonstrate introgression between these clades, which probably explains the discordance between nuclear and mitochondrial phylogenies. Demographic analyses also revealed the absence of gene flow between the north and south clades of M. fotsifotsy. Morphometric data revealed several major differences between M. soricoides and M. fotsifotsy, as well as more subtle differences between the two clades of M. fotsifotsy. In light of these results, we treat the south clade of M. fotsifotsy as a new candidate species. Our findings demonstrate the utility of integrating multiple data types to understand complex speciation histories, and contribute to a growing body of evidence that species diversity on Madagascar is underestimated.
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http://dx.doi.org/10.1111/mec.15433DOI Listing
May 2020

Molecular phylogenetics of slit-faced bats (Chiroptera: Nycteridae) reveal deeply divergent African lineages.

J Zool Syst Evol Res 2019 Nov 20;57(4):1019-1038. Epub 2019 Aug 20.

Integrative Research Center, Field Museum of Natural History Chicago Illinois.

The bat family Nycteridae contains only the genus , which comprises 13 currently recognized species from Africa and the Arabian Peninsula, one species from Madagascar, and two species restricted to Malaysia and Indonesia in South-East Asia. We investigated genetic variation, clade membership, and phylogenetic relationships in Nycteridae with broad sampling across Africa for most clades. We sequenced mitochondrial cytochrome () and four independent nuclear introns (2,166 bp) from 253 individuals. Although our samples did not include all recognized species, we recovered at least 16 deeply divergent monophyletic lineages using independent mitochondrial and multilocus nuclear datasets in both gene tree and species tree analyses. Mean pairwise uncorrected genetic distances among species-ranked clades (17% for and 4% for concatenated introns) suggest high levels of phylogenetic diversity in Nycteridae. We found a large number of designated clades whose members are distributed wholly or partly in East Africa (10 of 16 clades), indicating that diversity has been historically underestimated and raising the possibility that additional unsampled and/or undescribed species occur in more poorly sampled Central and West Africa. Well-resolved mitochondrial, concatenated nuclear, and species trees strongly supported African ancestry for SE Asian species. Species tree analyses strongly support two deeply diverged subclades that have not previously been recognized, and these clades may warrant recognition as subgenera. Our analyses also strongly support four traditionally recognized species groups of . Mitonuclear discordance regarding geographic population structure in appears to result from male-biased dispersal in this species. Our analyses, almost wholly based on museum voucher specimens, serve to identify species-rank clades that can be tested with independent datasets, such as morphology, vocalizations, distributions, and ectoparasites. Our analyses highlight the need for a comprehensive revision of Nycteridae.
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http://dx.doi.org/10.1111/jzs.12313DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6919933PMC
November 2019

Sympatric lineages in the Mantidactylus ambreensis complex of Malagasy frogs originated allopatrically rather than by in-situ speciation.

Mol Phylogenet Evol 2020 03 3;144:106700. Epub 2019 Dec 3.

Department of Evolutionary Biology, Zoologisches Institut, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany. Electronic address:

Madagascar's biota is characterized by a high degree of microendemism at different taxonomic levels, but how colonization and in-situ speciation contribute to the assembly of local species communities has rarely been studied on this island. Here we analyze the phylogenetic relationships of riparian frogs of the Mantidactylus ambreensis species complex, which is distributed in the north of Madagascar and was originally described from Montagne d'Ambre, an isolated mountain of volcanic origin, currently protected within Montagne d'Ambre National Park (MANP). Data from mitochondrial DNA, and phylogenomic data from FrogCap, a sequence capture method, independently confirm that this species complex is monophyletic within the subgenus Ochthomantis, and identify two main clades within it. These two clades are separated by 5.6-6.8% pairwise distance in the mitochondrial 16S rRNA gene and co-occur in MANP, with one distributed at high elevations (940-1375 m a.s.l.) and the other at lower elevations (535-1010 m a.s.l.), but show almost no haplotype sharing in the nuclear RAG1 gene. This occurrence in syntopy without admixture confirms them as independent evolutionary lineages that merit recognition as separate species, and we here refer to them as high-elevation (HE) and low-elevation (LE) lineage; they will warrant taxonomic assessment to confidently assign the name ambreensis to one or the other. Populations of the M. ambreensis complex from elsewhere in northern Madagascar all belong to the LE lineage, although they do occur over a larger elevational range than in Montagne d'Ambre (285-1040 m a.s.l.). Within LE there are several phylogroups (LE1-LE4) of moderately deep divergence (1.5-2.8% in 16S), but phylogroup LE4 that occurs in MANP has a deeply nested phylogenetic position, as recovered separately by mitochondrial and sequence capture datasets. This suggests that HE and LE did not diverge by a local fission of lower and upper populations, but instead arose through a more complex biogeographic scenario. The branching pattern of phylogroups LE1-LE4 shows a clear south-to-north phylogeographic pattern. We derive from these results a testable hypothesis of vicariant speciation that restricted the HE lineage to MANP and the LE candidate species to a climatic refugium further south, with subsequent northwards range expansion and secondary colonization of MANP by LE. These results provide an example for complex assembly of local microendemic amphibian faunas on Madagascar.
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http://dx.doi.org/10.1016/j.ympev.2019.106700DOI Listing
March 2020

Molecular phylogenetics of the African horseshoe bats (Chiroptera: Rhinolophidae): expanded geographic and taxonomic sampling of the Afrotropics.

BMC Evol Biol 2019 08 22;19(1):166. Epub 2019 Aug 22.

Integrative Research Center, Field Museum of Natural History, Chicago, IL, 60605, USA.

Background: The Old World insectivorous bat genus Rhinolophus is highly speciose. Over the last 15 years, the number of its recognized species has grown from 77 to 106, but knowledge of their interrelationships has not kept pace. Species limits and phylogenetic relationships of this morphologically conservative group remain problematic due both to poor sampling across the Afrotropics and to repeated instances of mitochondrial-nuclear discordance. Recent intensive surveys in East Africa and neighboring regions, coupled with parallel studies by others in West Africa and in Southern Africa, offer a new basis for understanding its evolutionary history.

Results: We investigated phylogenetic relationships and intraspecific genetic variation in the Afro-Palearctic clade of Rhinolophidae using broad sampling. We sequenced mitochondrial cytochrome-b (1140 bp) and four independent and informative nuclear introns (2611 bp) for 213 individuals and incorporated sequence data from 210 additional individuals on GenBank that together represent 24 of the 33 currently recognized Afrotropical Rhinolophus species. We addressed the widespread occurrence of mito-nuclear discordance in Rhinolophus by inferring concatenated and species tree phylogenies using only the nuclear data. Well resolved mitochondrial, concatenated nuclear, and species trees revealed phylogenetic relationships and population structure of the Afrotropical species and species groups.

Conclusions: Multiple well-supported and deeply divergent lineages were resolved in each of the six African Rhinolophus species groups analyzed, suggesting as many as 12 undescribed cryptic species; these include several instances of sympatry among close relatives. Coalescent lineage delimitation offered support for new undescribed lineages in four of the six African groups in this study. On the other hand, two to five currently recognized species may be invalid based on combined mitochondrial and/or nuclear phylogenetic analyses. Validation of these cryptic lineages as species and formal relegation of current names to synonymy will require integrative taxonomic assessments involving morphology, ecology, acoustics, distribution, and behavior. The resulting phylogenetic framework offers a powerful basis for addressing questions regarding their ecology and evolution.
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http://dx.doi.org/10.1186/s12862-019-1485-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6704657PMC
August 2019

Phylogeography of the Rufous Vanga and the role of bioclimatic transition zones in promoting speciation within Madagascar.

Mol Phylogenet Evol 2019 10 14;139:106535. Epub 2019 Jun 14.

Department of Biology, Loyola University Chicago, 1032 W. Sheridan Road, Chicago, IL 60660, USA; Bell Museum of Natural History and Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, St. Paul, MN 55108, USA.

Madagascar is known as a biodiversity hotspot, providing an ideal natural laboratory for investigating the processes of avian diversification. Yet, the phylogeography of Madagascar's avifauna is still largely unexamined. In this study, we evaluated phylogeographic patterns and species limits within the Rufous Vanga, Schetba rufa, a monotypic genus of forest-dwelling birds endemic to the island. Using an integrative taxonomic approach, we synthesized data from over 4000 ultra-conserved element (UCE) loci, mitochondrial DNA, multivariate morphometrics, and ecological niche modeling to uncover two reciprocally monophyletic, geographically circumscribed, and morphologically distinct clades of Schetba. The two lineages are restricted to eastern and western Madagascar, respectively, with distributions broadly consistent with previously described subspecies. Based on their genetic and morphological distinctiveness, the two subspecies merit recognition as separate species. The bioclimatic transition between the humid east and dry west of Madagascar likely promoted population subdivision and drove speciation in Schetba during the Pleistocene. Our study is the first evidence that an East-West bioclimatic transition zone played a role in the speciation of birds within Madagascar.
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http://dx.doi.org/10.1016/j.ympev.2019.106535DOI Listing
October 2019

Evolutionary dynamics of sexual size dimorphism in non-volant mammals following their independent colonization of Madagascar.

Sci Rep 2019 02 5;9(1):1454. Epub 2019 Feb 5.

Field Museum of Natural History, Chicago, IL, USA.

As predicted by sexual selection theory, males are larger than females in most polygynous mammals, but recent studies found that ecology and life history traits also affect sexual size dimorphism (SSD) through evolutionary changes in either male size, female size, or both. The primates of Madagascar (Lemuriformes) represent the largest group of mammals without male-biased SSD. The eco-evo-devo hypothesis posited that adaptations to unusual climatic unpredictability on Madagascar have ultimately reduced SSD in lemurs after dispersing to Madagascar, but data have not been available for comparative tests of the corresponding predictions that SSD is also absent in other terrestrial Malagasy mammals and that patterns of SSD changed following the colonization of Madagascar. We used phylogenetic methods and new body mass data to test these predictions among the four endemic radiations of Malagasy primates, carnivorans, tenrecs, and rodents. In support of our prediction, we found that male-biased SSD is generally absent among all Malagasy mammals. Phylogenetic comparative analyses further indicated that after their independent colonization of Madagascar, SSD decreased in primates and tenrecs, but not in the other lineages or when analyzed across all species. We discuss several mechanisms that may have generated these patterns and conclude that neither the eco-evo-devo hypothesis, founder effects, the island rule nor sexual selection theory alone can provide a compelling explanation for the observed patterns of SSD in Malagasy mammals.
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http://dx.doi.org/10.1038/s41598-018-36246-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6363729PMC
February 2019

Phylogeography and population genetics of the endemic Malagasy bat, s.s. (Chiroptera: Hipposideridae).

PeerJ 2019 17;7:e5866. Epub 2019 Jan 17.

School of Life Sciences, University of Kwa-Zulu Natal, Pietermaritzburg, Kwa-Zulu Natal, South Africa.

(Hipposideridae), a bat species endemic to Madagascar, is widespread across the island and utilizes a range of habitat types including open woodland, degraded habitats, and forested areas from sea level to 1,325 m. Despite being widely distributed, there is evidence that exhibits morphological and bioacoustic variation across its geographical range. We investigated the fine-scale phylogeographic structure of populations in the western half of the island using extensive spatial sampling and sequence data from two mitochondrial DNA regions. Our results indicated several lineages within Individuals collected from northern Madagascar formed a single monophyletic clade (clade C). A second clade (clade B) included individuals collected from the south-western portion of the island. This second clade displayed more phylogeographical partitioning with differences in mtDNA haplotypes frequency detected between populations collected in different bioclimatic regions. Lineage dispersal, genetic divergence, and timing of expansion events of . were probably associated with Pleistocene climate fluctuations. Our data suggest that the northern and the central western regions of Madagascar may have acted as refugia for this species during periods of cooler and drier climate conditions associated with the Pleistocene.
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http://dx.doi.org/10.7717/peerj.5866DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6339777PMC
January 2019

Polychromophilus spp. (Haemosporida) in Malagasy bats: host specificity and insights on invertebrate vectors.

Malar J 2018 Aug 31;17(1):318. Epub 2018 Aug 31.

UMR PIMIT "Processus Infectieux en Milieu Insulaire Tropical", INSERM 1187, CNRS 9192, IRD 249, Plateforme de Recherche CYROI, Université de La Réunion, 97490, Sainte Clotilde, La Réunion, France.

Background: Bats are home to diverse haemosporidian parasites namely Plasmodium and Plasmodium-related. While information is available at a worldwide level, haemosporidian infection in bats from Madagascar is still scarce and recent changes in the taxonomy of the island's bat fauna, particularly the description of several new species, require a reassessment of previously described patterns, including blood parasite ecology and vectorial transmission.

Methods: A sample representing seven of the nine known bat families and 31 of the 46 currently recognized taxa from Madagascar and collected in the western and central portions of the island were screened by PCR for the presence of Polychromophilus. In addition, Nycteribiidae flies parasitizing Miniopteridae and Vespertilionidae were screened for parasites with the aim to better understand aspects of vector transmission. Phylogenetic reconstruction using the mitochondrial cytochrome b encoding gene was used in a Bayesian analysis to examine the relationship between Polychromophilus recovered from Malagasy bats and those identified elsewhere.

Results: Polychromophilus infection was restricted to Miniopterus spp. (Miniopteridae), Myotis goudoti (Vespertilionidae), and Paratriaenops furculus (Rhinonycteridae), with an overall infection rate of 13.5%. Polychromophilus melanipherus was found infecting Miniopterus spp. and P. furculus, whereas Polychromophilus murinus was only recovered from M. goudoti. These two protozoan parasites species were also detected in bat flies species known to parasitize Miniopterus spp. and M. goudoti, respectively. Generalized linear model analyses were conducted to elucidate the effect of species and sex on haemoparasites infection in Miniopterus spp., which revealed that males have higher risk of infection than females and prevalence differed according to the considered Miniopterus host. Molecular screening of nycteribiid flies revealed three positive species for Polychromophilus spp., including Penicillidia sp. (cf. fulvida), Penicillidia leptothrinax, and Nycteribia stylidiopsis. These three fly species are known to parasitize Miniopterus spp. and M. goudoti and should be considered as potential vectors of Polychromophilus spp.

Conclusion: Phylogenetic analyses demonstrated the existence of at least four distinct clades within the genus Polychromophilus, two of which were documented in the present study. The screening of nycteribiid flies overlaid on the highly diversified genus Miniopterus, provides considerable insight into parasite transmission, with bat infection being associated with their roosting behaviour and the occurrence of specific arthropod vectors.
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http://dx.doi.org/10.1186/s12936-018-2461-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6119311PMC
August 2018

Isotopic evidence for niche partitioning and the influence of anthropogenic disturbance on endemic and introduced rodents in central Madagascar.

Naturwissenschaften 2018 Jun 29;105(7-8):44. Epub 2018 Jun 29.

Association Vahatra, BP 3972, 101, Antananarivo, Madagascar.

We applied a multi-isotope approach to examine aspects of niche partitioning, competition, and mobility for rodents in the Central Highlands of Madagascar. Specifically, we used carbon (δC), nitrogen (δN), and strontium (Sr/Sr) isotope ratios in bone to investigate diet and mobility for endemic tufted tail rats (Eliurus spp.), and introduced black rats (Rattus rattus) and house mice (Mus musculus) within and outside a fragment of montane humid forest in the Ambohitantely Special Reserve. There was a clear spatial segregation in trapping success for different species: Eliurus was only in the forest interior and edge, Mus only outside of the fragment in a marsh and park housing complex, and Rattus in all habitats except the housing complex. We find only moderate support for mobility of rodents among habitats. Mus may routinely move between the marsh and housing complex. However, regular movement between the forest edge and interior, or between the forest fragment and surrounding grassland is not supported. Taxa appear to target different foods: Rattus tends to feed at a higher trophic level than Eliurus, and Mus consumes some C resources. To date, strontium isotopes have been underutilized in ecological research. Here, we show that they are highly complementary to carbon and nitrogen isotope data. Even in localities with relatively uniform underlying geology, it may be possible to distinguish individuals that regularly forage in different habitats.
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http://dx.doi.org/10.1007/s00114-018-1564-yDOI Listing
June 2018

Bat Astrovirus in Mozambique.

Virol J 2018 06 20;15(1):104. Epub 2018 Jun 20.

Université de La Réunion, UMR Processus Infectieux en Milieu Insulaire Tropical (PIMIT), INSERM 1187, CNRS 9192, IRD 249, 2 rue Maxime Rivière (GIP CYROI), 97490 Sainte-Clotilde, La Réunion, France.

Astroviruses (AstVs) are responsible for infection of a large diversity of mammalian and avian species, including bats, aquatic birds, livestock and humans. We investigated AstVs circulation in bats in Mozambique and Mayotte, a small island in the Comoros Archipelago located between east Africa and Madagascar. Biological material was collected from 338 bats and tested for the presence of the AstV RNA-dependent RNA-polymerase gene with a pan-AstV semi-nested polymerase chain reaction assay. None of the 79 samples obtained from Mayotte bats (Pteropus seychellensis comorensis and Chaerephon pusillus) tested positive; however, 20.1% of bats sampled in Mozambique shed AstVs at the time of sampling and significant interspecific variation in the proportion of positive bats was detected. Many AstVs sequences obtained from a given bat species clustered in different phylogenetic lineages, while others seem to reflect some level of host-virus association, but also with AstVs previously reported from Malagasy bats. Our findings support active circulation of a large diversity of AstVs in bats in the western Indian Ocean islands, including the southeastern African coast, and highlight the need for more detailed assessment of its risk of zoonotic transmission to human populations.
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http://dx.doi.org/10.1186/s12985-018-1011-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6011250PMC
June 2018

Rates of hematophagous ectoparasite consumption during grooming by an endemic Madagascar fruit bat.

Parasit Vectors 2018 Jun 1;11(1):330. Epub 2018 Jun 1.

Association Vahatra, BP 3972, (101), Antananarivo, Madagascar.

Background: Few details are available on the consumption of ectoparasites, specifically bat flies (Diptera: Nycteribiidae and Streblidae), by their chiropteran hosts while grooming. Such details are important to document consumption rates of ectoparasites by their bat host provide details on the dynamics of host-parasite interactions. We present data on ectoparasite consumption rates for an endemic Malagasy fruit bat (Pteropodidae: Rousettus madagascariensis) occupying a cave day roost colony in northern Madagascar. Using quantified behavioral analyses, grooming and associated ingestion rates were measured from infrared videos taken in close proximity to day-roosting bats. The recorded individual bats could be visually identified to age (adult, juvenile) and sex (male, female), allowing analyses of the proportion of time these different classes allocated to consuming ectoparasites via auto-grooming (self) or allo-grooming (intraspecific) per 10 min video recording session. These figures could then be extrapolated to estimates of individual daily consumption rates.

Results: Based on video recordings, adults spent significantly more time auto-grooming and allo-grooming than juveniles. The latter group was not observed consuming ectoparasites. Grooming rates and the average number of ectoparasites consumed per day did not differ between adult males and females. The mean extrapolated number consumed on a daily basis for individual adults was 37 ectoparasites. When these figures are overlaid on the estimated number of adult Rousettus occurring at the roost site during the dry season, the projected daily consumption rate was 57,905 ectoparasites.

Conclusions: The details presented here represent the first quantified data on bat consumption rates of their ectoparasites, specifically dipterans. These results provide new insights in host-parasite predation dynamics. More research is needed to explore the mechanism zoonotic diseases isolated from bat flies might be transmitted to their bat hosts, specifically those pathogens that can be communicated via an oral route.
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http://dx.doi.org/10.1186/s13071-018-2918-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984742PMC
June 2018

Biogeography of Leptospira in wild animal communities inhabiting the insular ecosystem of the western Indian Ocean islands and neighboring Africa.

Emerg Microbes Infect 2018 Apr 4;7(1):57. Epub 2018 Apr 4.

Université de La Réunion, UMR PIMIT (Unité Mixte Processus Infectieux en Milieu Insulaire Tropical), INSERM U1187, CNRS UMR 9192, IRD UMR 249, Plateforme CYROI, 2 rue Maxime Rivière, 97490, Sainte Clotilde, La Réunion, France.

Understanding the processes driving parasite assemblages is particularly important in the context of zoonotic infectious diseases. Leptospirosis is a widespread zoonotic bacterial infection caused by pathogenic species of the genus Leptospira. Despite a wide range of animal hosts, information is still lacking on the factors shaping Leptospira diversity in wild animal communities, especially in regions, such as tropical insular ecosystems, with high host species richness and complex biogeographical patterns. Using a large dataset (34 mammal species) and a multilocus approach at a regional scale, we analyzed the role of both host species diversity and geography in Leptospira genetic diversity in terrestrial small mammals (rodents, tenrecs, and shrews) and bats from 10 different islands/countries in the western Indian Ocean (WIO) and neighboring Africa. At least four Leptospira spp. (L. interrogans, L. borgpetersenii, L. kirschneri, and L. mayottensis) and several yet-unidentified genetic clades contributed to a remarkable regional Leptospira diversity, which was generally related to the local occurrence of the host species rather than the geography. In addition, the genetic structure patterns varied between Leptospira spp., suggesting different evolutionary histories in the region, which might reflect both in situ diversification of native mammals (for L. borgpetersenii) and the more recent introduction of non-native host species (for L. interrogans). Our data also suggested that host shifts occurred between bats and rodents, but further investigations are needed to determine how host ecology may influence these events.
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http://dx.doi.org/10.1038/s41426-018-0059-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5883017PMC
April 2018

Caught in the act: Incipient speciation across a latitudinal gradient in a semifossorial mammal from Madagascar, the mole tenrec Oryzorictes hova (Tenrecidae).

Mol Phylogenet Evol 2018 09 28;126:74-84. Epub 2018 Feb 28.

University of Alaska Museum, 907 Yukon Drive, Fairbanks, AK 99775, USA; Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA.

Madagascar is one of the world's foremost biodiversity hotspots, yet a large portion of its flora and fauna remains undescribed and the driving forces of in situ diversification are not well understood. Recent studies have identified a widespread, latitudinally structured phylogeographic pattern in Madagascar's humid-forest mammals, amphibians, reptiles, and insects. Several factors may be driving this pattern, namely biogeographic barriers (i.e., rivers or valleys) or past episodes of forest contraction and expansion. In this study, we describe the phylogeographic structure of the small, semifossorial mammal Oryzorictes hova, one of Madagascar's two species of mole tenrec, found throughout Madagascar's eastern humid forest belt, from high-elevation montane forest to low-elevation forests, as well as disturbed habitat such as rice fields. Using one mitochondrial locus, four nuclear loci, and 31 craniomandibular measurements, we identified three distinct populations of O. hova associated with the northern, central, and southern regions of the island. We found little evidence of gene flow among these populations, so we treated each population as a potential species. We validated species limits using two Bayesian methods: BP&P, employing only DNA sequence data, and iBPP using both DNA and morphological data, and we assessed whether these methods are susceptible to producing false positive errors. Molecular and morphological data support the recognition of each of the three populations of O. hova as distinct species, but formal species descriptions will require additional data from type specimens. This study illustrates the importance of using integrative datasets, multiple methodological approaches, and extensive geographic sampling for species delimitation and adds evidence for a widespread phylogeographic pattern in Madagascar's humid forest taxa.
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http://dx.doi.org/10.1016/j.ympev.2018.02.024DOI Listing
September 2018

Hidden diversity of forest birds in Madagascar revealed using integrative taxonomy.

Mol Phylogenet Evol 2018 07 21;124:16-26. Epub 2018 Feb 21.

Department of Biology, Loyola University Chicago, 1032 W. Sheridan Road, Chicago, IL 60660, USA.

Madagascar is renowned as a global biodiversity hotspot with high levels of microendemism. However, there are few molecular phylogenetic studies of Malagasy birds, particularly for forest-dwelling species, signifying a substantial gap in current measures of species diversity in the absence of genetic data. We evaluated species limits and explored patterns of diversification within the genus Newtonia (Family Vangidae), a group of forest-dwelling songbirds endemic to Madagascar. Our modern systematics approach combined genomic, morphometric, and ecological niche data to analyze the evolutionary history of the group. Our integrative analysis uncovered hidden species-level diversity within N. amphichroa, with two deeply divergent and morphologically distinct lineages isolated in different regions of humid forest. We describe the southern lineage as a new species. Conversely, N. brunneicauda, which we initially hypothesized may harbor cryptic diversity owing to its large distribution spanning a range of habitats, was found to have no distinct lineages and shared haplotypes across much of its distribution. The contrasting diversification patterns between Newtonia lineages may be the result of their elevational tolerances. Newtonia brunneicauda has a broad habitat tolerance and elevational range that appears to have facilitated population expansion and gene flow across the island, limiting opportunities for diversification. On the other hand, N. amphichroa is found predominantly in mid-elevation and montane humid forests, a restriction that appears to have promoted speciation associated with climatic fluctuations during the Pleistocene. Our findings indicate that species diversity of Malagasy forest-dwelling birds may be greater than currently recognized, suggesting an urgent need for further studies to quantify biodiversity in Madagascar's rapidly disappearing native forests.
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http://dx.doi.org/10.1016/j.ympev.2018.02.017DOI Listing
July 2018

Hidden diversity of Nycteribiidae (Diptera) bat flies from the Malagasy region and insights on host-parasite interactions.

Parasit Vectors 2017 12 29;10(1):630. Epub 2017 Dec 29.

Centre de Recherche et de Veille sur les maladies émergentes dans l'Océan Indien, Plateforme technologique CYROI, Sainte Clotilde, La Réunion, France.

Background: We present information on Nycteribiidae flies parasitizing the bat families Pteropodidae, Miniopteridae and Vespertilionidae from the Malagasy Region, contributing insight into their diversity and host preference.

Results: Our phylogenetic analysis identified nine clusters of nycteribiid bat flies on Madagascar and the neighbouring Comoros Archipelago. Bat flies sampled from frugivorous bats of the family Pteropodidae are monoxenous: Eucampsipoda madagascariensis, E. theodori and Cyclopodia dubia appear wholly restricted to Rousettus madagascariensis, R. obliviosus and Eidolon dupreanum, respectively. Two different host preference patterns occurred in nycteribiids infecting insectivorous bats. Flies parasitizing bats of the genera Miniopterus (Miniopteridae) and Myotis (Vespertilionidae), namely Penicillidia leptothrinax, Penicillidia sp. and Nycteribia stylidiopsis, are polyxenous and showed little host preference, while those parasitizing the genera Pipistrellus and Scotophilus (both Vespertilionidae) and referable to Basilia spp., are monoxenous. Lastly, the inferred Bayesian phylogeny revealed that the genus Basilia, as currently configured, is paraphyletic.

Conclusion: This study provides new information on the differentiation of nycteribiid taxa, including undescribed species. Host preference is either strict as exemplified by flies parasitizing fruit bats, or more relaxed as found on some insectivorous bat species, possibly because of roost site sharing. Detailed taxonomic work is needed to address three undescribed nycteribiid taxa found on Pipistrellus and Scotophilus, tentatively allocated to the genus Basilia, but possibly warranting different generic allocation.
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http://dx.doi.org/10.1186/s13071-017-2582-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5747079PMC
December 2017

Astroviruses in bats, Madagascar.

Emerg Microbes Infect 2017 06 21;6(6):e58. Epub 2017 Jun 21.

University of Reunion Island, UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical), INSERM 1187, CNRS 9192, IRD 249. GIP CYROI, 2 Rue Maxime Rivière, 97490 Sainte-Clotilde, La Réunion, France.

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http://dx.doi.org/10.1038/emi.2017.47DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5520320PMC
June 2017

Insight into the global evolution of Rodentia associated Morbilli-related paramyxoviruses.

Sci Rep 2017 05 16;7(1):1974. Epub 2017 May 16.

Centre de Recherche et de Veille sur les maladies émergentes dans l'Océan Indien (CRVOI), Plateforme de Recherche CYROI, Sainte Clotilde, La Réunion, France.

One portion of the family Paramyxoviridae is a group of Unclassified Morbilli-Related Viruses (UMRV) recently recognized in wild small mammals. At a global level, the evolutionary history of these viruses is not properly understood and the relationships between UMRV and their hosts still remain largely unstudied. The present study revealed, for the first time, that Rodentia associated UMRV emerged from a common ancestor in southern Africa more than 4000 years ago. Sequenced UMRV originating from different regions in the world, clustered into four well-supported viral lineages, which suggest that strain diversification occurred during host dispersal and associated exchanges, with purifying selection pressure as the principal evolutionary force. In addition, multi-introductions on different continents and islands of Rodentia associated UMRV and spillover between rodent species, most probably Rattus rattus, were detected and indicate that these animals are implicated in the vectoring and in the worldwide emergence of this virus group. The natural history and the evolution dynamics of these zoonotic viruses, originating from and hosted by wild animals, are most likely shaped by commensalism related to human activities.
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http://dx.doi.org/10.1038/s41598-017-02206-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5434063PMC
May 2017

Broad and flexible stable isotope niches in invasive non-native Rattus spp. in anthropogenic and natural habitats of central eastern Madagascar.

BMC Ecol 2017 Apr 17;17(1):16. Epub 2017 Apr 17.

Association Vahatra, BP 3972, 101, Antananarivo, Madagascar.

Background: Rodents of the genus Rattus are among the most pervasive and successful invasive species, causing major vicissitudes in native ecological communities. A broad and flexible generalist diet has been suggested as key to the invasion success of Rattus spp. Here, we use an indirect approach to better understand foraging niche width, plasticity, and overlap within and between introduced Rattus spp. in anthropogenic habitats and natural humid forests of Madagascar.

Results: Based on stable carbon and nitrogen isotope values measured in hair samples of 589 individual rodents, we found that Rattus rattus had an extremely wide foraging niche, encompassing the isotopic space covered by a complete endemic forest-dwelling Malagasy small mammal community. Comparisons of Bayesian standard ellipses, as well as (multivariate) mixed-modeling analyses, revealed that the stable isotope niche of R. rattus tended to change seasonally and differed between natural forests and anthropogenic habitats, indicating plasticity in feeding niches. In co-occurrence, R. rattus and Rattus norvegicus partitioned feeding niches. Isotopic mismatch of signatures of individual R. rattus and the habitat in which they were captured, indicate frequent dispersal movements for this species between natural forest and anthropogenic habitats.

Conclusions: Since R. rattus are known to transmit a number of zoonoses, potentially affecting communities of endemic small mammals, as well as humans, these movements presumably increase transmission potential. Our results suggest that due to their generalist diet and potential movement between natural forest and anthropogenic habitats, Rattus spp. might affect native forest-dependent Malagasy rodents as competitors, predators, and disease vectors. The combination of these effects helps explain the invasion success of Rattus spp. and the detrimental effects of this genus on the endemic Malagasy rodent fauna.
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http://dx.doi.org/10.1186/s12898-017-0125-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393019PMC
April 2017
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