The nine-banded armadillo (Dasypus novemcinctus) is the most widespread xenarthran species across the Americas. Recent studies have suggested it is composed of 4 morphologically and genetically distinct lineages of uncertain taxonomic status. To address this issue, we used a museomic approach to sequence 80 complete mitogenomes and capture 997 nuclear loci for 71 Dasypus individuals sampled across the entire distribution. We carefully cleaned up potential genotyping errors and cross-contaminations that could blur species boundaries by mimicking gene flow. Our results unambiguously support 4 distinct lineages within the D. novemcinctus complex. We found cases of mito-nuclear phylogenetic discordance but only limited contemporary gene flow confined to the margins of the lineage distributions. All available evidence including the restricted gene flow, phylogenetic reconstructions based on both mitogenomes and nuclear loci, and phylogenetic delimitation methods consistently supported the 4 lineages within D. novemcinctus as 4 distinct species. Comparable genetic differentiation values to other recognized Dasypus species further reinforced their status as valid species. Considering congruent morphological results from previous studies, we provide an integrative taxonomic view to recognize 4 species within the D. novemcinctus complex: D. novemcinctus, D. fenestratus, D. mexicanus, and D. guianensis sp. nov., a new species endemic of the Guiana Shield that we describe here. The 2 available individuals of D. mazzai and D. sabanicola were consistently nested within D. novemcinctus lineage and their status remains to be assessed. The present work offers a case study illustrating the power of museomics to reveal cryptic species diversity within a widely distributed and emblematic species of mammals.
Tick-borne bacteria of the genera Ehrlichia and Anaplasma cause several emerging human infectious diseases worldwide. In this study, we conduct an extensive survey for Ehrlichia and Anaplasma infections in the rainforests of the Amazon biome of French Guiana. Through molecular genetics and metagenomics reconstruction, we observe a high indigenous biodiversity of infections circulating among humans, wildlife, and ticks inhabiting these ecosystems. Molecular typing identifies these infections as highly endemic, with a majority of new strains and putative species specific to French Guiana. They are detected in unusual rainforest wild animals, suggesting they have distinctive sylvatic transmission cycles. They also present potential health hazards, as revealed by the detection of Candidatus Anaplasma sparouinense in human red blood cells and that of a new close relative of the human pathogen Ehrlichia ewingii, Candidatus Ehrlichia cajennense, in the tick species that most frequently bite humans in South America. The genome assembly of three new putative species obtained from human, sloth, and tick metagenomes further reveals the presence of major homologs of Ehrlichia and Anaplasma virulence factors. These observations converge to classify health hazards associated with Ehrlichia and Anaplasma infections in the Amazon biome as distinct from those in the Northern Hemisphere.
Material properties of the diet of extant species is reflected by the microwear texture recorded on the enamel tooth surface, a signal that can be useful for estimating the diets of extinct species. Intra-specific dietary vari-ations can occur between sexes or depend on seasonal vegetation cover changes in their habitat. However, these factors cannot, or very rarely, be incorporated within a paleontological context, especially if the fossil record of an extinct species is mainly composed of isolated teeth. In order to assess the effects of these factors on microwear texture features, we studied 42 wild-caught specimens of two sympatric extant species of caviomorph rodents, Proechimys cuvieri and Proechimys guyannensis (Echimyidae, Octodontoidea) from the Cacao area located in French Guiana. Animals were captured between 2007 and 2012, in July and October, along a 1.5 km transect ranging from an old secondary forest to a disturbed forest. We applied a Scale Sensitive Fractal Analysis (SSFA) to the first upper molars of these specimens. Differences of dental microwear textures were found between sexes, between months, and between habitat, leading to one species overlapping in microwear texture parameter space with the other in some cases. The results obtained help identifying which factors might drive intra-population variations in dental microwear texture. Its understanding is indeed a key-step to better interpret the disper-sion observed within a given fossil sample set to obtain refined dietary reconstructions.
The small Indian mongoose has been introduced into several important hotspots of biodiversity and is considered the wild carnivore with the greatest negative impact on autochthonous ecosystems. Understanding the introduction and dispersal history of the species is crucial in any effort to conserve global biodiversity. We investigated the genetic structure and diversity of the small Indian mongoose, with a focus on the Caribbean region, using genetic data from 496 individuals. We performed molecular genetic analyses using two mitochondrial and eleven newly designed microsatellite markers. We compared our results with historical records and scenarios inferred from the literature. Consistent with historical records, molecular results suggest multiple introduction events into Jamaica from India, as well as the subsequent introduction of the species from Jamaica into Grenada and Puerto Rico. Our results also suggest new scenarios for other introduced populations. For instance, the introduction history of the species into Guadeloupe may be more complex than previously thought, sharing a common origin with the populations of Jamaica, Trinidad and Guyana. In addition, microsatellite data reveal a strong structuration of the populations within the West Indian islands, including nearby islands within the Guadeloupean archipelago, highlighting the lack of dispersal events between islands after the initial introductions. Conversely, the absence of structure inside each island indicates the high dispersal ability of the small Indian mongoose within these islands. These results and the newly developed microsatellite markers represent valuable tools to identify the origin of potential new introductions.
We investigated a Q fever outbreak that occurred in an isolated area of the Amazon Rain Forest in French Guiana in 2014. Capybara fecal samples were positive for Coxiella burnetii DNA. Being near brush cutters in use was associated with disease development. Capybaras are a putative reservoir for C. burnetii.
The Amazonian savannas of French Guiana are rare and of high ecological and cultural value but are also highly threatened. They are socioecological systems that have been coconstructed by humans and nature and today form mosaic landscapes along the country’s coast. From pre-Columbian raised fields through colonial and Créole uses to contemporary uses, they have been largely shaped and modified by human activities. They are currently threatened by changes in fire regimes, agricultural practices, invasive species, and infrastructure development. Less than 3% are protected, despite their importance for several endangered animal and plant species. A shift is required in the way we think about their conservation to create a new strategy that would be completely different from existing French environmental protection tools and adapted to the complexity of these landscapes.
Recent field surveys of bats (Chiroptera) in various localities of French Guiana have been accompanied by the collection and preservation of ectoparasites, mainly bat flies (Diptera: Streblidae and Nycteribiidae). Most specimens of ectoparasites was collected haphazardly during the course of bats inventories, but systematic surveys on the whole chiropteran community were realized at five opportunities. Concerning Streblidae, 813 individuals have been examined, which represent 46 species and/or subspecies belonging to 15 genera and 6 taxa for confirmation and/or future description. For Nycteribiidae, 44 individuals of 3 identified species and 2 for confirmation and/or future description. Other ectoparasites have been found (Hemiptera and acarids), which are also listed with details on their bat-host, place and date of collect. For six species of bats in which at least 10 animals were carrying ectoparasites, a brief description of the frequencies of their ectoparasites provides some preliminary characteristics of their infracommunities.
We studied the litter sizes of small rodents and opossums caught in the Guianan Region (Brazilian Amapa, French Guiana, Suriname, and Guyana) by pooling the data of animals collected during various field trips conducted primarily between 1990 and 2017. A series of 569 counts of embryos (or of pouch young for marsupials) in 40 species of Didelphidae (N = 12 species), Sigmodontinae (18), Murinae (2), and Echimyidae (8) allowed for a more detailed characterization of the reproductive condition of 14 species known each by more than 10 pregnant females. For eight species with at least 20 pregnant females, an examination of seasonality in breeding occurrence documented that the two months with the lowest percentage of pregnant females are July and August (16.0 and 17.3%, respectively) during the end of the long wet season and beginning of the dry season. By contrast, January and February showed the highest abundance of pregnancies (57.9% and 55.8%, respectively) during the beginning of the long wet season. This timing coincides with most juveniles foraging during the height of the wet season in May when food is presumably most prevalent.
Abstract For deciphering the biodiversity of native mammals on the island of Martinique (Lesser Antilles), bats (Chiroptera) were netted in various localities during the course of two separate studies spanning 2004–2015. A total of 2613 individuals were caught in ground-level mist nets at 79 localities. In this study, we concentrate on 1859 captures of nine species of bats caught at 24 capture-rich localities. We provide sex-ratio values, forearm and body weight measurements for each taxon. The order of decreasing abundance in captures was Artibeus jamaicensis, Sturnira angeli, Brachyphylla cavernarum, Monophyllus plethodon, Myotis martiniquensis, Molossus molossus, Ardops nichollsi, Pteronotus davyi and Tadarida brasiliensis. Our results suggest a strong sex-bias in capture rates, with males much more abundant for Ardops and Monophyllus, whereas females are more abundant for Molossus, Pteronotus and Sturnira. A clear sexual dimorphism exists with larger females in Ardops and Pteronotus, whereas males are larger in Molossus, Monophyllus and Sturnira. Reproductive females (pregnant, lactating) were found almost exclusively during the dry season (January to June) for A. jamaicensis, M. plethodon and S. angeli.
DNA barcoding has become a standard method for species identification in taxonomically complex groups. An important step of the barcoding process is the construction of a library of voucher-based material that was properly identified by independent methods, free of inaccurate identification, and paralogs. We provide here a cytochrome oxidase I (mt-Co1) DNA barcode database for species of the genus Oligoryzomys, based on type material and karyotyped specimens, and anchored on the mitochondrial genome of one species of Oligoryzomys, O. stramineus. To evaluate the taxonomic determination of new COI sequences, we assessed species intra/interspecific genetic distances (barcode gap), performed the General Mixed Yule Coalescent method (GMYC) for lineages' delimitation, and identified diagnostic nucleotides for each species of Oligoryzomys. Phylogenetic analyses of Oligoryzomys were performed on 2 datasets including 14 of the 23 recognized species of this genus: a mt-Co1 only matrix, and a concatenated matrix including mt-Co1, cytochrome b (mt-Cytb), and intron 7 of the nuclear fibrinogen beta chain gene (i7Fgb). We recovered nuclear-mitochondrial translocated (Numts) pseudogenes on our samples and identified several published sequences that are cases of Numts. We analyzed the rate of non-synonymous and synonymous substitution, which were higher in Numts in comparison to mtDNA sequences. GMYC delimitations and DNA barcode gap results highlight the need for further work that integrate molecular, karyotypic, and morphological analyses, as well as additional sampling, to tackle persistent problems in the taxonomy of Oligoryzomys.
Abstract: Postnatal growth and development of the small Neotropical mouse Oecomys rutilus (Sigmodontinae: Cricetidae) were investigated from birth to day 143, in the laboratory. Morphometric measurements at age of 3 days, of both sexes combined, revealed body weight to be 3.4 ± 0.3 g, mean tail length as 27.4 ± 1.1 mm, and mean hind foot length as 9.3 ± 0.7 mm. Body weight was found to increase steadily until at least 69 days, whereas the instantaneous growth rates of other measurements declined earlier: the daily growth of hind foot length declined to a minimum at age of 24 days, and the growth of tail and of ear declined by the age of 33 days. Average litter size for 12 captive births was 2.5, ranging from 2 to 3. The preserved eye crystalline lens was weighted in 23 captive-born animals of known age, allowing a rough estimate of the age of reproduction in wild-caught animals. Based on the inferred relation between eye-lens weight and age, the youngest reproductive (pregnant) wild-caught females had an estimated age of 90 and 95 days.
As the invasive murine rodents have too often been neglected in Neotropical faunal inventories, a synthesis on the presence of the House mouse, the Black rat, and the Norway rat was ascertained for French Guiana. We relied on preserved museum-specimens, on caught and released animals, on identified remains extracted from Barn owl (Tyto alba) pellets, and on bona-fide visual observations. The aggregated data allowed documenting the presence of at least one invasive Murinae in 31 localities throughout the country. Most observations and/or captures concern the northern coastal areas, where the vast majority of villages and cities are to be found. All three murines were found together in only two localities (Sinnamary; Cayenne) whereas globally the most frequent species was Rattus rattus, followed by Mus musculus, and finally R. norvegicus. Invasive murines were also found on five offshore islands, and the House mouse was caught in an isolated gold-mining camp in the center of the country. Biometric data are provided for characterizing some external and cranio-dental variables in M. musculus and R. rattus. Owl pellets materials indicate that both species of Rattus can be easily sorted by the crown-length non-overlapping values of their upper and/or lower molars.
A series of 14 new observations of Hyladelphys kalinowskii (Didelphidae) provides novel natural history information about this rare Neotropical opossum, which appears to occur throughout French Guiana, from highly degraded forest patches of the littoral zone to large tracks of pristine primary forests in the interior. Six nests were found containing one to several individuals, including females with suckling young. It appears that the components (dry leaves, small twigs) of some nests are glued together with a whitish cement of unknown origin. Including previously reported records, a total of 18 individuals of H. kalinowskii have now been caught or observed in French Guiana. External and cranial measurements of five adult specimens are tabulated.
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Mitochondrial genomes of animals have long been considered to evolve under the action of purifying selection. Nevertheless, there is increasing evidence that they can also undergo episodes of positive selection in response to shifts in physiological or environmental demands. Vampire bats experienced such a shift, as they are the only mammals feeding exclusively on blood and possessing anatomical adaptations to deal with the associated physiological requirements (e.g., ingestion of high amounts of liquid water and iron). We sequenced eight new chiropteran mitogenomes including two species of vampire bats, five representatives of other lineages of phyllostomids and one close outgroup. Conducting detailed comparative mitogenomic analyses, we found evidence for accelerated evolutionary rates at the nucleotide and amino acid levels in vampires. Moreover, the mitogenomes of vampire bats are characterized by an increased cytosine (C) content mirrored by a decrease in thymine (T) compared with other chiropterans. Proteins encoded by the vampire bat mitogenomes also exhibit a significant increase in threonine (Thr) and slight reductions in frequency of the hydrophobic residues isoleucine (Ile), valine (Val), methionine (Met), and phenylalanine (Phe). We show that these peculiar substitution patterns can be explained by the co-occurrence of both neutral (mutational bias) and adaptive (positive selection) processes. We propose that vampire bat mitogenomes may have been impacted by selection on mitochondrial proteins to accommodate the metabolism and nutritional qualities of blood meals.
The spiny rats, genus Proechimys, have the highest species richness within the Echimyidae family, as well as species with high genetic variability. The genus distribution includes tropical South America and Central America south to Honduras. In this study, we evaluate the phylogeographic histories of Proechimys guyannensis and P. cuvieri using cytochrome b, in a densely sampled area in northeastern Amazon where both species are found in sympatry in different environments. For each species, Bayesian and Maximum Likelihood phylogenetic analysis were congruent and recovered similar clades in the studied area. Bayesian phylogenetic analysis using a relaxed molecular clock showed that these clusters of haplotypes diversified during Pleistocene for both species. Apparently, the large rivers of the region did not act as barriers, as some clades include specimens collected from opposite banks of Oiapoque, Araguari and Jari rivers. Bayesian skyline plot analysis showed recent demographic expansion in both species. The Pleistocene climatic changes in concert with the geologic changes in the Amazon fan probably acted as drivers in the diversification that we detected in these two spiny rats. Proechimys cuvieri and P. guyannensis show genetic structure in the eastern part of the Guiana region. Greater genetic distances observed in P. guyannensis, associated with highly structured groups, suggest that more detailed studies of systematics and ecology should be directed to this species.
Summary DNA barcoding and metabarcoding are increasingly used as alternatives to traditional morphological identifications. For animals, the standard barcode is a c. 658‐bp portion of the COI gene, for which reference libraries now cover a large proportion of described mammal species. Unfortunately, because its sequence is too long and does not contain highly conserved primer binding sites, this marker is not adapted for metabarcoding. Although alternative metabarcodes have been developed, their performances are generally seldom assessed. We evaluate the reliability of a short metabarcode located in the mitochondrial 12S ribosomal RNA for the identifications of Amazonian mammals. We (i) constitute a nearly exhaustive reference library for species found in French Guiana, (ii) assess the taxonomic resolution of the marker and validate its use with dipteran blood meal analyses, (iii) assess the conservation of the primer binding sites, and (iv) compare its theoretical performances with that of a newly designed metabarcode located within the standard COI barcode. About 576 specimens representing 164 species were gathered and sequenced. We show that the 12S marker allows remarkably accurate taxonomic assignations despite its very short size, and that primer binding sites are highly conserved, which is important to avoid PCR amplification bias potentially leading to detection failure. Additionally, our results stress that the identifications should only be considered at the generic level when they are based on incomplete reference libraries, even when a stringent similarity cut‐off is used. A new short COI metabarcode was designed based on 569 reference sequences of mammals retrieved on BOLD. Our results clearly show that, while both markers provide similar taxonomic resolution, much higher rates of primer mismatches are found with COI. Besides demonstrating the accuracy of the short 12S marker for the identification of Amazonian mammals and providing a reliable molecular reference database, this study emphasizes that the accuracy of taxonomic assignations highly depends on the comprehensiveness of the reference library and that great caution should be taken for interpreting metabarcoding results based on scarce reference libraries. The comparison with a short COI metabarcode also provides novel evidence in support for the use of ribosomal markers in metabarcoding studies.
Among mammals, rodents play a key role in the emergence of viral diseases. In French Guiana, with 36 rodent species recorded in various ecosystems (pristine forests, savannas, anthropized environments), some natural habitats today encounter anthropogenic perturbations that induce changes in community structure and population dynamics. These modifications are sometimes associated with the circulation and emergence of viral pathogens. For 10 years, investigations on the circulation of two rodent-borne viruses, Hantavirus and Mammarenavirus, are underway in rodent populations as well as in humans for hantavirus. These investigations identified viruses from both genera in their potential reservoirs and allow describing the most favourable habitats for the reservoirs of hantavirus where the risk of viral emergence may be higher. We suggest to investigate how anthropic perturbations in rodent communities can drive the emergence of viruses that are currently confined to a small scale and search for evidence of infection in the human population.