The small mammal fauna of Réserve Spéciale d'Analamazaotra,Madagascar: the effects of human disturbance on endemic species diversity

This study represents the first long-term small mammal survey of the mid-altitude rain forest reserve of Analamazaotra, Madagascar. Twenty-three visits were made to the reserve between April 1988 and May 1990. Live-trapping with Sherman and pitfall traps at four sites subjected to varying levels of human disturbance revealed the presence of seven endemic tenrec species, three endemic rodent species and an introduced rat. Greater species richness was demonstrated at the most undisturbed site, though individual species abundance was reduced. Human disturbance associated with tourism was correlated with a decrease in endemic species richness and an increase in abundance of introduced rats. Forest subjected to infrequent logging by local people exhibited an intermediate level of species richness. It is recommended that core areas of the reserve be left undisturbed in order to preserve small mammal species diversity.     

Late Quaternary climatic vegetational shifts in an ecological transition zone of northern Madagascar: insights from genetic analyses of two endemic rodent species

The Loky‐Manambato region, located in northern Madagascar, is a biotically rich contact zone between different forest biomes. Local current forest cover is composed of both humid and dry formations, which show elevational stratification. A recent phylogeographical study of a regional dry forest rodent, Eliurus carletoni (subfamily Nesomyinae), found genetic evidence of forest contractions between 18 750 and 7500 years BP, which based on extrapolation of the pollen subfossil record, was thought to be associated with an expansion of local humid forests. Herein, we conduct a genetic test of this hypothesis and focused on populations on two neighbouring massifs of forest‐dependent rodent species, one associated with low‐elevation dry forests (E. carletoni) and the other with higher elevation humid forests (Eliurus tanala). Using mitochondrial markers and a combination of traditional and coalescent‐based phylogeographical, historical demographic and population genetic methods, we found evidence of historical connections between populations of E. tanala. Adjacent populations of E. carletoni and E. tanala exhibit opposite historical demographic patterns, and for both, evidence suggests that historical demographic events occurred within the last 25 000 years BP. These findings strongly support the proposed late Quaternary shifts in the floristic composition of the Loky‐Manambato region.     

Ecological niche modeling for conservation planning of an endemic snail in the verge of becoming a pest in cardamom plantations in the Western Ghats biodiversity hotspot

Conservation managers and policy makers are often confronted with a challenging dilemma of devising suitable strategies to maintain agricultural productivity while conserving endemic species that at the early stages of becoming pests of agricultural crops. Identification of environmental factors conducive to species range expansion for forecasting species distribution patterns will play a central role in devising management strategies to minimize the conflict between the agricultural productivity and biodiversity conservation. Here, we present results of a study that predicts the distribution of Indrella ampulla, a snail endemic to the Western Ghats biodiversity hotspot, which is becoming a pest in cardamom (Ellettaria cardamomum) plantations. We determined the distribution patterns and niche overlap between I. ampulla and Ellettaria cardamomum using maximum entropy (MaxEnt) niche modeling techniques under current and future (2020–2080) climatic scenarios. The results showed that climatic (precipitation of coldest quarter and isothermality) and soil (cation exchange capacity of soil [CEC]) parameters are major factors that determine the distribution of I. ampulla in Western Ghats. The model predicted cardamom cultivation areas in southern Western Ghats are highly sensitive to invasion of I. ampulla under both present and future climatic conditions. While the land area in the central Western Ghats is predicted to become unsuitable for I. ampulla and Ellettaria cardamomum in future, we found 71% of the Western Ghats land area is suitable for Ellettaria cardamomum cultivation and 45% suitable for I. ampulla, with an overlap of 35% between two species. The resulting distribution maps are invaluable for policy makers and conservation managers to design and implement management strategies minimizing the conflicts to sustain agricultural productivity while maintaining biodiversity in the region.     

Cofeeding intra‐ and interspecific transmission of an emerging insect‐borne rickettsial pathogen

Cat fleas (Ctenocephalides felis) are known as the primary vector and reservoir of Rickettsia felis, the causative agent of flea‐borne spotted fever; however, field surveys regularly report molecular detection of this infectious agent from other blood‐feeding arthropods. The presence of R. felis in additional arthropods may be the result of chance consumption of an infectious bloodmeal, but isolation of viable rickettsiae circulating in the blood of suspected vertebrate reservoirs has not been demonstrated. Successful transmission of pathogens between actively blood‐feeding arthropods in the absence of a disseminated vertebrate infection has been verified, referred to as cofeeding transmission. Therefore, the principal route from systemically infected vertebrates to uninfected arthropods may not be applicable to the R. felis transmission cycle. Here, we show both intra‐ and interspecific transmission of R. felis between cofeeding arthropods on a vertebrate host. Analyses revealed that infected cat fleas transmitted R. felis to naïve cat fleas and rat fleas (Xenopsylla cheopis) via fleabite on a nonrickettsemic vertebrate host. Also, cat fleas infected by cofeeding were infectious to newly emerged uninfected cat fleas in an artificial system. Furthermore, we utilized a stochastic model to demonstrate that cofeeding is sufficient to explain the enzootic spread of R. felis amongst populations of the biological vector. Our results implicate cat fleas in the spread of R. felis amongst different vectors, and the demonstration of cofeeding transmission of R. felis through a vertebrate host represents a novel transmission paradigm for insect‐borne Rickettsia and furthers our understanding of this emerging rickettsiosis.     

Trophic Niche Differentiation and Microhabitat Utilization in a Species‐rich Montane Forest Small Mammal Community of Eastern Madagascar

Unraveling the mechanisms facilitating species coexistence in communities is a central theme in ecology. Species‐rich tropical mammal communities provide excellent settings to explore such mechanisms as they often harbor numerous congeneric species with close phylogenetic relationships. Explicit tests for the mechanisms that allow syntopic occurrence in these assemblages, however, is often hampered because of the difficulty in obtaining detailed ecological data on the organisms making up the community. Using stable nitrogen and carbon ratios of hair samples, we examine whether trophic niche differentiation and microhabitat segregation explain the coexistence of 21 small mammal species at a montane humid forest site in eastern Madagascar. Overall, the community was trophically diverse and covered wide isotopic space. This diversity was based on: (1) a multi‐layered trophic community structure with mainly frugivorous‐granivorous rodents (subfamily Nesomyinae) as primary consumers and insectivorous tenrecs (family Tenrecidae) as secondary and tertiary consumers; (2) trophic segregation of rodents and tenrecs with the latter occupying different microhabitats; and (3) a dense and regular packing of species in the community. The 12 locally occurring Microgale shrew tenrecs (subfamily Oryzorictinae) showed high trophic redundancy, but were maximally spaced from each other within the trophic space covered by the genus. Results of stable isotope analysis suggest that in combination the differentiation of microhabitats and trophic niches explain the coexistence of small mammals in this community. Congeneric species appeared to be under more intense competition compared with non‐congeneric species and their coexistence can only partly be explained by trophic and microhabitat niche segregation.     

Reversing expansion of Calamagrostis epigejos in a grassland biodiversity hotspot: Hemiparasitic Rhinanthus major does a better job than increased mowing intensity

Questions

Can hemiparasitic Rhinanthus major originating from a local population suppress the competitive clonal grass Calamagrostis epigejos and reverse its expansion in species‐rich semi‐natural grasslands? Does sowing seeds of R. major facilitate restoration of target meadow vegetation? Is R. major more beneficial for biodiversity restoration/conservation than increased mowing intensity, a conventional measure to suppress C. epigejos?

Location

?ertoryje National Nature Reserve, Bílé Karpaty (White Carpathians) Protected Landscape Area, Czech Republic.

Methods

We conducted a before‐after‐control‐impact experiment in meadow patches heavily infested by C. epigejos: eight blocks, each containing four plots with four treatment combinations: (1) traditional management, i.e. mowing once in summer, (2) mowing in summer and autumn (3) mowing in summer and seed sowing of R. major, (4) mowing in summer and autumn and seed sowing of R. major. Above‐ground biomass of C. epigejos and vegetation composition of each of the plots were monitored every year from 2013 to 2016. To assess the effects of treatments, we analysed biomass production of C. epigejos, herb layer cover and vegetation composition.

Results

Both sowing R. major and an additional autumn meadow cut significantly suppressed C. epigejos. Their effects were additive and of comparable size. Both treatments also had significant but markedly different effects on community composition. Rhinanthus major facilitated directional community composition change towards the regional Brachypodio‐Molinetum meadows. In contrast, increased mowing intensity significantly decreased frequency of threatened species, which however may have also been influenced by R. major.

Conclusions

Sowing of autochthonous R. major seeds was demonstrated as an efficient tool to suppress C. epigejos and facilitate community restoration. It can be combined with an additional meadow cut to further accelerate decline of the grass. The additional cut should however be used as a short‐term practice (1–2 years) only to minimize potential negative effects of its long‐term application on some threatened plant species. The effects of R. major are comparable to those of Rhinanthus alectorolophus reported previously. As a species occurring naturally in species‐rich dry grasslands, R. major has a broader and longer‐term application potential than R. alectorolophus in ecological restoration and conservation of these communities.     

Genetic diversity loss in a biodiversity hotspot: ancient DNA quantifies genetic decline and former connectivity in a critically endangered marsupial

The extent of genetic diversity loss and former connectivity between fragmented populations are often unknown factors when studying endangered species. While genetic techniques are commonly applied in extant populations to assess temporal and spatial demographic changes, it is no substitute for directly measuring past diversity using ancient DNA (aDNA). We analysed both mitochondrial DNA (mtDNA) and nuclear microsatellite loci from 64 historical fossil and skin samples of the critically endangered Western Australian woylie (Bettongia penicillata ogilbyi), and compared them with 231 (n = 152 for mtDNA) modern samples. In modern woylie populations 15 mitochondrial control region (CR) haplotypes were identified. Interestingly, mtDNA CR data from only 29 historical samples demonstrated 15 previously unknown haplotypes and detected an extinct divergent clade. Through modelling, we estimated the loss of CR mtDNA diversity to be between 46% and 91% and estimated this to have occurred in the past 2000–4000 years in association with a dramatic population decline. In addition, we obtained near‐complete 11‐loci microsatellite profiles from 21 historical samples. In agreement with the mtDNA data, a number of ‘new’ microsatellite alleles was only detected in the historical populations despite extensive modern sampling, indicating a nuclear genetic diversity loss >20%. Calculations of genetic diversity (heterozygosity and allelic rarefaction) showed that these were significantly higher in the past and that there was a high degree of gene flow across the woylie's historical range. These findings have an immediate impact on how the extant populations are managed and we recommend the implementation of an assisted migration programme to prevent further loss of genetic diversity. Our study demonstrates the value of integrating aDNA data into current‐day conservation strategies.     

Diversification in a biodiversity hot spot: landscape correlates of phylogeographic patterns in the African spotted reed frog

The Eastern Afromontane Biodiversity Hotspot is known for microendemism and exceptional population genetic structure. The region's landscape heterogeneity is thought to limit gene flow between fragmented populations and create opportunities for regional adaptation, but the processes involved are poorly understood. Using a combination of phylogeographic analyses and circuit theory, I investigate how characteristics of landscape heterogeneity including regional distributions of slope, rivers and streams, habitat and hydrological basins (drainages) impact genetic distance among populations of the endemic spotted reed frog (Hyperolius substriatus), identifying corridors of connectivity as well as barriers to dispersal. Results show that genetic distance among populations is most strongly correlated to regional and local hydrologic structure and the distribution of suitable habitat corridors, not isolation by distance. Contrary to expectations, phylogeographic structure is not coincident with the two montane systems, but instead corresponds to the split between the region's two major hydrological basins (Zambezi and East Central Coastal). This results in a paraphyletic relationship for the Malawian Highlands populations with respect to the Eastern Arc Mountains and implies that the northern Malawian Highlands are the diversity centre for H. substriatus. Although the Malawian Highlands collectively hold the greatest genetic diversity, individual populations have lower diversity than their Eastern Arc counterparts, with an overall pattern of decreasing population diversity from north to south. Through the study of intraspecific differentiation across a mosaic of ecosystem and geographic heterogeneity, we gain insight into the processes of diversification and a broader understanding of the role of landscape in evolution.     

Let them eat termites—prey‐baiting provides effective control of Argentine ants,Linepithema humile,in a biodiversity hotspot

Invasive ants threaten biodiversity, ecosystem services and agricultural systems. This study evaluated a prey‐baiting approach for managing Argentine ants in natural habitat invaded by Argentine ants. Blackmound termites (Amitermes hastatus) were topically exposed to fipronil and presented to Argentine ants (Linepithema humile). In laboratory assays, L. humile colonies were offered fipronil‐treated termites within experimental arenas. The termites were readily consumed, and results demonstrate that a single termite topically treated with 590 ng fipronil is capable of killing at least 500 L. humile workers in 4 days. Field studies were conducted in natural areas invaded by L. humile. Fipronil‐treated termites scattered within experimental plots provided rapid control of L. humile and ant densities throughout the treated plots declined by 98 ± 5% within 21 days. Results demonstrate that the prey‐baiting approach is highly effective against L. humile and may offer an effective alternative to traditional bait treatments. Furthermore, prey‐baiting offers environmental benefits by delivering substantially less toxicant to the environment relative to current control methods which rely on commercial bait formulations and may offer greater target specificity.     

Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe

The widespread occurrence of Wolbachia in arthropods and nematodes suggests that this intracellular, maternally inherited endosymbiont has the ability to cross species boundaries. However, direct evidence for such a horizontal transmission of Wolbachia in nature is scarce. Here, we compare the well‐characterized Wolbachia infection of the European cherry fruit fly, Rhagoletis cerasi, with that of the North American eastern cherry fruit fly, Rhagoletis cingulata, recently introduced to Europe. Molecular genetic analysis of Wolbachia based on multilocus sequence typing and the Wolbachia surface protein wsp showed that all R. cingulata individuals are infected with wCin2 identical to wCer2 in R. cerasi. In contrast, wCin1, a strain identical to wCer1 in R. cerasi, was present in several European populations of R. cingulata, but not in any individual from the United States. Surveys of R. cingulata from Germany and Hungary indicated that in some populations, the frequency of wCin1 increased significantly in just a few years with at least two independent horizontal transmission events. This is corroborated by the analysis of the mitochondrial cytochrome oxidase II gene that showed association of wCin1 with two distinct haplotypes in Germany, one of which is also infected with wCin1 in Hungary. In summary, our study provides strong evidence for a very recent inter‐specific Wolbachia transmission with a subsequent spatial spread in field populations.     

Losing ground: past history and future fate of Arctic small mammals in a changing climate

According to the IPCC, the global average temperature is likely to increase by 1.4–5.8 °C over the period from 1990 to 2100. In Polar regions, the magnitude of such climatic changes is even larger than in temperate and tropical biomes. This amplified response is particularly worrisome given that the so‐far moderate warming is already impacting Arctic ecosystems. Predicting species responses to rapid warming in the near future can be informed by investigating past responses, as, like the rest of the planet, the Arctic experienced recurrent cycles of temperature increase and decrease (glacial–interglacial changes) in the past. In this study, we compare the response of two important prey species of the Arctic ecosystem, the collared lemming and the narrow‐skulled vole, to Late Quaternary climate change. Using ancient DNA and Ecological Niche Modeling (ENM), we show that the two species, which occupy similar, but not identical ecological niches, show markedly different responses to climatic and environmental changes within broadly similar habitats. We empirically demonstrate, utilizing coalescent model‐testing approaches, that collared lemming populations decreased substantially after the Last Glacial Maximum; a result consistent with distributional loss over the same period based on ENM results. Given this strong association, we projected the current niche onto future climate conditions based on IPCC 4.0 scenarios, and forecast accelerating loss of habitat along southern range boundaries with likely associated demographic consequences. Narrow‐skulled vole distribution and demography, by contrast, was only moderately impacted by past climatic changes, but predicted future changes may begin to affect their current western range boundaries. Our work, founded on multiple lines of evidence suggests a future of rapidly geographically shifting Arctic small mammal prey communities, some of whom are on the edge of existence, and whose fate may have ramifications for the whole Arctic food web and ecosystem.     

Wildfire risk for main vegetation units in a biodiversity hotspot: modeling approach in New Caledonia,South Pacific

Wildfire has been recognized as one of the most ubiquitous disturbance agents to impact on natural environments. In this study, our main objective was to propose a modeling approach to investigate the potential impact of wildfire on biodiversity. The method is illustrated with an application example in New Caledonia where conservation and sustainable biodiversity management represent an important challenge. Firstly, a biodiversity loss index, including the diversity and the vulnerability indexes, was calculated for every vegetation unit in New Caledonia and mapped according to its distribution over the New Caledonian mainland. Then, based on spatially explicit fire behavior simulations (using the FLAMMAP software) and fire ignition probabilities, two original fire risk assessment approaches were proposed: a one‐off event model and a multi‐event burn probability model. The spatial distribution of fire risk across New Caledonia was similar for both indices with very small localized spots having high risk. The patterns relating to highest risk are all located around the remaining sclerophyll forest fragments and are representing 0.012% of the mainland surface. A small part of maquis and areas adjacent to dense humid forest on ultramafic substrates should also be monitored. Vegetation interfaces between secondary and primary units displayed high risk and should represent priority zones for fire effects mitigation. Low fire ignition probability in anthropogenic‐free areas decreases drastically the risk. A one‐off event associated risk allowed localizing of the most likely ignition areas with potential for extensive damage. Emergency actions could aim limiting specific fire spread known to have high impact or consist of on targeting high risk areas to limit one‐off fire ignitions. Spatially explicit information on burning probability is necessary for setting strategic fire and fuel management planning. Both risk indices provide clues to preserve New Caledonia hot spot of biodiversity facing wildfires.     

Photogrammetry: a useful tool for three‐dimensional morphometric analysis of small mammals

Recently, the improvement of methods for shape analysis has revolutionized the field of morphometrics. While three‐dimensional (3D) imaging technology is increasingly available, many studies of 3D structures still use two‐dimensional (2D) data, even when this may result in the loss of important information. This is particularly conspicuous in the study of small mammals, as devices precise enough for 3D digitization of small objects are the most expensive. Thus, the development of low‐cost methods aimed to recover 3D shape from small mammals would be of wide interest. Photogrammetry allows for obtaining 3D data with a lower cost than other 3D techniques, but it has not been previously applied to the study of small mammals. Accordingly, here we test the suitability of photogrammetric techniques to obtain 3D landmarks on mouse skulls as a model for small mammals. Shape and size of 3D models obtained with photogrammetric techniques were consistent among replicates, even when different sets of photographs were used. The linear measurements obtained from 3D models produced here were highly correlated with measurements obtained with callipers on actual crania, and differences among both sets of measures were smaller than those among individuals in most of the tested measures. These results show for the first time that photogrammetry is a precise technique for 3D shape analysis of small mammals. Photogrammetry also proved to be accurate for obtaining linear measurements between 3D landmarks; however, further studies are needed to demonstrate that this technique is also accurate to recreate 3D shapes.     

Carving out turf in a biodiversity hotspot: multiple,previously unrecognized shrew species co‐occur on Java Island,Indonesia

In theory, competition among species in a shared habitat results in niche separation. In the case of small recondite mammals such as shrews, little is known about their autecologies, leaving open questions regarding the degree to which closely related species co‐occur and how or whether ecological niches are partitioned. The extent to which species are able to coexist may depend on the degree to which they exploit different features of their habitat, which may in turn influence our ability to recognize them as species. We explored these issues in a biodiversity hotspot, by surveying shrew (genus Crocidura) diversity on the Indonesian island of Java. We sequenced portions of nine unlinked genes in 100–117 specimens of Javan shrews and incorporated homologous data from most known Crocidura species from other parts of island South‐East Asia. Current taxonomy recognizes four Crocidura species on Java, including two endemics. However, our phylogenetic, population genetic and species delimitation analyses identify five species on the island, and all are endemic to Java. While the individual ranges of these species may not overlap in their entirety, we found up to four species living syntopically and all five species co‐occurring on one mountain. Differences in species' body size, use of above ground‐level habitats by one species and habitat partitioning along ecological gradients may have facilitated species diversification and coexistence.     

Incapacitating effects of fungal coinfection in a novel pathogen system

As globalization lowers geographic barriers to movement, coinfection with novel and enzootic pathogens is increasingly likely. Novel and enzootic pathogens can interact synergistically or antagonistically, leading to increased or decreased disease severity. Here we examine host immune responses to coinfection with two closely related fungal pathogens: Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Both pathogens have had detrimental effects on amphibian populations, with Bd now largely enzootic, while Bsal is currently spreading and causing epizootics. Recent experimental work revealed that newts coinfected with Bd and Bsal had significantly higher mortality than those infected with either pathogen alone. Here we characterize host immunogenomic responses to chytrid coinfection relative to single infection. Across several classes of immune genes including pattern recognition receptors, cytokines, and MHC, coinfected host gene expression was weakly upregulated or comparable to that seen in single Bd infection, but significantly decreased when compared to Bsal infection. Combined with strong complement pathway downregulation and keratin upregulation, these results indicate that coinfection with Bd and Bsal compromises immune responses active against Bsal alone. As Bsal continues to invade naïve habitats where Bd is enzootic, coinfection will be increasingly common. If other Bd‐susceptible species in the region have similar responses, interactions between the two pathogens could cause severe population and community‐level declines.     

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

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.     

Effects of forest disturbance on the fitness of an endemic rodent in a biodiversity hotspot

Praomys delectorum occurs abundantly in both disturbed and intact forests in the Ukaguru Mountains within the Eastern Arc Mountains (EAM), Morogoro, Tanzania. While previous studies have reported that anthropogenic disturbances such as grazing, wood cutting, and harvesting have a positive effect on the population density of P. delectorum, the impact of habitat disturbance on its demographic traits is still unknown. We performed a capture–mark–recapture study in both disturbed and intact forests from June 2018 to February 2020 in order to investigate the effects of habitat disturbance on abundance and two demographic traits: survival and maturation of P. delectorum in the Ukaguru Mountains. We found no variation in abundance or maturation between intact and disturbed forests, but habitat type did affect survival. However, this effect was sex‐dependent since female survival was higher in disturbed forests, while male survival remained similar across the two forest types potentially due to differences in predation pressure or food availability between the two habitats. Continuous demographic monitoring of P. delectorum in EAM is necessary given that the increasing human population surrounding the landscape is leading to higher deforestation rates and expansion of the pine plantation in the forest reserve.