Microendemic Species Research Articles

Paepalanthusserpens, a new microendemic species of Eriocaulaceae from the Espinhaço Range, Minas Gerais, Brazil.

We describe and illustrate Paepalanthus serpens, a microendemic species of Eriocaulaceae from the Espinhaço Range. The species is known from a single population growing in rocky areas of the Serra do Cipó, Minas Gerais. It is placed in Paepalanthus ser. Paepalanthus, and is easily distinguished from its congeneric species by its elongated, lignescent stem, thickened by the marcescent sheaths of the linear leaves, which are arranged in a rosette at the stem apex, scapes equalling the leaf height, and capitulae with straw-coloured involucral bracts. Comparisons with the morphologically similar species are provided, as well as comments on distribution, ecology, phenology and conservation status.

A likely microendemic new species of terrestrial iguana, genus Chalarodon, from Madagascar.

A new species of the hitherto monotypic genus Chalarodon is described from southern Madagascar and a lectotype (ZMB 4360) is designated for C. madagascariensis Peters, 1854. The new species of terrestrial iguana, Chalarodon steinkampi sp. nov., is defined by several morphological characters and by concordant differentiation in mitochondrial and nuclear DNA with >5% uncorrected pairwise genetic distance in the 16S rRNA gene. It can be most clearly recognized by the presence of smooth (vs. keeled) gular and ventral scales, a spotted pattern extending from flanks onto belly, and an unpigmented throat. The new species is known from only a small area between the villages of Amboasary Sud and Esomony, located west of the Andohahela Massif, while C. madagascariensis appears to be widespread over much of southern and western Madagascar. We highlight the need for further exploration of this unprotected region which might host several other microendemic species.

Two new endangered species of Anomaloglossus (Anura: Aromobatidae)from Roraima State, northern Brazil.

We describe two new species of Anomaloglossus from Roraima State, Brazil, that are likely endemic to single mountains currently isolated among lowland forest and savanna ecosystems. The first species, Anomaloglossus tepequem sp. nov. was collected in 1986 and 1992 along a single stream at >500 m elevation on a tepui-like mountain named Tepequém, but was not detected during recent investigations. It is mainly diagnosed from other Anomaloglossus species by its well developed foot webbing, immaculate cream abdomen colouration and small body size (males: 18.2-20.1 mm, females: 21.7-24.5). The second species, Anomaloglossus apiau sp. nov. was found along several streams between 500 and 1400 m elevation on Serra do Apiaú, and is mainly diagnosed from congeners by its weakly webbed feet, males with swollen third finger and ventrolateral stripe formed by white dots, and its advertisement call; a long trill (up to almost 40 s) consisting of pairs of very short pulses. The discovery of these two apparently microendemic species suggests that additional Anomaloglossus species remain to be described in the Guiana Shield. Both species should be considered critically endangered given their seemingly reduced range size, association with highland habitat, and the anthropogenic pressure they currently face.

On the ecology of Cletocamptus gomezi Suárez-Morales, Barrera-Moreno & Ciros-Pérez 2013 (Crustacea, Copepoda, Harpacticoida) micro-endemic to Lake Alchichica, Central Mexico

Cletocamptus gomezi Suárez-Morales, Barrera-Moreno & Ciros-Pérez (2013) is a recently described new species of meiobenthic Harpacticoida copepod, micro-endemic to Lake Alchichica, Puebla, Central Mexico. Cletocamptus gomezi lives in saline water (K25 =12.6 mS cm-1) dominated by sodium, magnesium, chloride, and bicarbonate ions and markedly alkaline (pH 9.0±0.1). Cletocamptus gomezi occurs in a depth range of surface to 10 m with preference to shallow (<3 m), well oxygenated (above saturation) and warm (>20ºC) waters; fine sandy sediments (2.3 ϕ), rich in organic matter (8.4%) and carbonate concentrations (29%), and abundant aquatic vegetation coverage. In the littoral zone the average density and biomass of Cletocamptus gomezi reaches 4106±10,962 ind m-2 and 3.66±9.75 mg C m-2. Below 3 m, along the lake’s slope, the density reduces dramatically down to 265±593 ind m-2 and 0.23±0.51 mg C m-2 at 10 m. Cletocamptus gomezi is absent below 10 m down to 62 m, the maximum depth of the lake. Spatially, except L3 (whose density and biomass values are the lowest) that differs (P<0.05) from L4 (whose density and biomass values are the highest), the littoral sampling stations are statistically similar in density and biomass (P>0.5). Temporally, there are no statistical differences (P>0.5) in density or biomass. The fact of finding Cletocamptus gomezi far away from the coast line (>100 km) and at high altitude (2335 m asl) is uncommon since most reports of Cletocamptus are from coastal brackish waters, and consequently, at sea level. Migrating waterbirds, as dispersal agents could be the explanation of Cletocamptus gomezi successfully inhabiting Lake Alchichica. Cletocamptus gomezi shares the same habitat with dense populations of tubificid oligochaetes, amphipods, leeches, chironomids, and nematodes. The disappearance of Cletocamptus gomezi habitat by the lake’s -natural and mostly anthropogenic- desiccation process, seriously threatens the survival of this and the other numerous micro-endemic species of Lake Alchichica.

A new species of nocturnal gecko (Paroedura) from karstic limestone in northern Madagascar

Paroedura hordiesi sp. n. is described from Montagne des Français, a karstic limestone massif in the far north of Madagascar recently established as nature reserve. The new species has the nostril in contact with the rostral scale and shares many characters with P. karstophila and especially with P. homalorhina which are also restricted to karstic habitats. Paroedura hordiesi differs from P. karstophila by a smoother skin on dorsum and legs, by original and regenerated tails being both entirely smooth, by colouration, and by larger snout-vent length. Morphologically the new species is most similar to P. homalorhina from the Ankarana reserve from which it can be distinguished by shorter limbs and a less slender habitus. Published molecular data place the new species as close relative of P. homalorhina and another undescribed species from Nosy Hara Island, while newly determined data of the cox1 gene for P. karstophila confirm the distinctness of the new species from this taxon. Integrating the information from published and novel molecular data, the new species differs from all nominal Paroedura (except P. vahiny for which no molecular data are available to date) by strong genetic divergences. P. hordiesi might be another microendemic species of the Montagne des Français region. We suggest its IUCN Red List classification as “Critically Endangered” on the basis that it has an extent of occurrence of at most 50 km², it is known from a single location, and there is a continuing decline in the extent and quality of its habitat.

The rediscovery of Perret’s toad, Amietophrynus perreti (Schiøtz, 1963) after more than 40 years, with comments on the species’ phylogenetic placement and conservation status

Perret’s toad, Amietophrynus perreti, has not been seen since 1970 and thus believed to be lost. We searched for the species 50 years after its original description and successfully recorded its continued presence at the type locality, where it seems to maintain a viable population. We failed however, to record the species at suitable sites elsewhere and A. perreti could thus indeed be a micro-endemic species, specialized and restricted to the granite inselbergs of the Idanre Hills, Nigeria. We recorded and discuss potential threats and suggest keeping the toad’s current conservation status as ‘Vulnerable’. We investigated the systematic status of Perret’s toad using a mitochondrial fragment of the 16S rRNA gene and could confirm that it is a member of the genus Amietophrynus despite its aberrant larval biology, different to the rest of the genus. In spite of this biological difference, A. perreti is not a phylogenetically isolated lineage, but is nested within a clade of western African Amietophrynus species, such as A. maculatus, A. regularis, A. latifrons and A. togoensis and is sister to the widespread and savannah dwelling A. maculatus.

Distribution extension for Anolis pseudokemptoni Köhler, Ponce, Sunyer & Batista, 2007 (Reptilia: Squamata: Dactyloidae), a microendemic species in the Serranía de Tabasará of the Comarca Ngöbe-Buglé of western Panama

We report new localities for Anolis pseudokemptoni Köhler, Ponce, Sunyer & Batista, 2007, along the Serranía de Tabasará in the Comarca Ngöbe-Buglé of western Panama. These records extend the known geographic distribution of this lizard about 6 km eastward and 9 km northwestward, as well as the known vertical distribution approximately 470 m lower and 380 m higher. We also provide photos of specimens from different localities and comment on their morphology. No population of this Panamanian microendemic species, which is classifiable as Critically Endangered, lives inside a protected area.

Climate and soil type together explain the distribution of microendemic species in a biodiversity hotspot.

The grasshopper genus Caledonula, endemic to New Caledonia, was studied to understand the evolution of species distributions in relation to climate and soil types. Based on a comprehensive sampling of 80 locations throughout the island, the genus was represented by five species, four of which are new to science, of which three are described here. All the species have limited distributions in New Caledonia. Bioclimatic niche modelling shows that all the species were found in association with a wet climate and reduced seasonality, explaining their restriction to the southern half of the island. The results suggest that the genus was ancestrally constrained by seasonality. A molecular phylogeny was reconstructed using two mitochondrial and two nuclear markers. The partially resolved tree showed monophyly of the species found on metalliferous soils, and molecular dating indicated a rather recent origin for the genus. Adaptation to metalliferous soils is suggested by both morphological changes and radiation on these soils. The genus Caledonula is therefore a good model to understand the origin of microendemism in the context of recent and mixed influences of climate and soil type.

A trait-based approach to assess the vulnerability of European aquatic insects to climate change

Aquatic insects are the dominant taxon group in most freshwater ecosystems. As temperature is the main driver of their life cycle development, metabolic activity, and geographic distribution, these macroinvertebrates are particularly suitable for large scale and comparative studies of freshwater community responses to climate change. A dataset of bio-ecological traits of 1,942 Ephemeroptera, Plecoptera, and Trichoptera (EPT) taxa was used to analyze (1) the relationships among traits, (2) the potential vulnerability of EPT species to climate change, and (3) the geographical occurrence patterns of these potentially endangered species at the scale of European ecoregions. By means of a fuzzy correspondence analysis (FCA), two gradients emerged: (1) a longitudinal gradient, describing successive upstream–downstream features, and (2) a biogeographical gradient, separating endemic and micro-endemic species from widely distributed taxa. Moreover, aquatic insects of southern European ecoregions emerged as those most endangered in terms of potential vulnerability to climate change. Comparative multi-taxon studies provide important new insights into freshwater ecosystem functioning and responses to climate change, and could be the first step toward developing integrative monitoring or assessment tools (e.g., trait-based indicators at the species level) by means of non-arbitrary statistical methods.

From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil

Many species of tropical amphibians are restricted to very small ranges, and this microendemism coupled with ongoing habitat loss and susceptibility to emerging pathogens imperils the long-term persistence of these species. Incomplete taxonomic and distributional knowledge may obscure conservation assessment, particularly in putatively widespread species that are typically considered to be of Least Concern in Red List assessments, but that in fact may constitute complexes of partly microendemic species. Such is the case in the Steindachner’s Robber Frog, Ischnocnema guentheri which, together with the recently recognized Ischnocnema henselii, is thought to occupy most of the Brazilian Atlantic Forest. To test whether these taxa may constitute a species complex of range-restricted and thus potentially threatened species, we analyzed 160 samples of I. guentheri and/or I. henselii for two molecular markers, 16S rRNA (16S) and recombination activation gene 1 (RAG1). To verify the monophyly of the complex, closely related species were also included in the 16S analysis. Congruent evidence from the molecular data and from analyses of advertisement calls support the existence of six distinct species within the complex: I. guentheri and I. henselii as well as four candidate new species. The lineages are distributed as a mosaic in the Atlantic Forest and are sympatric at some localities without indication of admixture. Their phylogeographical pattern partially agrees with paleo-models for the Atlantic Forest, but also suggests the existence of micro-refugia in less stable areas. I. guentheri, previously considered to be widespread, was found only in its type locality, a reserve within the urban area of Rio de Janeiro city. Although none of the species studied appears highly threatened with extinction, we recommend their IUCN threat status to be re-evaluated carefully for the next comprehensive update of the Red List of Brazil’s amphibians.

Resolving an enigma by integrative taxonomy: Madagascarophis fuchsi (Serpentes: Lamprophiidae), a new opisthoglyphous and microendemic snake from northern Madagascar.

Herpetological surveys in the dry forests of the limestone massif Montagne des Français in the far north of Madagascar have recently yielded a number of undescribed reptile species. Here we describe an additional new and potentially microendemic species of the snake genus Madagascarophis (Squamata: Serpentes: Pseudoxyrhophiinae) which lives in this massif syntopically with M. colubrinus septentrionalis and differs distinctly from M. colubrinus and M. meridionalis in its mitochondrial and nuclear DNA sequences. Morphologically Madagascarophis fuchsi sp. nov. is characterized by a broad contact between the posterior inframaxillaries (genials), 25 dorsal scale rows at midbody, and a low number of ventrals (171-172). We redescribe the holotype of M. ocellatus and present new data on the morphological variation of the northern subspecies M. c. septentrionalis and M. c. citrinus. Although Montagne des Français has recently been included into the network of nature reserves in Madagascar, continuous deforestation is strongly threatening this important center of reptile endemism. In line with the assessment of other microendemic reptiles of this massif we suggest to consider the new species as Critically Endangered according to the IUCN criteria and encourage new efforts to protect this area more efficiently.

Understanding the mechanisms underlying the distribution of microendemic montane frogs (Brachycephalus spp., Terrarana: Brachycephalidae) in the Brazilian Atlantic Rainforest

The small geographical range of highly endemic species is an important factor to be considered in conservation initiatives because it can increase their risk of extinction, as well decrease their probability of discovery. In this study, we use environmental niche modeling (ENM) to investigate the distribution of Brachycephalus, an anuran genus characterized by microendemic species living mostly in montane habitats along the Brazilian Atlantic Rainforest. Given that traditional ENM is not possible in the case of Brachycephalus because most of its species have limited geographical ranges, we analyzed an ensemble dataset that combined records of most described species, as well as new species that are currently being described, while accounting for heterogeneity in their climatic niches. Niche heterogeneity was quantified by ordination of the bioclimatic variables associated with their occurrence records, followed by unguided clustering of the resulting ordination scores. Out of an initial dataset of 544 records, careful curation reduced it to 75 records of 24 species and 71 localities. Interestingly, the three major clusters of climatic niches found in Brachycephalus corresponded largely to the three previously recognized phylogenetic lineages in the genus. The pernix cluster included the highly endemic species from southern Brazil that were most restricted to high-elevation areas, whereas the didactylus cluster encompassed species with broader geographical ranges that extended into lowland regions of the Atlantic Rainforest. Finally, the ephippium cluster included species from southeastern Brazil with intermediate levels of endemism. The detection of several isolated locations with potentially suitable habitats indicate that the diversity of Brachycephalus could still be considerably underestimated.

Secondary sympatry caused by range expansion informs on the dynamics of microendemism in a biodiversity hotspot.

Islands are bounded areas where high endemism is explained either by allopatric speciation through the fragmentation of the limited amount of space available, or by sympatric speciation and accumulation of daughter species. Most empirical evidence point out the dominant action of allopatric speciation. We evaluate this general view by looking at a case study where sympatric speciation is suspected. We analyse the mode, tempo and geography of speciation in Agnotecous, a cricket genus endemic to New Caledonia showing a generalized pattern of sympatry between species making sympatric speciation plausible. We obtained five mitochondrial and five nuclear markers (6.8 kb) from 37 taxa corresponding to 17 of the 21 known extant species of Agnotecous, and including several localities per species, and we conducted phylogenetic and dating analyses. Our results suggest that the diversification of Agnotecous occurred mostly through allopatric speciation in the last 10 Myr. Highly microendemic species are the most recent ones (<2 Myr) and current sympatry is due to secondary range expansion after allopatric speciation. Species distribution should then be viewed as a highly dynamic process and extreme microendemism only as a temporary situation. We discuss these results considering the influence of climatic changes combined with intricate soil diversity and mountain topography. A complex interplay between these factors could have permitted repeated speciation events and range expansion.

Biogeography and conservation status assessment ofPseudolaelia(Orchidaceae)

Pseudolaelia is endemic to eastern Brazil, with 12 recognized species occurring primarily in the Atlantic Forest and the cerrado, two of the world's biodiversity hotspots. The aims of this study were to: characterize the geographical distribution patterns, richness, diversity and endemism of Pseudolaelia spp.; compare their distribution with that of Full Protection Conservation Units (FPCUs) and priority areas for biodiversity conservation in Brazil; and determine the species conservation status, indicating areas important for conservation. The biogeography of Pseudolaelia was analysed using herbarium specimens and natural populations, parsimony analysis and geographic information systems. The conservation status was defined according to the International Union for Conservation of Nature. Half of Pseudolaelia spp. are known from less than five sites, and four are micro-endemic, being known from a single site. Nine species should be considered as endangered as a result of habitat degradation. Four species are protected within FPCUs; micro-endemic species are not found in the priority areas for biodiversity conservation. The region of greatest richness, endemism and diversity encompasses the mountainous area in the north-west and north of Espirito Santo and the border with Minas Gerais, this being the central portion of the Cadeia do Espinhaco (Minas Gerais), a centre of secondary richness and diversity. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, ●●, ●●–●●.

Integrating field surveys and remote sensing data to study distribution, habitat use and conservation status of the herpetofauna of the Comoro Islands

We studied the non-marine reptile and amphibian species of the volcanic Comoro archipelago in the Western Indian Ocean, a poorly known island herpetofauna comprising numerous microendemic species of potentially high extinction risk and widespread, non-endemic and often invasive taxa. According to our data, the Comoro islands are inhabited by two amphibian species and at least 28 species of reptiles although ongoing genetic studies and unconfirmed historical records suggest an even higher species diversity. 14 of the 28 currently recognized species of terrestrial reptiles (50%) and the two amphibians are endemic to a single island or to the Comoro archipelago. The majority of species are most abundant at low elevation. However, a few endemic species, like the gekkonid lizards Paroedura sanctijohannis and Phelsuma nigristriata, are more common in or even confined to higher altitudes. We created habitat maps from remotely sensed data in combination with detailed species distribution maps produced using comprehensive data from field surveys between 2000 and 2010, literature, and historical locality records based on specimens in zoological collections. Using these data, we assessed the conservation status of the endemic terrestrial reptiles and amphibians according to the IUCN Red List criteria. Our results show that although little area of natural forest remains on the Comoros, many species are abundant in degraded forest or plantations. Competition and predation by invasive species appears to be the most important threat factor for the endemic herpetofauna, together with habitat degradation and destruction, which further favours invasive species. We propose the status Endangered for three species, Vulnerable for one species, Near Threatened for six species, Least Concern for four and Data Deficient for two species. The endemic subspecies Oplurus cuvieri comorensis is proposed for the status Critically Endangered. Based on the results of this study, seven areas of importance for reptile and amphibian conservation on the Comoros are identified. This study shows how remote sensing data can contribute to increasing accuracy and objectiveness of conservation assessments.

A new relictual and highly troglomorphic species of Tomoceridae (Collembola) from a deep Croatian cave

Tritomurus veles sp. n. (Tomoceridae) is described from a Croatian cave. It is characterized by troglomorphic features (absence of eyes, reduced pigmentation, slender claw, pointed tibiotarsal tenent hairs) that only compare, among Tomoceridae, to the microendemic species Tritomurus falcifer from the Pyrénées. Tritomurus veles also shares with Tritomurus falcifer the absence of macrochaetae on head, a presumably non-adaptive character that within Tomoceridae is unique to these two species. Both species have no known epigean relatives in their respective distribution areas and can be considered as relictual.

Allozyme diversity levels in two congeneric Dioon spp. (Zamiaceae, Cycadales) with contrasting rarities

Springer-Verlag 2010 Abstract Allozyme diversity and population genetic structure studies were conducted in populations of two Mexican cycad species occurring in adjacent and closely related biogeographic regions. We evaluated if rarity traits in Dioon caputoi, a micro-endemic species, and Dioon merolae, a regional endemic with a wider distribution, influence levels of genetic diversity in different ways. We also explored if genetic structure differs in these species, considering that they have similar population histories. Our results indicate that D. caputoi harbors lower levels of genetic diversity and allelic richness (HE = 0.358, P = 76.9, Ar = 1.86) than D. merolae (HE = 0.446, P = 92.3, Ar = 2). However, genetic structure does not differ between the two species despite their contrasting geographic distributions (FST = 0.06 vs. 0.07; D. caputoi and D. merolae, respec- tively). The comparison of population genetic structure information with historical and geographical aspects of the populations suggests that the rarity of D. caputoi might be due to relatively recent local ecological factors.

The Effects of Governmental Protected Areas and Social Initiatives for Land Protection on the Conservation of Mexican Amphibians

Traditionally, biodiversity conservation gap analyses have been focused on governmental protected areas (PAs). However, an increasing number of social initiatives in conservation (SICs) are promoting a new perspective for analysis. SICs include all of the efforts that society implements to conserve biodiversity, such as land protection, from private reserves to community zoning plans some of which have generated community-protected areas. This is the first attempt to analyze the status of conservation in Latin America when some of these social initiatives are included. The analyses were focused on amphibians because they are one of the most threatened groups worldwide. Mexico is not an exception, where more than 60% of its amphibians are endemic. We used a niche model approach to map the potential and real geographical distribution (extracting the transformed areas) of the endemic amphibians. Based on remnant distribution, all the species have suffered some degree of loss, but 36 species have lost more than 50% of their potential distribution. For 50 micro-endemic species we could not model their potential distribution range due to the small number of records per species, therefore the analyses were performed using these records directly. We then evaluated the efficiency of the existing set of governmental protected areas and established the contribution of social initiatives (private and community) for land protection for amphibian conservation. We found that most of the species have some proportion of their potential ecological niche distribution protected, but 20% are not protected at all within governmental PAs. 73% of endemic and 26% of micro-endemic amphibians are represented within SICs. However, 30 micro-endemic species are not represented within either governmental PAs or SICs. This study shows how the role of land conservation through social initiatives is therefore becoming a crucial element for an important number of species not protected by governmental PAs.

Unexplored richness: discovery of 31 new species of Giant Pill-Millipedes endemic to Madagascar, with a special emphasis on microendemism (Diplopoda, Sphaerotheriida)

Thirty-one new species of giant pill-millipedes (order Sphaerotheriida) endemic to Madagascar are described: Zoosphaerium haackeri n. sp., Z. album n. sp., Z. discolor n. sp., Z. mitoho n. sp., Z. pulchellum n. sp., Z. endemicum n. sp., Z. xerophilum n. sp., Z. aureum n. sp., Z. pseudopriapus n. sp., Z. pseudoplatylabum n. sp., Z. solitarium n. sp., Z. tsingy n. sp., Z. corystoides n. sp., Z. broelemanni n. sp., Z. amabile n. sp., Z. trichordum n. sp., Z. smaragdinum n. sp., Z. ambrense n. sp., Z. isalo n. sp., Z. bilobum n. sp., Z. tampolo n. sp., Z. ignotum n. sp., Z. tainkintana n. sp., Z. viridissimum n. sp., Z. denticulatum n. sp., Z. pseudoblandum n. sp., Z. micropiligerum n. sp., Z. pseudopiligerum n. sp., Z. analavelona n. sp. and Z. fisheri n. sp., and Microsphaerotherium anjozorobe n. sp.. Twenty-eight of the Zoosphaerium species already fit into established species-groups. A key to all 55 recognizable Malagasy Sphaerotheriida species is given. Forty-two of the 55 giant pill-millipede species are ecosystem endemics, while 26 are geographically microendemic. The number of microendemic species is disproportionately distributed among Malagasy ecosystems. All 13 species restricted to the montane rainforest as well as all five species restricted to the Eastern littoral forest are microendemic. On the other hand, only two out of seven dry forest species, one out of seven rainforest species and one out of five spiny forest species are microendemics. A special emphasis is placed on two species endemic to the unique Western rainforest site of Analavelona, which is currently not protected.

On the mating and laying sites of Uromenus brevicollis ssp. insularis in Corsica (Ensifera, Tettigoniidae)

Abstract Mating and laying sites of Uromenus brevicollis insularis, a Cyrno-Sardininian micro-endemic species, are described from observations conducted at night in several Corsican localities. Asphodelus ramosus was found to be a key host species as both mating and oviposition of this insect take place mainly on the erect dry stems of the plant. Some aspects of the meeting of the sexes are assessed: male stridulation does not appear to play an important role. The females lay their eggs, creating vertical lines in the stem by chewing regularly spaced holes containing nearly 3 eggs per hole. One to three laying lines can be observed on a single stem. Ferula communis is frequently used as an alternative laying site when A. ramosus is absent or rare, but in this case, the eggs can be attacked by woodpeckers (Dendrocopos sp.) or parasitized by Hymenoptera.