Scientists discover that for Australia the long-beaked echidna may not be a thing of the past

The western long-beaked echidna, one of the world’s five egg-laying species of mammal, became extinct in Australia thousands of years ago…or did it? Smithsonian scientists and colleagues have found evidence suggesting that not only did these animals survive in Australia far longer than previously thought, but that they may very well still exist in parts of the country today. The team’s findings are published in the Dec. 28, 2012 issue of the journal ZooKeys.

With a small and declining population confined to the Indonesian portion of the island of New Guinea, the western long-beaked echidna (Zaglossus bruijnii) is listed as "Critically Endangered" on the International Union for Conservation of Nature’s Red List of Threatened Species. It is also considered extinct in Australia, where fossil remains from the Pleistocene epoch demonstrate that it did occur there tens of thousands of years ago. Ancient Aboriginal rock art also supports the species’ former presence in Australia. However, no modern record from Australia was known to exist until scientists took a closer look at one particular specimen stored in cabinets in the collections of the Natural History Museum in London. Previously overlooked, the specimen’s information showed that it was collected from the wild in northwestern Australia in 1901―thousands of years after they were thought to have gone extinct there.

"Sometimes while working in museums, I find specimens that turn out to be previously undocumented species," said Kristofer Helgen of the Smithsonian Institution, the lead author and the scientist to first report the significance of the echidna specimen. "But in many ways, finding a specimen like this, of such an iconic animal, with such clear documentation from such an unexpected place, is even more exciting."

Long-beaked echidnas are known as monotremes―a small and primitive order of mammals that lay eggs rather than give birth to live young. The platypus, the short-beaked echidna, and the three species of long-beaked echidna (Western, Eastern and Sir David Attenborough’s) are the only monotremes that still exist. The platypus is found only in eastern Australia, the short-beaked echidna is found in Australia and New Guinea, and the long-beaked echidnas were previously known as living animals only from the island of New Guinea. Long-beaked echidnas, which grow to twice the size of the platypus or the short-beaked echidna, are beach-ball sized mammals covered in coarse blackish-brown hair and spines. They use their long, tubular snout to root for invertebrates in the forests and meadows of New Guinea. Among many peculiar attributes, reproduction is one of the most unique―females lay a single leathery egg directly into their pouch where it hatches in about 10 days.

The re-examined specimen in London reveals that the species was reproducing in Australia at least until the early 20th century. It was collected in the West Kimberley region of Western Australia by naturalist John T. Tunney in 1901, on a collecting expedition for the private museum of Lord L. Walter Rothschild in England. Despite collecting many species of butterflies, birds and mammals (some new to science at the time), no full report on his specimens has ever been published. The collection, including the long-beaked echidna specimen, was then transferred to the Natural History Museum in London in 1939 after Rothschild’s death. It was another 70 years before Helgen visited the museum in London and came across the specimen with the original Tunney labels, which both challenged previous thinking about the species’ recent distribution and offered insight into where it may still occur.

"The discovery of the western long-beaked echidna in Australia is astonishing," said Professor Tim Flannery of Macquarie University in Sydney, referring to the new study. "It highlights the importance of museum collections, and how much there is still to learn about Australia’s fauna."

Learning whether the western long-beaked echidna still exists in Australia today will take time. "The next step will be an expedition to search for this animal," Helgen said. "We’ll need to look carefully in the right habitats to determine where it held on, and for how long, and if any are still out there." To find it, Helgen hopes to draw on his experience with the species in New Guinea and to interview those who know the northern Australian bush best. "We believe there may be memories of this animal among Aboriginal communities, and we’d like to learn as much about that as we can," he said.

With the species in danger of extinction, finding Australian survivors or understanding why and when they vanished is an important scientific goal. "We hold out hope that somewhere in Australia, long-beaked echidnas still lay their eggs," said Helgen.

Original source
Helgen KM, Miguez RP, Kohen JL, Helgen LE (2012) Twentieth century occurrence of the Long-Beaked Echidna Zaglossus bruijnii in the Kimberley region of Australia. ZooKeys 255: 103–132. doi: 10.3897/zookeys.255.3774

A new fish species from Lake Victoria named in honor of the author of Darwin’s Dreampond

Two new species of cichlid fish from Lake Victoria are described by biologists from Naturalis Biodiversity Center (Research Department Marine Zoology) and the Institute of Biology Leiden (Section Integrative Zoology), the Netherlands. One of these species is named in honour of Tijs Goldschmidt, author of Darwin’s Dreampond. This book, published in nine languages, describes the dramatic extinction of hundreds of cichlid species in Lake Victoria in the 1980s due to the introduced Nile perch and other human induced environmental changes.

In 1985, Leiden biologists made a survey in the Tanzanian part of the lake, with an old ferry as floating lab, to establish the status of the rapidly declining cichlids. During this expedition Tijs studied the egg spots on the anal fin of cichlids for their possible role in the rapid speciation of these fish. In the Emin Pasha Gulf, among a species nicknamed Haplochromis "argens", individuals were found with aberrant egg dummies and lacking red in the fins. Just the kind of example Tijs was looking for to test his theory of speciation by sexual selection. The aberrant individuals were provisionally named H. "dusky argens".

Both "species" play a part in Tijs’ PhD thesis and in other studies. However, a taxonomic description was never made and whether H. "dusky argens" was a separate species or a colour morph remained unclear. In 1987, most cichlid species from the offshore waters of the lake had disappeared, and with them the urge of taxonomic descriptions.

Now, 25 years later, about a quarter of the cichlid species have recovered in the "Nile perch desert", some of them became even more abundant than in the past, but the former common H. "argens" is still extremely rare. The status of H. "dusky-argens" is unknown as it was only caught in the remote Emin Pasha Gulf, which is not sampled nowadays. Research on successfully resurgent species shows that they were able to adapt morphologically to the new environmental conditions. Their body shape, for instance, changed, so that burst swimming to escape predators improved. Preliminary results suggest that such a response is not found in H. "argens".

The above observations triggered the present taxonomic study as a baseline for further research. It shows that several taxonomic characters differ more between the co-occurring populations of H. "argens" and H. "dusky argens" in the Emin Pasha Gulf, than between populations from different locations. This suggests that they are indeed two species, which are morphologically driven apart at places where they co-occur. In case of H. "argens" the nickname was upgraded to the formal name, while H. "dusky-argens" is now named H. goldschmidti.

Original source
de Zeeuw MP, Westbroek I, van Oijen MJP, Witte F (2013) Two new species of zooplanktivorous haplochromine cichlids from Lake Victoria, Tanzania. ZooKeys 256: 1–34. doi: 10.3897/zookeys.256.3871

Additional Information
Goldschmidt T, de Visser J (1990) On the possible role of egg mimics in speciation. Acta Biotheoretica 38: 125-134.

van Rijssel JC, Witte F (2012) Adaptive responses in resurgent Lake Victoria cichlid over the past 30 years. Evolutionary Ecology. doi: 10.1007/s10682-012-9596-9

Cave dwelling nettle discovered in China

South West China, Myanmar and Northern Vietnam contain one of the oldest exposed outcrops of limestone in the world. Within this area are thousands of caves and gorges. It is only recently that botanists have sought to explore the caves for plants. This exploration is yielding many new species new to science, that are known only from these habitats. The current study was published in the open access journal PhytoKeys.

Kew botanist and nettle expert Alex Monro says, "When my Chinese colleague Wei Yi-Gang from the Guangxi Institute of Botany first mentioned cave-dwelling plants to me, I thought that he was mis-translating a Chinese word into English. When we stepped into our first cave, Yangzi cave, I was spell-bound. It had an eerie moonscape look to it and all I could see were clumps of plants in the nettle family growing in very dark condition".

The plants do not grow in complete darkness but do grow in extremely low light levels, deep within the entrance caverns of the caves (sometimes, in as little as 0.04% full sunlight). The British and Chinese authors have been collecting plants from the Nettle family in this limestone landscape for several years and have just published a paper describing three new species, one from a cave and another two from deep gorges.

The cave-dwelling nettle species in question, was found growing in two caves in the Guangxi province of China. Of the species discovered in gorges, one is known from an unusual and striking rock mineral formation called petaloid travertine. Petaloid travertine is a form of limestone deposited by mineral springs that over time forms large petals of rock, in this case clinging to the vertical walls of a gorge.

These plants are members of a genus of Nettles known as Pilea, that is believed to have over 700 species Worldwide, up to one third of which may remain undescribed.

Original source
Monro AK, Wei YG, Chen CJ (2012) Three new species of Pilea (Urticaceae) from limestone karst in China. PhytoKeys 19: 51–66. doi: 10.3897/phytokeys.19.3968

33 new trapdoor spider species discovered in the American southwest

A researcher at the Auburn University Museum of Natural History and Department of Biological Sciences has reported the discovery 33 new trapdoor spider species from the American Southwest. These newly described species all belong to the genus Aptostichus that now contains 40 species, two of which are already famous – Aptostichus stephencolberti and Aptostichus angelinajolieae.

The genus now includes other such notable species as Aptostichus barackobamai, named for Barack Obama, the 44th President of the United States, and reputed fan of Spiderman comics; Aptostichus edwardabbeyi, named for environmentalist and author Edward Abbey (1927-1989); Aptostichus bonoi from Joshua Tree National Park, named for the lead singer of the Irish rock band U2; Aptostichus pennjillettei named for illusionist and intellectual Penn Jillette; Aptostichus chavezi, named for Mexican American and civil rights and labor activist César Chávez (1927-1993).

Other notable new species names include Aptostichus anzaborrego, known only from the Anza Borrego Desert State Park in southern California; and Aptostichus sarlacc from the Mojave Desert, named for George Lucas’ Star Wars creature, the Sarlacc from the fictional desert planet Tatooine.

The researcher, Prof. Jason Bond, who is a trapdoor spider expert and the director of the Auburn University Museum of Natural History was excited at the prospect of such a remarkable and large find of new species here in the United States and particularly California.

"California is known as what is characterized as a biodiversity hotspot. Although this designation is primarily based on plant diversity, the region is clearly very rich in its animal diversity as well. While it is absolutely remarkable that a large number of species from such a heavily populated area have gone unnoticed, it clearly speaks volumes to how little we know of the biodiversity around us and that many more species on the planet await discovery " Bond said.

Like other trapdoor spider species, individuals are rarely seen because they live their lives in below-ground burrows that are covered by trapdoors, made by the spider using mixtures of soil, sand, and/or plant material, and silk. The trapdoor serves to hide the spider when it forages for meals at the burrow entrance, usually at night.

Aptostichus species are found in an amazing number of Californian habitats to include coastal sand dunes, chaparral, desert, oak woodland forests, and at high altitudes in the alpine habitats of the Sierra Nevada mountain range.

Bond said, "this particular group of trapdoor spiders are among some of the most beautiful with which I have worked; species often have gorgeous tiger-striping on their abdomens. Aptostichus to my mind represents a true adaptive radiation – a classical situation in evolutionary biology where diversification, or speciation, has occurred such that a large number of species occupy a wide range of different habitats".

Bond also noted that while a number of the species have rather fanciful names, his favorite is the one named for his daughter Elisabeth. "Elisabeth’s spider is from an incredibly extreme desert environment out near Barstow, California that is the site of a relatively young volcanic cinder cone. The spiders make their burrows among the lava tubes that extend out from the cone – it is a spectacular place to visit but the species is very difficult to collect because the spiders build rather deep burrow among the rocks".

Original source
Bond JE (2012) Phylogenetic treatment and taxonomic revision of the trapdoor spider genus Aptostichus Simon (Araneae, Mygalomorphae, Euctenizidae). ZooKeys 252: 1. doi: 10.3897/zookeys.252.3588

Additional information
Bond JE and AK Stockman. 2008. An Integrative Method for Delimiting Cohesion Species: Finding the Population-Species Interface in a Group of Californian Trapdoor Spiders with Extreme Genetic Divergence and Geographic Structuring. Systematic Biology, 57: 628-646, doi: 10.1080/10635150802302443

Small wasps to control a big pest?

With the purpose of developing new biological methods to control one of the major pests affecting the southwest Europe pine stands, a joint collaboration leaded by the Instituto Nacional de Investigação Agrária e Veterinária, Portugal (R. Petersen-Silva, P. Naves, E. Sousa), together with the Universidad de Barcelona, Spain (J. Pujade-Villar) and a member of the Museum and Institute of Zoology from the Polish Academy of Sciences, Poland, (S. Belokobylskij) initiated a research to detect the parasitoid guild of the Pine Wood Nematode (PWN) vector, Monochamus galloprovincialis (Olivier).

As the disease slowly spreads across the far west corner of Europe, numerous studies and research lines are being developed. In the last two years, an extensive field work across the entire Portuguese territory, found the presence of 5 small wasps species that directly attack the younger life stages of this pest carrier. The study was published in the open access journal ZooKeys.

"Also considering previous reliable records, showed that worldwide there is now a total of 14 species of potential candidates associated with the bio-control of the vector" said the leading author R. Petersen-Silva. Besides Portugal, some of these findings have been made in other countries such as Italy and Russia (Siberia).

Two of the species now found in Portugal offer promising perspectives: "Despite their generalist habits, they are the most frequent and promising candidates for studies aiming the biological control of the pine sawyer", according to the leading author. All of these wasps are no bigger than a few millimeters, and are known to base their lifecycle on the parasitism of much larger insect hosts. The biology and behavior of these small wasps is not well known yet, and should be studied in the future to help define the best candidate for the control of this pine sawyer.

The obtained results showed that well managed pine stand allow the maintenance of more stable insect communities that more easily control de proliferation of invasive forest pests.

As a result, future trials on the ecology and suitability of these small wasps are being planned by the various researchers working on this project. This approach to the PWN problem could be an additional and deeply-needed step on the fight against the spreading of the disease. This study was co-funded by an European project (REPRHAME) intended to the Development of improved methods for detection, control and eradication of pine wood nematode in support of EU Plant Health Policy.

Original source
Petersen-Silva R, Pujade-Villar J, Naves P, Sousa E, Belokobylskij S (2012) Parasitoids of Monochamus galloprovincialis (Coleoptera, Cerambycidae), vector of the pine wood nematode, with identification key for the Palaearctic region. ZooKeys 251: 29-48. doi: 10.3897/zookeys.251.3986

Additional Information
Naves P, Kenis M, Sousa E (2005) Parasitoids associated with Monochamus galloprovincialis (Olivier) (Coleoptera: Cerambycidae) within the pine wilt nematode-affected zone in Portugal. Journal of Pest Science 78: 5. doi: 10.1007/s10340-004-0068-z
Sousa E, Bravo M, Pires J, Naves P, Penas A, Bonifácio L, Mota M (2001) Bursaphelenchus xylophilus (Nematoda; Aphelenchoididae) associated with Monochamus galloprovincialis (Coleoptera; Cerambycidae) in Portugal. Nematology 3: 89. doi: 10.1163/156854101300106937

‘Mind the gap!’

How well does Natura 2000 cover species of European interest?

The designation of Natura 2000 sites has been based on species and habitats listed in the Annexes of the Habitats and Birds Directive. The effectiveness of the selection process and the resulting Natura 2000 network has often been questioned as each country made its designations largely independently and in most cases without considering the theories of optimal reserve site selection.

Although there have been a series of meetings between the European Commission, the countries and others (including some NGOs), the effectiveness of the selection process and the resulting Natura 2000 network has never been explicitly analysed at the European scale by an independent group.

"Here we present such an analysis, focusing on the representation of different species in the sites, selected for the network. Our results show that it is mostly effective in covering target species and minimizing the number of gap species (i.e. species not represented in a single site of the Natura 2000 network)" said Prof. Klaus Henle, from the Helmholtz Centre for Environmental Research – UFZ in Leipzig, Germany and member of the research team. Their article was published in the Open Access, peer-reviewed scientific journal Nature Conservation.

The authors, however, also demonstrate that the representation is uneven among species. Some species are overrepresented while others are only represented in a low number of sites. "This is mainly due to differing patterns in species ranges, as wide-spread species are inevitably represented in many sites, but narrow ranged species are often covered only by a small number of sites in a particular area" Prof Henle adds.

The team also proposes a representation index,that would detect species that are underrepresented and could be used to direct future conservation efforts – and not only in Europe. "Systematic approaches in planning reserve networks have been intensively developed in the past, to guide efficient reserve site selection. However, on a global scale, no concerted action plan exists to nominate conservation areas, despite repeated calls for international coordination" concludes Prof Henle.

Original source
Gruber B, Evans D, Henle K, Bauch B, Schmeller DS, Dziock F, Henry P-Y, Szabolcs L, Margules C, Dormann CF (2012) "Mind the gap!" – How well does Natura 2000 cover species of European interest?. Nature Conservation 3: 45. doi: 10.3897/natureconservation.3.3732

Boreal bird species of conservation concern affected by climate change

A protected area network should ensure the maintenance of biodiversity, but climate is changing rapidly, thereby creating further demand for the protected area network to be efficient in preserving biota. Due to climate change species ranges are expected to move polewards, which poses challenges to the protected area network.

Population changes of different bird species groups according to their habitat preferences in boreal protected areas in Finland were studied on the basis of large-scale bird censuses carried out in 1981 and in 2000. Mean temperatures rose clearly between the two time slices in Finland, for example, mean April-June temperature by 0.7 °C.

The study "Preserving species populations in the boreal zone in a changing climate: contrasting trends of bird species groups in a protected area network" by Raimo Virkkala from the Finnish Environment Institute and Ari Rajasärkkä from Metsähallitus was published in the open access journal Nature Conservation. Bird censuses were compiled and organized by Metsähallitus, which governs the stated-owned protected areas in Finland. Tens of competent ornithologists carried out the censuses, which included altogether over 11,600 km of line transects.

According to the study, population densities of common forest habitat generalists remained the same between the two periods, while densities of species of conservation concern showed contrasting trends: species preferring old-growth or mature forests increased, but those living on mires and wetlands, and species of Arctic mountains decreased.

"These trends are most probably connected with climate change, but successional changes in protected areas and regional habitat alteration should also be taken into account," says Dr Virkkala, the leading author of the study. Of species preferring old-growth or mature forests, a larger proportion are southern than among species of mires and wetlands, or of Arctic mountains, most or all of which, respectively, had a northerly distribution.

In general, northern species have decreased and southern species increased. It is suggested that climate change effects on species in natural boreal and Arctic habitats most probably are habitat-specific with large differences in response times and susceptibility. Open mires and mountain heaths change more rapidly in consequence of climate warming than old-growth forests, for which reason populations on mires and mountain heaths may also be more affected by climate change.

Original source
Virkkala R, Rajasärkkä A (2012) Preserving species populations in the boreal zone in a changing climate: contrasting trends of bird species groups in a protected area network. Nature Conservation 3: 1. doi: 10.3897/natureconservation.3.3635

Advance in chromosomal evolution in sea cradles

The study of chromosome changes arisen during species evolution is a current and intriguing topic that evolutionary biology proposes. However, in several groups (for example, molluscs), and chitons in particular, chromosome studies are scarce, with a few species investigated and analyses performed mostly with simple methods.

Only 2,5% of about 900 living species of chitons have been so far karyologically investigated, all of them in the same order (Chitonida). The authors note that the species of suborder Chitonina all have a karyotype of 2n=24 chromosomes, all biarmed, that is metacentric or submetacentric. The species studied by the authors, formerly included in Chitonida, also possesses 2n=24 elements, but many are uniarmed and, therefore, resembling to the chromosome complement of species of the suborder Acanthochitonina. This provides support to recent attribution of the studied sea cradle to the latter suborder.

Furthermore, the comparison among the karyotypes of the suborder Acanthochitonina allows the authors to propose that in this group of chromosome changes mainly occurred by fusion among uniarmed elements. This kind of change is that mainly involved in chromosome animal evolution. The study was published in the open access journal Comparative Cytogenetics.

Original source
Petraccioli A, Maio N, Odierna G (2012) Chromosomes of Lepidochitona caprearum (Scacchi, 1836) (Polyplacophora, Acanthochitonina, Tonicellidae) provide insights into Acanthochitonina karyological evolution. Comparative Cytogenetics 6(4): 397. doi: 10.3897/CompCytogen.v6i4.3722

Additional information
Odierma G, Aprea G, Barucca M. Biscotti M, Canapa A, Capriglione T, Olmo E (2008) Karyology of the Antarctic chiton Nuttallochiton mirandus (Thiele, 1906) (Mollusca: Polyplacophora) with some considerations on chromosome evolution in chitons. Chromosome Research 16: 899. doi: 10.1007/s10577-008-1247-1

A pattern given by nature

A ‘regular hexagonal pattern’ was found in a plant-parasitic nematode worm

A new plant-parasitic nematode worm (Meloidoderita salina) was found in a tidal salt marsh at Mont Saint Michel Bay (MSMB) in France, where its abbey is a world-famous historical heritage. The species name ‘salina’ refers to salty soil and is derived from the Latin word ‘sal’ or ‘salis’ meaning ‘salt’. The study was published in the peer-reviewed, open source scientific journal ZooKeys.

The female nematode worm of Meloidoderita salina deposits its eggs in two different structures. One of them is called egg mass which is an external gelatinous matrix, the other one is a cystoid, which is a swollen uterus containing some eggs. Cystoid are harder and stronger than gelatinous matrix. On the surface of the cystoids of Meloidoderita salina, nematologists observed a specific and unique hexagonal beaded pattern.

"This discovery is probably the first observation of a real hexagonal pattern in the group of nematode worms so far, and further research is needed to find out its unknown origin", said Prof. Dr. Gerrit Karssen, one of the senior members of the team.

A tidal salt marsh, a transition zone between land and water, is a highly divers ecosystem. In MSMB, where this new nematode species was found, a large part of its area are tidal salt marshes in which a high number of ecological studies were done, although nematode worms have been mostly neglected.

"Meloidoderita salina is the first plant-parasitic nematode worm described from Mont Saint Michel Bay", said leading author Samad Ashrafi. This new roundworm parasitizes Sea purslane which is a halophytic plant (is found in salt waters). As a vegetable, the leaves of the plant have a salty, spinach-like taste and are edible raw or cooked and are also served in restaurants.

Based on the distribution map of Sea purslane in Europe, the team expects to find this new plant-parasitic nematode worm in "other western European countries such as Belgium, The Netherlands, Germany and the UK".

The nematologists who described this nematode worm predict it is likely to find Meloidoderita salina on other halophytic plants, grown in similar salt marsh areas.

Original Source
Ashrafi S, Mugniéry D, van Heese EYJ, van Aelst AC, Helder J, Karssen G (2012) Description of Meloidoderita salina sp. n. (Nematoda, Sphaeronematidae) from a micro-tidal salt marsh at Mont-Saint-Michel Bay in France. ZooKeys 249: 1–26. doi: 10.3897/zookeys.249.4138

Travels in northeastern Brazil: Unfolding the reptile fauna of Lençóis Maranhenses

In order to be effective, a Conservation Unit must have available a list of the species that live within it. They also should have detailed information about the distribution of species among the available habitats. It would be difficult to correctly plan the conservation actions and/or monitoring programs without some minimal knowledge about the species (who are the object of those measures). "This is why our study is so important to the park", said Dr. Miranda from Universidade Federal do Maranhão (CCAA/UFMA), leading author of the article, published in the open access journal ZooKeys.

In Lençóis Maranhenses National Park 42 species of reptiles were found. Approximately 80% of them live only in restinga habitats, which comprise about 20% of the area currently protected by the park. Restingas have been strongly disturbed by the clandestine openings of paths created to transport tourists to the dunes in the park, using off-road vehicles. This problem is more severe during the rainy season when paths become muddy quickly, and new ones are continuously opening. This could be extremely harmful to those habitats because their poor soil might severely limit natural recomposition.

"We recorded endangered species in Lençóis Maranhenses; particularly sea turtles located in the beach habitats. No one has any idea about the animal activity there! Are they spawning? It’s very likely, but we don’t have any data! It would be very important to study and monitor those species in the 70 km of beaches of the Lençóis Maranhenses National Park" adds Dr. Miranda.

Another turtle species, which deserves attention in Lençóis Maranhenses, is the Brazilian Slider Turtle, which has a limited geographic distribution in the coast of Maranhão, northeastern Brazil. This turtle is used as a source of food by the extremely poor inhabitants of Lençóis Maranhenses and surrounding areas.

"We believe that it would be helpful to promote awareness campaigns to help the conservation of that species, but it is equally important to provide alternatives to the people that live there. These inhabitants, for example, could be placed into the tourism business by providing training courses. They could work as tourist guides, waiters, or cooks. This would not only improve their economic capacity, but also free them of the need to use the Brazilian Slider Turtle as a food item. The efforts for conservation will only be successful with a joint effort of scientists, policymakers and society. We have to talk to one another and look for solutions together", concluded Dr. Miranda.

Original source
Miranda JP, Costa JCL, Rocha CFD (2012) Reptiles from Lençóis Maranhenses National Park, Maranhão, northeastern Brazil. ZooKeys 246: 51. doi: 10.3897/zookeys.246.2593