Description of the male of the Critically Endangered tarantula Typhochlaena curumim Bertani, 2012 (Araneae, Theraphosidae), with comments on tarantula trade and conservation

Abstract The genus Typhochlaena C.L. Koch, 1850 consists of five small size arboreal tarantula species with remarkable colored abdominal patterns and a very restricted geographic range in Brazil. Here, we describe the male of Typhochlaena curumim Bertani, 2012, which was collected in an area of Brazilian Atlantic Rainforest. The new record extends the northern limit of the geographic range for both the genus and species. As Typhochlaena spp. are now especially popular and requested in the pet market, and because T. curumim is classified as Critically Endangered, we discuss the impacts of the international trade and other challenges on conservation of the genus.


Introduction
The genus Typhochlaena C.L. Koch, 1850 was erected 170 years ago (Koch 1850) to include Typhochlaena seladonia (C.L. Koch, 1841) and Typhochlaena caesia (C.L. Koch, 1842) (now in Caribena Fukushima & Bertani, 2017). The first taxonomic revision and description of other species was only published in 2012 by Bertani (2012), who described Typhochlaena amma Bertani, 2012, Typhochlaena costae Bertani, 2012, Typhochlaena paschoali Bertani, 2012, and Typhochlaena curumim Bertani, 2012, all species endemic to Brazil. The genus is characterized by having a domed, short distal segment of the posterior lateral spinneret in all stages and a sternum, in adults, as long as wide and truncated behind (Bertani 2012). They are well known as small arboreal tarantulas with remarkable colored abdominal patterns, and they are becoming popular and increasingly requested in the pet trade, probably due to these characteristics.
Typhochlaena curumim is a species known from only three female specimens that were found under loose bark in an area of Atlantic Rainforest in the state of Paraíba, Brazil. Recently, males of the species were collected during arachnological expeditions in the state of Rio Grande do Norte, Brazil, and the aim of this paper is, therefore, to describe the previously unknown male of T. curumim and discuss problems of conservation as they relate to this genus.

Material and methods
Specimens were deposited at the Museu Nacional, Rio de Janeiro (MNRJ) and at Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP). A specimen from "Coleção de Arachnida" of the "Centro de Coleções Taxonômicas da Universidade Federal de Minas Gerais" (UFMG) was examined by photography.
The general format of the description is based on Bertani (2012). All the measurements are in millimeters (mm). A Leica M205C stereomicroscope with a DFC 450 camera attached, combined with a Leica LAS Montage and LAS 3D modules, was used to obtain images and measurements of small body parts. Large body parts, such as leg articles and carapace, were measured with digital Mitutoyo calipers with an error of 0.005 rounded up to two significant decimals. The measurements of legs and palps were taken on the dorsal aspect of the left side, unless appendages were lost, damaged, or obviously regenerated. Structures of the left side of the specimens were chosen for descriptions. Geographical coordinates and other locality details of the new records are redacted from this publication due to concerns that they may facilitate illegal collecting for the pet trade (Lindenmayer and Scheele 2017). Researchers interested in those records may obtain them directly from the institutions where the specimens are deposited. The map was made using the R package red -IUCN Redlisting Tools (Cardoso 2017). In the absence of better information, we assumed that the area within the convex hull polygon encompassing all known records had similar density of suitable habitat, i.e. Atlantic Rainforest remnants (according to SOS Mata Atlântica 2018), as the three states within it. As we expect the species to be present in several fragments within this polygon, we calculated the area of occupancy (AOO) as equal to extent of occurrence (EOO) multiplied by the proportion of Atlantic Rainforest in the three states. Terminology for urticating setae follows Cooke et al. (1972). Abbreviations: ALE = anterior lateral eye; AME = anterior median eye; ITC = inferior tarsal claw; PLE = posterior lateral eye; PLS = posterior lateral spinneret; PME = posterior median eye; PMS = posterior median spinneret. Figures 1-12 Diagnosis. Males of T. curumim resemble those of T. seladonia by having a long embolus, two or more times the tegulum length. Males of T. curumim differ from males of T. seladonia by the presence of shorter and broader embolus (≤ 2.5× length of tegulum in T. curumim versus > 3.5× in T. seladonia; 0.24 mm basal embolus width in T. curumim versus 0.1 mm in T. seladonia). They also differ by the brownish carapace and legs and abdomen dorsum with a black longitudinal stripe and lateral spots (Figs 1, 3). Apart from the long embolus (Figs 6-10), males of T. curumim differ from males of Typhochlaena costae and Typhochlaena amma by the characteristic abdominal color pattern (Figs 1, 3). Additionally, they differ from those of T. costae by the absence of long, curled, yellow setae over the carapace. For females, see the diagnosis by Bertani (2012). Fovea: slightly procurved, shallow, 0.66 wide. Eyes: eye tubercle 0.88 high, 0.81 long, 1.48 wide. Clypeus absent. Anterior row of eyes procurve. Posterior row of eyes slightly recurve. Eye sizes and interdistances: AME 0.35, ALE 0.35, PME 0.23, PLE 0.28, AME-AME 0.20, AME-ALE 0.19, AME-PME 0.05, ALE-ALE 0.20, ALE-PME 0.29, PME-PME 0.83, PME-PLE 0.05, PLE-PLE 1.11, ALE-PLE 0.2, AME-PLE 0.26.
Labium: 0.60 long, 1.04 wide, with 50 cuspules spaced by one diameter of each other on the anterior half. Labio-sternal groove shallow and flattened, with two slightly separate, large sigilla.
Chelicera: rastellum absent, basal segment with seven teeth and some small teeth on promargin.
Sternum: 2.45 long, 2.40 wide. Sigilla: three pairs, posterior and median rounded, less than one diameter from margin; anterior not visible.
Distribution. In Brazil in the states of Rio Grande do Norte and Ceará (new records), and Paraíba (Bertani 2012), in remnants of Brazilian Atlantic Rainforest (Fig. 12).
Color pattern ontogeny. There are no drastic ontogenetic changes of color pattern. Males have reduced lateral black stripes when compared to females and immatures. Natural History. Males from a more northerly site in Rio Grande do Norte (approximately at 6.02°S, 35.2°W) were resting on a leaf in a bush near a trail during the night, or high in a tree, walking on branches during the day. Males from a southern site in Rio Grande do Norte (approximately at 6.46°S, 35.0°W) were also found to be active at night in trees; one individual was seen at breast height and another at less than 2 m above the ground.  Bertani, 2012. A large spatial error has been introduced to avoid revealing exact localities.

Discussion
As in other genera of Aviculariinae, Typhochlaena species have a very restricted geographic range, with no overlap in the distribution among species (Bertani 2012). As proposed for species occurring in the Brazilian Atlantic Rainforest (Pellegrino et al. 2005), the geographic ranges of Typhochlaena species are mostly concordant with with river basins (Bertani 2012). The southernmost record for this genus is southern Espírito Santo; however, a new record of T. curumim, from northern Ceará, is the most northern for Typhochlaena.
Although two other aviculariine species, Iridopelma hirsutum Pocock, 1901 andPachistopelma rufonigrum Pocock, 1901, have similar distributions to T. curumim, T. curumim is probably more affected by habitat loss, given its rarity (Bertani 2012). Moreover, the habits and ecological traits of T. curumim are poorly known, making it difficult to monitor and propose measures for its conservation. As Typhochlaena is the sister group of a large clade within Aviculariinae, conservation actions towards this species are equally applicable for preservation of the evolutionary diversity of the entire subfamily (Vane-Wright et al. 1991;Faith 1992).
Considering the whole genus as of 2012, only 40 specimens are deposited in zoological collections (Bertani 2012), and the current situation is most likely not much different. In contrast, the number of specimens detected in the pet trade is much higher. A brief online search revealed specimens of Typhochlaena spp. being sold in Germany, Spain, Czech Republic, Austria, South Africa, Poland, United Kingdom, Canada, and USA. Although Brazilian environmental law precludes the collection, possession, transport, export, and commercialization of Brazilian wildlife apart from exceptional cases (IBAMA 1998 -Lei de Crimes Ambientais 9605/98), theraphosid specimens are constantly smuggled out of the country to supply the pet trade.
The international pet trade is an important driver of biodiversity loss (Bush et al. 2014). However, since invertebrates are usually overlooked when formulating conservation actions and policies (Cardoso et al. 2011), tarantula trafficking has low priority for enforcement authorities. Loopholes in Brazilian environmental law, permeability of borders, and the ease of smuggling spiders internationally by "brown-boxing" specimens (i.e. sent in unlabeled packages by post) also contribute to the flow of tarantulas from Brazil to other points of the world. Once out of the country, many Brazilian specimens of tarantulas are sold in the pet trade. Although the presence of Brazilian tarantulas on the North American and European markets is not recent, records of seizures are very scarce (Caldas et al. 2018). Curbing tarantula trafficking is further complicated by the differing legislation and attitudes among the various countries. In the European Union, for example, it is allowed to acquire most non-CITES wildlife without restrictions, but in the USA the situation is quite different. The release of an official communication from the United States Fish and Wildlife Services (USFWS) applying the Lacey Act (http://www.thetkc.org/usfws-statement-regarding-contraband/) to a shipment of Typhochlaena seladonia of a well-known breeder demonstrates this differ-ence. The Lacey Act requires US citizens to comply with laws enacted in foreign countries related to flora and fauna endemic to those countries (Lacey , and all US citizens possessing or trading in imported Brazilian tarantula specimens, or their offspring, are violating US law because such activities are illegal in Brazil. Even though there was not any repatriation or re-introduction in the wild, the application of the Lacey Act to tarantula commercial shipments may be crucial in bringing attention to the pet trade, its association with wildlife trafficking, and in initiating an important discussion about the role of hobbyists, breeders, and traders in promoting or curbing this illegal activity. Typhochlaena curumim, along with T. seladonia, was included in the Brazilian Red List of Threatened Species (ICMBio 2018). Typhochlaena curumim was classified as Critically Endangered, whereas T. seladonia was considered Endangered. The fact that T. curumim was known only from a single locality, an enclave of forest surrounded by dry areas, was a relevant reason for the assessors to consider the species as Critically Endangered. Although there are no data on the number of locations or if this species is severely fragmented, the inferred continuing decline in the extent and quality of habitat is still present and the new records presented here extend the species' area of occupancy to 204 km 2 . This might contribute to a future change in classification from Critically Endangered to Endangered.
There are several difficulties in assessing the risk of extinction of invertebrates, mainly due to the scarcity of data on distribution and population size (Cardoso et al. 2011). Furthermore, invertebrates are normally described using one or very few specimens from a single locality; therefore, new species are frequently fit into the higher categories of threat after their first description. An example is Phoneutria bahiensis Simó & Brescovit, 2001, described in 2001(Simó and Brescovit 2001 from four localities approximately 400 km apart and included in the Brazilian Red List in 2003 (MMA 2003). Just a few years later, the distribution of this species was considerably extended (Martins and Bertani 2007;Dias et al. 2011) and P. bahiensis was subsequently removed from the Red List (ICMBio 2014). Thus, it is necessary to pay attention to this peculiarity when assessing species for the Red List, as new data can rapidly discredit assessments of little-known species, as well as the whole list.
Despite the Brazilian Red List having no status of law, a species' presence on the list increases the penalties for environmental crimes in Brazil by at least tenfold (MMA 2008). In this sense, it should discourage one to collect and to smuggle Red-Listed species. However, the penalties have not been sufficient to prevent international trafficking. The presence of a species in the trade can potentially affect wild populations, particularly in range-restricted species that have attracted international demand (Jansen and Leupen 2019), which is the case of Typhochlaena spp. A helpful conservation action would be the inclusion of Typhochlaena spp. in the global IUCN Red List, as this would draw the attention of international authorities and decision makers worldwide. Another important tool to regulate and to protect species from trade overexploitation is CITES, the Convention on International Trade in Endangered Species of Wild Fau-na and Flora. The addition of all Typhochlaena spp. in CITES appendix I, which lists species threatened with extinction due to trafficking from the wild (and consequently prohibited from international trade unless the import purpose is non-commercial) (CITES 2020), would control or at least make tracking the rampant trade of the genus mandatory. This would be particularly relevant to the EU, as its lack of a consistent approach to legislation related to the trade in wild exotic pets (Endcap 2012) make it the primary destination of smuggled wildlife.