Two rare species in Espírito Santo state, Brazil: rediscovery of Apostolepis longicaudata Gomes, 1921 (Squamata, Dipsadidae) and Drymoluber brazili (Gomes, 1918) (Squamata, Colubridae)

. We report the rediscovery of two species of rare snake in Espírito Santo state, Brazil: Aposto­ lepis longicaudata Gomes, 1921 (also rare elsewhere in Brazil) and Drymoluber brazili (Gomes, 1918). Apostolepis longicaudata has gone undetected in Espírito Santo for 66 years and Drymoluber brazili for 46 years. Espírito Santo state has only 10% of its forests remaining, and so the rediscovery of these forest‑dwelling species emphasizes the importance of small forest remnants for the conservation. These species have been assessed as Critically Endangered and Endangered in Espírito Santo state.


INTRODUCTION
Rarity describes the geographical distribution and abundance of an organism (Gaston 1994) and is when a species is restricted to a few areas and in these places, there are few individuals compared to other species in the same taxonomic group.Additionally, these taxa often have unique characteristics, such as cryptic or furtive behavior, special life history strategies (Gaston and Curnutt 1998), or a clumped or patchy distribution in the habitat (McDonald and Thompson 2004) which reduces the probability of their detection (McDonald and Thompson 2004;Raphael and Molina 2007).Rarity can lead to underestimating a species' distribution and abundance if, for example, the sampling is not at the appropriate season or time of day (Raphael and Molina 2007).
Snakes are silent and elusive organisms (Greene 2001), and they are arboreal, terrestrial, aquatic, cryp tozoic, or fossorial in varied types of habitats, including forest, mangroves, savanna, and cities, and are absent only in the polar zones (Castro and Silva-Soares 2016).In Brazil, 435 snake species occur (Guedes et al. 2023), of which 82 species are found in Espírito Santo state (Castro et al. 2020;Guedes et al. 2023).Some of the species of snake in this state are rather rare, such as Apostolepis longicaudata Gomes, 1921 andDrymoluber brazili (Gomes, 1918).
Apostolepis longicaudata is endemic to Brazil, with populations occurring in the Cerrado biome, but it also lives in the ecotone between the Cerrado and Caatinga biomes.Only a few records are known from the states of Tocantins, Piauí, Pará, Maranhão, Rio Grande do Norte, Paraíba, and Espírito Santo (Curcio et al. 2011;França et al. 2018;Mesquita et al. 2018;Santos et al. 2018;Nogueira et al. 2019;Marques et al. 2021;Guedes et al. 2023).Its fossorial and cryptozoic habits make it difficult to find, and therefore this species is little represented in collections.The only known population of A. longicaudata from the Atlantic Forest biome is in Espírito Santo (Curcio et al. 2011).
Drymoluber brazili occurs in 12 Brazilian states (Guedes et al. 2023) extending from the northeast to the southeast in the Atlantic Forest, Cerrado, and Caatinga biomes.It also lives in ecotones areas between the Atlantic Forest and the Cerrado, as well as in Paraguay (Costa et al. 2013;Nogueira et al. 2019).Its broad geographical distribution is associated with a large number of voucher specimens in museum collections (Nogueira et al. 2019), and this would lead us to classify this species as common.However, regionally, in Espírito Santo, D. brazili appears to be rare.Here, we present the latest occurrence records in Espírito Santo for A. longicaudata and D. brazili, both rare in the state.Apostolepis longicaudata is also rare elsewhere in Brazil.

METHODS
Fieldwork in northern and mid-western Espírito Santo state was carried out between 2016 and 2021.We explored five forested sites for reptiles.We used pitfalls traps and visual surveys in potential microhabitats such as in leaf litter and trees, under rocks and dead tree trunks, and along streams and lagoons.Pitfall traps, consisting of a 40 L bucket buried to ground level, placed in the interior of the surveyed forest fragments.Specimen collection, when necessary, was authorized by a national and regional permit issue (IEMA no. 020/2016, IEMA no. 016/2018, and IEMA no. 031/2021).Apostolepis longicaudata and the first individual of Drymoluber brazili were found during fieldwork expeditions.The second individual of D. brazili was found during faunal rescue activity.
The collected individual of A. longicaudata was fixed in 100% ethanol and stored in 70% ethanol.The individuals of D. brazili were fixed in 10% formalin and stored in 70% ethanol.All these specimens are deposited in the Museu de Biologia Mello Leitão (MBML), which is part of the Instituto Nacional da Mata Atlântica (Santa Teresa municipality, Espírito Santo, Brazil).
Geographic coordinates were obtained with a Garmin Map60csX GPS receiver using the WGS84 datum.

Apostolepis longicaudata Gomes, 1921
Figure 1 New record.BRAZIL -Espírito Santo The collected individual was identified as A. longicaudata because the following characters: absence of an internal scale and a black band on the tip of the tail (Ferrarezzi et al. 2005;Zaher et al. 2009); The collected individuals were identified as D. brazili because the following characters: 182-202 ventral and 109-127 subcaudal scales, 8 supralabial scales, the 4th and 5th in contact with the eyes, 9 infralabial scales, a single anal plate, split sub-tail scales, and dorsal scales arranged in 17/17/15 (Costa et al. 2013).

DISCUSSION
Apostolepis longicaudata and Drymoluber brazili have not found in Espírito Santo state for many years.Our record in 2016 represents the second record and the rediscovery of this species after 66 years.Therefore, in 2018 we found the fourth record for this species in ES, after 46 years.Northern area of Espírito Santo have been inventoried over the years (Bautz 2020), mainly the last remaining larger forest fragments (e.g.Reserva Natural Vale, Reserva Biológica de Sooretama, and Reserva Biológica do Córrego do Veado; Bérnils et al. 2014), while in the center-west of the state has fewer forest fragments inventoried mainly because of their size (small to medium) associated with their isolation in a matrix of grassland, pasture, and monocultures.The fragments in the mid-west have received less attention by scientific community, but brief inventories have recently been done in small and medium-sized fragments in the northern areas of the midwest, and these two species were not found.
Apostolepis longicaudata has been recorded few times over the years in Espírito Santo, but it is also rare elsewhere in Brazil.This is likely due to its cryptozoic and fossorial habits (typical of Apostolepis species), which makes it difficult to observe A. longicaudata in the field (Harvey 1999).However, D. brazili is not a rare species in Brazil.One of the reasons for few records from Espírito Santo is its preference for open areas in the Caatinga and Cerrado and ecotones between Mata Atlântica and Cerrado biomes (Costa et al. 2013).There are also isolated records in Baixo Guandu and Colatina municipalities (both in Espírito Santo) at  the Espírito Santo-Minas Gerais boundary (Costa et al. 2013;Nogueira et al. 2019).
Espírito Santo was historically covered with the dense Atlantic Forests, and due to the preference of Drymoluber brazili to open habitats, it is unlikely that this species was ever common in the state.Alves et al. (2013) published the rediscovery of Xenodon histricus after 46 years; they mentioned habitat degradation as a threat to this species, which is expected for a forest-specialist species.This is exactly contrary to one of our hypotheses of the rediscovery of Drymoluber brazili, which has preference to open areas and has benefited from human-caused deforestation (Costa et al. 2013).
In a study of patterns of rarity in snake communities worldwide, Luiselli (2006) found that snake species with narrow ecological niches, fossorial, and dietary specialists are more susceptible to rarity, independent of continent, habitat, or climatic.Apostolepis longicaudata and D. brazili appear to present some of these characteristics.
Data on the diet of A. longicaudata is scarce, and there are only one observation of this species preying on a species of Amphisbaena Linnaeus, 1758 (Leite et al. 2022).However, records of predation for other Apostolepis species indicate a preference for Amphisbaena and small snakes: A. multicincta Harvey 1999 preying on Epictia striatula (Smith & Laufe, 1945) (Embert and Reichle 2003); A. multicincta preying on Amphisbaena cegei Montero, Sáfadez, Álvarez, 1997 (Sosa et al. 2015); A. ammodites Werner, 1924 preying upon Psomophis joberti (Sauvage, 1884) (Azevedo et al. 2018).In Brazil, there are 81 species of Amphisbaenia and only seven occurrence in Espírito Santo.Snakes belonging to the families Anomalepididae, Leptotyphlopidae, and Typhlopidae, and others in the family Dipsadidae, are also uncommon in Espírito Santo (Guedes et al. 2023).The uncommonness of its prey may be a reason for the rarity of A. longicaudata in Espírito Santo.
We assume that the rarity of D. brazili in Espírito Santo is for the same reason, although data on its diet are scarce; there is one record of this species preying on a species of Gymnophthalmidae (França et al. 2008), and Pavan and Dixo (2004) have suggested the preference of D. brazili for small frogs.It is probable that the diet of D. brazili is similar to other species of Drymoluber Amaral, 1930, which is mainly composed of gymnophthalmid lizards and small frogs (as we have knowledge).The family Gymnophthalmidae has 101 described species in Brazil, but only six species are known to occur in Espírito Santo (Guedes et al. 2023), and this be a caused of the rarity of D. brazili in this state.
Finally, rare species are at a greater risk of extinction than common species, mainly because small population size are more affected by demographic and environmental events (Boyce 1992).For this reason, understanding the causes of rarity, when it is not natural, is fundamental to promote conservation of populations of D. brazili and A. longicaudata.We recommend additional studies on the taxonomy, geographic distribution, population size, biology, and ecology of these snake species, which will serve as a baseline for conservation actions, such as the creation of conservation units.The new data presented here are from small forest fragments without any protection.Both D. brazili and A. longicaudata are threatened in Espírito Santo, where they been assessed as Endangered and Critically Endangered, respectively (Espírito Santo 2022).
The first record of A. longicaudata from Espírito Santo is from Sooretama municipality in 1950 (MZUSP 2465).The earliest records of D. brazili from the state are from Baixo Guandu municipality in1933 and  1934 (IBSP 8312 and IBSP 8836, respectively), and the third record (IBSP 37413) originates from Colatina municipality in 1974.

Figure 2 .
Figure 2. A. Distribution of Drymoluber brazili (green circles) and Apostolepis longicaudata (pink triangles) in Brazil.B. New occurrence records in the state of Espírito Santo are shown as red triangles for Apostolepis longicaudata and red circles for Drymoluber brazili.