Herpetology Notes, volume 13: 661-666 (2020) (published online on 05 August 2020)

Distribution extension and updated map of Taeniophallus occipitalis (Jan 1863) (, Dipsadidae), with a relevant record to , Northeast

Nilton C. Aquino1,2, Henrique A.C. Maia3,*, Marcelo A.S. Jucá2, and Daniel C. Passos2,4

The tribe Echinantherini (Dipsadidae: ) scales (in Taeniophallus), and the number of pre- is composed by three genera of small to mid-sized diastemal teeth (> 25 in Echinanthera) (Schargel et al., South-American : Echinanthera, Sordellina and 2005; Santos Jr. et al., 2008). Taeniophallus occipitalis Taeniophallus (Pyron et al., 2013; Zaher et al., 2019). and T. quadriocellatus share a large spine in medium- Currently, the Taeniophallus genus is composed by basal region of the assucade side of the hemipenis, nine species, eight of them occurring in Brazil (Costa and a typical dorsal colour pattern of paired vertebral and Bérnils, 2018). The exception, Taeniophallus black blotches. However, in T. quadriocellatus there are nebularis Schargel et al., 2005, is only known from four whitish ocelli on the posterior half of the head and its type locality (Cerro Humo, Venezuela) and remains beginning of the trunk, while T. occipitalis presents only uncertainty assigned to the genus (Schargel et al., 2005). two occipital ocelli (Santos Jr. et al., 2008). The genus is subdivided in three major groups proposed Taeniophallus occipitalis is a small-sized by Schargel et al. (2005): the nebularis group (with (Schargel et al., 2005), has diurnal activity and presents T. nebularis, despite its taxonomic uncertainties), the terrestrial and cryptozoic habits (Guedes et al., 2014), affinis group (composed by T. affinis, T. poecilopogon, being usually found under the litter (Rocha and Prudente, T. persimilis, and T. bilineatus), and the occipitalis group 2010). This species is widely distributed, being recorded (with T. occipitalis and T. quadriocellatus – updated by in Paraguay, Uruguay, Peru, Bolivia, Argentina and Santos Jr. et al. [2008]). The two species of the occipitalis Brazil (Santos Jr. et al., 2008). In Brazil, it can be found group can be distinguished from others Echinantherini in all regions (Santos Jr. et al., 2008; Guedes et al., taxa by having 15–15–15 or 15–15–13 rows of dorsal 2014). In the Northeast, T. occipitalis has been recorded mostly on forested areas of Floresta Atlântica (Atlantic Forest) and Cerrado biomes (Santos Jr. et al., 2008; Sales et al., 2009), besides transition zones between Caatinga and Floresta Atlântica (Atlantic Forest), Cerrado, or Complexo Vegetacional Litorâneo (Amaral, 1 Universidade do Estado do Rio Grande do Norte. Rua Almino 1934; Guedes et al., 2014; Roberto and Loebmann, Afonso, 478, Centro, CEP 59610-210, Mossoró, Rio Grande 2016). In the Caatinga biome, its occurrence is generally do Norte, Brazil. associated with high altitudes, as in Chapada Diamantina 2 Laboratório de Ecologia e Comportamento , and Brejos de Altitude, or close to the coast, in transition Universidade Federal Rural do Semiárido. Av. Francisco Mota, 572, Costa e Silva, CEP 59625-900, Mossoró, Rio areas associated or not with patches of Cerrado (Guedes Grande do Norte, Brazil. et al., 2014; Roberto and Loebmann, 2016). The only 3 Programa de Pós-Graduação em Zoologia, Museu Paraense records to areas of sensu stricto Caatinga are at least Emílio Goeldi and Universidade Federal do Pará. UFPA, 500 m of altitude (e.g. Paulo Afonso/BA – Guedes et al., ICB, Rua Augusto Corrêa, 01, Guamá, CEP 66075-110, 2014) or regions with influence from adjacent biomes Belém, Pará, Brazil. (e.g. Araruna/PB – Arzabe et al., 2005). 4 Programa de Pós-Graduação em Ecologia e Conservação, Herein, we document the first record of Taeniophallus Universidade Federal Rural do Semi-Árido. Av. Francisco Mota, 572, Costa e Silva, CEP 59625-900, Mossoró, Rio occipitalis for Depressão Sertaneja Setentrional Grande do Norte, Brazil. ecoregion in Rio Grande do Norte state, being also * Corresponding author. E-mail: [email protected] the lowest elevation record for this species in an area 662 Nilton C. Aquino et al. of sensu stricto Caatinga. Furthermore, we provide (Myers, 1974; Santos Jr. et al., 2008). The description an updated map of the geographical distribution of of the colour pattern was based on photographic T. occipitalis and a biogeographic overview of its records of live specimens (Fig. 1A). The morphometric occurence in Northeast Brazil. characterisation (1 mm resolution) was made by the The records of Taeniophallus occipitalis were following measures: snout-vent length (SVL), tail performed at Estação Experimental da Universidade length (TL), and head length (HL). The pholidosis was Federal Rural do Semi-Árido – EEU (37.40°W, checked using a stereoscopic microscope, counting the 5.056389°S; WGS84), located in district of Alagoinha, following attributes: number of anterior, middle and rural zone of Mossoró municipality, Rio Grande do posterior rows of dorsals scales, and number of ventral, Norte state. The Mossoró municipality is inserted within subcaudal, cloacal and supralabial scales. the ecoregion of Depressão Sertaneja Setentrional (DSS We compiled all available records of T. occipitalis in – up to 1,127 m a.s.l.), presents a semi-arid hot and dry the scientific literature to provide an updated geographic climate (BSwh’ – Köppen-Geiger), that is marked by distribution map for the species. We considered the elevated daily temperatures and annual averages of 27.5 centroid of the municipality or locality of occurrence ºC of air temperatures, 68.9% of relative air humidity when the exact coordinates of the collection site were and 673.9 mm of annually pluviometric precipitation not available in publications. Since this method can lead (Santos et al., 2014). The collected specimens were to a bias of the elevation information, we considered the sampled by two methods: time-constrained searches elevational range within a 10 km radius from centroids. (TS) and pitfall traps (PT). The voucher specimens were The maps were constructed with QGIS v. 3.4 software euthanised according to the Portaria CFBio 148/2012, (QGIS Development Team, 2018), using vectoral fixed following Aurichio and Salomão (2002), and are delimitations of Brazilian biomes (Olson et al., 2001) housed in the scientific collection Coleção Herpetológica and Caatinga ecoregions (Velloso et al., 2002). For do Semiárido – CHSA at Universidade Federal Rural do environmental categorisation of occurence sites given in Semi-Árido – UFERSA. The taxonomic determination Table 1, we follow Guedes et al. (2014), as here briefly was conducted assessing colour pattern, morphometry explained. We considered “Caatinga” as predominant and pholidosis, and comparisons with the literature semiarid environment characterised by common xeric

Figure 1. Colour pattern in life of Taeniophillus occipitalis (voucher CHSA-R 575) recorded in the Mossoró municipality, Rio Grande do Norte state (A). Details of cephalic pattern and pholidosis of specimen CHSA-R 575 (B). Ilustrations by Nilton Aquino and photo by Daniel Passos. Distribution extension and updated map of Taeniophallus occipitalis 663

Table 1. Details of the geographic locations of Taeniophillus occipitalis in Caatinga domain, in descending order of1 altitudinal elevation for each environment type. Criteria for environmental categorization is provided in methods session. For records Table 1. Details of the geographic locations of Taeniophillus occipitalis in Caatinga domain, in descending order of which exactaltitudinal coordinates elevation were fornot each available environment in publications type. Criteria we provided for environmental the elevation categorization range in isa 10 provided km radius in methods from centroid of municipality/locality.session. For Therecords present which record exact coordinates is highlighted were in not bold. available in publications we provided the elevation range in a 10 km radius from centroid of municipality/locality. The present record is highlighted in bold.

Source Municipality – State Elevation (m) Environment Garda et al. (2013) Paulo Afonso – BA 652 Caatinga Arzabe et al. (2005) Araruna – PB 228 Caatinga Present study Mossoró – RN 80 Caatinga Guedes et al. (2014) Poções – BA 564-1050 Transition zone Santos Jr. et al. (2008) Avelino Lopes – BA 379-677 Transition zone Guedes et al. (2014) Itabaiana – SE 103-658 Transition zone Santos Jr. et al. (2008) Feira de Santana – BA 110-608 Transition zone Rocha and Prudente (2010) Piripiri – PI 100-300 Transition zone Guedes et al. (2014) Piracuruca – PI 74-224 Transition zone Guedes et al. (2014) Teresina – PI 51-199 Transition zone Guedes et al. (2014) Horizonte – CE 21-146 Transition zone Guedes et al. (2014) Fortaleza – CE 0-99 Transition zone Guedes et al. (2014) São Gonçalo do Amarante – CE 39 Transition zone Guedes et al. (2014) Mucugê – BA 676-1650 Wet highland Guedes et al. (2014) Morro do Chapéu – BA 861-1207 Wet highland Guedes et al. (2014) Pacotí – CE 133-1076 Wet highland Pereira Filho and Montingelli (2011) Madre de Deus – PE 1063 Wet highland Guedes et al. (2014) Mulungu – CE 151-1043 Wet highland Guedes et al. (2014) Meruoca – CE 77-1009 Wet highland Guedes et al. (2014) Lençóis – BA 337-1000 Wet highland Guedes et al. (2014) São Caetano – PE 514-949 Wet highland Guedes et al. (2014) Ubajara – CE 654-917 Wet highland Roberto and Loebmann (2016) Tianguá – CE 191-889 Wet highland Loebman and Haddad (2010) Viçosa – CE 110-831 Wet highland Ribeiro et al. (2012) Crato – CE 758 Wet highland Amaral (1934) Areia – PB 125-636 Wet highland

drought vegetation, generally low elevation (< 500 m), Prudente (2010) gives details from Piauí areas, and high mean annual temperatures and solar radiation, Moro et al. (2015) about northern coastal vegetation and scarce and irregular rainfall and low humidity along all its complex and ecotonal profile. the year. The exception landscapes from this profile, On 30 January 2018, a female individual of T. were considered as “wet highlands” (Brejos de Altitude) occipitalis (CHSA-R 575) was sampled by PT method or “transition zones”. The first are characterised by (Fig. 1), and on 22 September 2018, we collected the high elevation (> 600 m) surrounded by Caatinga, a second female specimen (CHSA-R 1229) by AS markedly presenting high pluviometric rate and lower method. This second individual was foraging among the mean temperatures, frequently harbouring complex leaf-litter when was caught. Both specimens presented humid and dense vegetation formations. We further the following chromatic pattern (see Fig. 1): two paired follow Pereira Filho and Montingelli (2011) and Moro light occipital ocelli; a pale line following the canthus et al. (2015) for specific area discrimination. The latter rostralis, that extends almost to the anterior suture of constitute ecotonal areas highly influenced by adjacent the parietal scales; light gular region, painted by small biomes and previously categorised within Caatinga and sparsely black dots from the mental plates to the biome at least in one classification. Further, Rocha and beginning of the trunk; trunk with dorsal black blotches 664 Nilton C. Aquino et al. anteriorly and spotted posteriorly; ventral region of 2014), 245 km NW from Araruna municipality, Paraíba the trunk yellowish, gently pigmented on the sides. state (Arzabe et al., 2005), and 260 W from Natal CHSA-R 575 and CHSA-R 1229 had respectively 240 municipality, Rio Grande do Norte state (Sales et al., and 390 mm SVL, 90 and 100 mm TL, 9.6 and 11.5 2009). Furthermore, this finding constitutes the second mm of HL, and presented respectively: 15–15–13 and record of T. occipitalis for the Rio Grande do Norte state, 15–15–15 rows of smooth dorsal scales without apical reporting by the first time the occurrence of species pits; 159 and 164 ventrals; 72 and 67 subcaudals; both for the semiarid region in this state. In fact, no other with divided cloacal plate and eight supralabials, with previous herpetological inventory in Caatinga areas of the second one in contact with the loreal and the third the state recorded this species (Lima-Verde, 1976; Freire to the fifth ones in contact with the orbit (Fig. 1). All et al., 2009; Caldas et al., 2016; Calixto and Morato, chromatic, meristic and morphometric characteristics of 2017). The only previous record of T. occipitalis in the both collected specimens matched with the descriptions Rio Grande do Norte state was made for the Parque and taxonomic reviews of Taeniophallus and allowed Estadual das Dunas do Natal, a coastal habitat inserted the precise determination of both specimens as T. in the Floresta Atlântica (Atlantic Forest) biome (Sales occipitalis (sensu Santos Jr. et al., 2008). et al., 2009, voucher specimen confirmed by Raul Sales The new records for Mossoró fulfilled a geographic as UFRN 1207). distribution gap of about 400 km, placing approximately The study site is located at 80 m above sea level 160 km E from the nearest previously recorded locality, (Table 1) and is inserted in the Depressão Sertaneja in Horizonte municipality, Ceará state (Guedes et al., Setentrional ecoregion (Fig. 2a). Thus, this report also

Figure 2. Updated distribution map of Taeniophillus occipitalis at two scales: A – all records along Brazilian biomes sensu Olson et al. (2001); B – records restricted to the Caatinga biome and its ecoregional divisions sensu Velloso et al. (2002). Red circle constitutes the new record to the Mossoró municipality in Rio Grande do Norte state. White symbols correspond to the previously known records to sensu stricto Caatinga areas (circles), wet highlands (triangles) and transition zones (squares). Distribution extension and updated map of Taeniophallus occipitalis 665 constitutes the lowest elevation record of T. occipitalis Acknowledgements. We are grateful to the administrative staff of for a sensu stricto Caatinga area. This species has been the Estação Experimental da UFERSA – EEU for all the logistical usually found above 500 m altitude (Table 1), and support that enabled the execution of this project. We thank all members of the Laboratório de Ecologia e Comportamento Animal most records of T. occipitalis in Caatinga domain were – LECA whom contributed with this research, in particular Pamella made in the wet highlands or transition zones (Table 1; Soares (by collection of the second specimen) and Jefferson Senna see also Guedes et al., 2014; Roberto and Loebmann, (by help with meristic counts). We also thank the Instituto Chico 2016 for same conclusion). Moreover, although there Mendes de Conservação da Biodiversidade – ICMBio by the are records below 100 m altitude (e.g. Teresina-PI authorisation to collect the voucher specimens (57265-1). and Horizonte-CE – Guedes et al., 2014), these areas constitute transition zones highly influenced by Cerrado References areas. Despite Horizonte-CE is theoretically included in Amaral, A. (1934): Collecta Herpetologica no Nordeste do Brasil. the Depressão Sertaneja Setentrional ecoregion, actually Memmorias do Instituto Butantan 8: 185–195. it is a Cerrado patch inside the Complexo Vegetacional Arzabe, C., Skuk, G., Santana, G.G., Delfim, F.R., Lima, Y.C.C., Litorâneo (see Moro et al., 2015). Therefore, record Abrantes, S.H.F. (2005): Herpetofauna da área de Curimataú, Paraíba. In: Análise das variações da biodiversidade do bioma from Horizonte must be considered as a transition zone, caatinga. Suporte a estratégias regionais de conservação, pp. not a sensu stricto Caatinga area (Velloso et al., 2002). 259–273. Araújo, F.S., Rodal, M.J.N., Barbosa, M.R.V., Orgs., The only two records effectively located in sensu stricto Brasília, Brazil, Secretaria de Biodiversidade e Florestas, Caatinga areas (Araruna-PB – Arzabe et al., 2005 and Ministério do Meio Ambiente. Paulo Afonso-BA – Garda et al., 2013) are located Caldas, F.L.S., Costa, T.B., Laranjeiras, D.O., Mesquita, D.O., above 200 m altitude, at different ecoregions, and at 485 Garda, A.A. (2016): Herpetofauna of protected areas in the km from each other (245 and 533 km from the present Caatinga V. Seridó Ecological Station (Rio Grande do Norte, Brazil). Check List 12: 1–14. record). Together, these features likely implicate in Calixto, P.O., Morato, S.A.A. (2017): Herpetofauna recorded by a environmental conditions (humidity and temperature) fauna rescue program in a Caatinga area of João Câmara, Rio and vegetational aspects (flora composition and Grande do Norte, Brazil. Check List 13: 647–657. phytophysiognomy) substantially distincts between Costa, H.C., Bérnils, R.S. (2018): Répteis do Brasil e suas unidades these areas. Additionaly, higher elevations can lead to federativas. Lista de espécies. Herpetologia Brasileira 8: 11– relatively milder climatic factors and harbour different 57. Freire, E.M.X., Sugliano, G.O.S., Kolodiuk, M.F., Ribeiro, L.B., vegetational composition other than a xeric drought Maggi, B.S., Rodrigues, L.S., et al. (2009): Répteis Squamata and hot climate adapted strictu sensu vegetation (e.g., das Caatinga do Seridó do Rio Grande do Norte e do Cariri carrasco, dry forest – Moro et al., 2015), which is the da Paraíba. Síntese do conhecimento atual e perspectivas. In: predominant profile below 100 m altitude. Thus, these Múltiplos olhares sobre o semiárido brasileiro. Perspectiva arguments reinforce the ecological relevance of the new interdisciplinar. Freire, E.M.X., Cândido, G.A., Azevedo, P.V., record herein reported to Mossoró municipality, once it Orgs., Natal, Brazil, EDUFRN. Garda, A.A., Costa, T.B., Santos-Silva, C.B., Mesquita, D.O., would be hitherto considered as an unlikely area for the Faria, R.G., Conceição, B.M., et al. (2013): Herpetofauna of occurrence of T. occipitalis. protected areas in the Caatinga I. Raso da Catarina Ecological At a large scale, a total of 240 records showed that the Station (Bahia, Brazil). Checklist 9: 405–414. species is widely distributed throughout South America, Guedes, T.B.N., Cristiano, M., Otavio, A.V. (2014): Diversty, occurring in all Brazilian biomes, with large amount of natural history, and geographic distribution of snakes in the records in both forested (Floresta Atlântica) and open Caatinga, Northeastern Brazil. Zootaxa 3863: 1–93. (Cerrado and Pampas) biomes (Fig. 2a). Based on over Lima-Verde, J.S. (1976): Fisioecologia e etologia de algumas serpentes da chapada do Apodi, estados do Ceará e Rio Grande 20 literature records of occurrence in Caatinga biome, T. do Norte (Brasil). Caatinga 1(1): 21–56. occipitalis occurred in almost all Caatinga ecoregions, Loebmann, D., Haddad, C.F.B. (2010): Amphibians and except in Depressão Sertaneja Meridional and Dunas from a highly diverse area of the Caatinga domain. Composition do São Francisco (Fig. 2b). Although this species might and conservation implications. Biota Neotropica 10: 227– 253. be usually associated to open landscapes, in Caatinga Moro, M.F., Macedo, M.B., Moura-fé, M.M., Castro, A.S.F., Costa, domain it has been predominantly recorded in ecotonal R.C. (2015): Vegetação, unidades fitoecológicas e diversidade paisagística do estado do Ceará, Brasil. Rodriguésia 66: 717– or high elevated forested habitats, which might suggest 743. a possible preference by mild climatic areas. However, Myers, C.C. (1974): The systematics of Rhadinaea (), a the present records indicate that low elevation semiarid genus of New World snakes. Bulletin of the American Museum habitats are not necessarily unsuitable for this species. of Natural History 153: 1–262. 666 Nilton C. Aquino et al.

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Accepted by Alessandro Morais