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NORTH-WESTERN JOURNAL OF ZOOLOGY International scientific research journal of zoology and animal ecology of the Herpetological Club - Oradea Univeristy of Oradea, Faculty of Sciences, Department of Biology Univeristatii str. No.1, Oradea – 410087, Romania Publisher: University of Oradea Publishing House Contact e-mail: sas.steve@gmail.com NORTH – WESTERN JOURNAL OF ZOOLOGY (International journal of zoology and animal ecology) ACCEPTED PAPER - Online until proofing - Authors: Jane C. F. OLIVEIRA; Gisele R. WINCK; Juliane P. RIBEIRO; Carlos Frederico Duarte ROCHA Title: Antropogenic or niche preference: contributions on the knowledge of Hemidactylus mabouia invasion in South America Journal: North-Western Journal of Zoology Article number: 152505 Status: awaiting English spelling editing awaiting proofing How to cite: Oliveira J.C.F., Winck G.R., Ribeiro J.P., Rocha C.F.D. (in press): Antropogenic or niche preference: contributions on the knowledge of Hemidactylus mabouia invasion in South America. North-Western Journal of Zoology (online first): art.152505 Date published: <2015-11-13> Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Antropogenic or niche preference: contributions on the knowledge of Hemidactylus 2 mabouia invasion in South America 3 Jane C. F. Oliveira1*, Gisele R. Winck1, Juliane P. Ribeiro1 and Carlos Frederico Duarte N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 1 4 Rocha1 5 1 6 Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, Maracanã, 7 20550-019, Rio de Janeiro, Rio de Janeiro, Brazil. 8 *corresponding author: janeherpeto@gmail.com , Jane de Oliveira Departamento de Ecologia, Instituto de Biologia Roberto de Alcantara Gomes, 9 10 11 12 13 14 15 16 17 18 19 20 1 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Abstract 22 The African gecko, Hemidactylus mabouia, has been recorded from natural habitats in 23 several Brazilian ecosystems. Its establishment seems to be in advanced stage in some N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 21 24 regions of the country. Here we document previously unrecorded populations in sandy 25 coastal plains from Atlantic Forest, associated to the intensity of habitat modification in 26 the studied sites. Our results suggest that the species is usually associated with disturbed 27 areas within larger natural habitats, especially those with some level of vegetation 28 opening (e.g., trails, roads, streets). 29 30 Key-words: Exotic gecko; gekkonid lizard; degradation; open habitat invasion. 31 32 Running title: Exotic gecko in Brazilian natural habitats 33 34 35 36 37 38 39 40 2 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 The African gekkonid lizard Hemidactylus mabouia (Moreau De Jonnès 1818) is a 42 nonindigenous species widely distributed in Brazil and other areas of the Americas (e.g. 43 Rocha et al. 2011, Fierro-Cabo & Rentfro 2014). It is usually associated to anthropic 44 environments (Vanzolini et al. 1980), using areas closer to artificial lighting sources as 45 hunting grounds (Daniells et al. 2008). In some cases, H. mabouia associates to the 46 local native assemblage in several levels (Anjos et al. 2008, Rocha & Vrcibradic 1998, 47 Hatano et al. 2001, Koski et al. 2013) N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 41 48 The records of H. mabouia in Brazilian natural environments are increasing, and 49 include most biomes (e.g. Vanzolini 1968, 1978; Telles et al. 2015) except Amazônia 50 (Rocha et al. 2011). In this study, we conducted surveys to identify new occurrences of 51 H. mabouia in natural environments along the coast of Espírito Santo state, southeastern 52 Brazil. We also documented the vegetation types (mesohabitats) and microhabitats used 53 by the species. Additionally, we evaluated if its presence is related to the intensity of 54 habitat modification. 55 56 57 Material and methods Restingas are sandy coastal habitats characterized by sand dune formations, with 58 relatively high temperatures and low availability of free water compared to other 59 ecosystems within the Atlantic Rainforest biome (Rocha et al. 2003). The vegetation 60 structure varies as the distance from the seashore increases, resulting in distinct 61 mesohabitats or vegetation zones: herbaceous, sparse shrubs, closed post-beach, and 62 restinga forest. 63 We surveyed five sandy dune sites along the state of Espírito Santo (datum 64 WGS84): Praia das Neves (21.14°N, 40.24°W), Paulo Cesar Vinha State Park (20.36°N, 3 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 40.24°W), Comboios Biological Reserve (19.40°N, 39.54°W), Conceição da Barra 66 Environmental Protection Area (18.35°N, 39.44°W) and Itaúnas State Park (18.20°N, 67 39.41°). We conducted visual searches for H. mabouia during day (from 0800 to 1300 68 h) and nighttime (from 1800 to 2300 h) along transections. We searched all potential 69 shelters and microhabitats for adults of H. mabouia or eggs. Eggs were identified 70 considering characteristics as size (approximately 8.5 x 10 mm), the number of eggs in 71 the nest (two or more) (Anjos & Rocha 2008), color and texture/consistency (apud Rose 72 1950). We measured the height from soil using a measuring tape when individuals were 73 perched. Our sampling comprised 75 hours of search from February 2011 to December 74 2013, totaling 15 hours in each vegetation zone in each restinga. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 65 75 We also estimated the occurrence of environmental modification factors in each 76 site (Table 1, modified from Rocha et al. 2007). We considered as "invaders" only those 77 individuals of H. mabouia found in natural environments. Therefore, all lizards 78 documented here were located at least one kilometer away from any residence or urban 79 area (following Cronk & Fuller 1995). We collected the individuals found in natural 80 habitats whenever possible as voucher specimens (SISBIO permit N. 28276). 81 82 Results 83 We found 45 adult individuals in natural environments at three of the five study sites, all 84 during nighttime search, and six eggs/hatched eggs (Table 2). Individuals were found in 85 six different microhabitats, both horizontally (e.g., under bush, sand) and vertically (tree 86 trunks), all of them associated to open vegetation areas (Table 2). Average (± 1SD) 87 height above ground that individuals were found perched was 31 ± 13.8 cm (Ntotal = 45, 88 0 – 75 cm), but most individuals were found perched at heights from ground level to 10 4 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 cm (N = 41, 0 – 10 cm). Our results showed that H. mabouia was usually present in 90 areas where human-mediated modifications in habitat were frequent (Figure 1). 91 However, in all sites where we found H. mabouia, we observed trails, roads and/or 92 streets. o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 89 93 94 Discussion 95 We provide further evidence that the invasion of H. mabouia in natural environments of 96 Espírito Santo state in an advanced stage. Furthermore, two previously undocumented 97 localities (see Rocha et al. 2011) for this species contribute to the knowledge on the 98 invasion of H. mabouia in Brazil. 99 The genus Hemidactylus has had great success in crossing the Atlantic Ocean, naturally colonizing several ecosystems in the Americas (Carranza & Arnold 2006). In 101 our study, we believe we found successful established populations of H. mabouia, due 102 to the occurrence of reproductive events (adults and eggs). Other well-established 103 populations were already documented in Brazilian coastal plains (e.g. Rocha et al. 104 2011), and our data add more information to these observations. The greater number of 105 invasions documented to sandy coastal plains regarding other Brazilian ecosystems may 106 suggest that these areas provide appropriated environmental conditions within their 107 ecological tolerance limits (Kluge 1969). N 100 108 Our results showed a frequent association of H. mabouia to human-modified 109 habitats within larger natural environments, especially those with some degree of 110 opening of vegetation (e.g., due to trails, roads or streets). Although there is still no 111 conclusive evidence whether natural invaded environments have to present some 112 modification level to allow invasion to occur (Silva et al. 2008, but see Gurevitch & 5 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Padilla 2004 to a review), our data suggests that H. mabouia may be benefiting by 114 human alterations in sandy dune habitats of Brazil, especially by vegetation removal. 115 Other evidence that reinforces this hypothesis is that two years after the end of our 116 samples, using the same methods, we recorded three H. mabouia individuals in Paulo 117 Cesar Vinha State Park. Although this restinga is one of the areas with the lowest 118 frequency of human modification, there is a considerable number of trails for beach 119 access. Some biological characteristics of the species favoring its successful 120 establishment in Brazilian environments, may be the wide range of trophic resources 121 and microhabitats used and its nighttime activity. These may facilitate its coexistence 122 with both native diurnal and nocturnal lizards from the invaded communities (e.g., 123 Carranza et al., 2006). There is still no evidence of effects of H. mabouia on native 124 communities (Winck et al. in press). However, we should focus in understanding how 125 much the removal of vegetation is a main factor facilitating its invasion, considering the 126 possibility of invasion by other exotic species. These data would supply the necessary 127 support for the development of appropriated strategies difficulting new invasions of 128 possible harmful species, if necessary. o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 113 129 130 131 N 132 133 134 135 6 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Acknowledgments 137 This study was supported by grants from Conselho Nacional do Desenvolvimento 138 Científico e Tecnológico – CNPq (processes Nos. 304791/2010-5 and 472287/2012-5) o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 136 139 and from Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de 140 Janeiro (FAPERJ) to CFDR (“Programa Cientistas do Nosso Estado” – Process No. E- 141 26/102.765.2012). JCFO thanks the Coordenação de Aperfeiçoamento de Pessoal de 142 Nível Superior – CAPES for providing a Graduate fellowship. GRW thanks FAPERJ for 143 postdoctoral grants (processes n. E-26/101.237/2013 and E-26/101.267/2013). 144 145 146 147 148 149 150 151 N 152 153 154 155 7 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 References 157 Anjos, L.A., Almeida, W.O., Vasconcelos, A., Freire, E.M.X., Rocha, C.F.D. (2007): 158 The Alien and Native Pentastomids Fauna of an Exotic Lizard Population from o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 156 Brazilian Northeast. Parasitology Research 101: 627-628. 160 Anjos, L.A. & Rocha, C.F.D. (2008): Hemidactylus mabouia, a fixed clutch size invader 161 species: how do this gekkonid maximize their reproductive success? Iheringia, Série 162 Zoologia, 98: 1-5. 163 Carranza, S., Arnold, E.N. (2006): Systematics, biogeography, and evolution of 164 Hemidactylus geckos (Reptilia: Gekkonidae) elucidated using mitochondrial DNA 165 sequences. Molecular Phylogenetics and Evolution 38: 531-545. 166 Cronk, Q.C.B., Fuller, J.L. (1995): Plant invaders. Chapman and Hall, London. 167 Daniells, E.A., Ackley, J.W., Carter, R.E., Muelleman, P.J., Rudman, S.M., Turk, P.A., 168 Vélez-Espinet, N.J., White, L.A., Wyszynski, N.N. (2008): An annotated checklist of 169 the amphibians and reptiles of Dominica, West Indies. Iguana 15: 130-141. 170 Fierro-Cabo, A., Rentfro, A. (2014): First record of tropical house gecko Hemidactylus 171 mabouia (Moreau de Jonnès, 1818) in Texas. bioInvasions Records 3(4): 309-312. 172 Gurevitch, J., Padilla, D.K. (2004): Are invasive species a major cause of extinctions? 173 Trends in Ecology and Evolution 19: 470-474. 174 Hatano, F.H., Vrcibradic, D., Galdino, C.A.B., Cunha-Barros, M., Rocha, C.F.D., Van 175 Sluys, M. (2001): Thermal ecology and activity patterns of the lizard community of the 176 restinga of Jurubatiba, Macaé, RJ. Revista Brasileira de Biologia 61: 287-294. 177 Koski, D.A, Koski, A.P.V., Merçon, L, Messas, Y.F. (2013): Hemidactylus mabouia 178 (Tropical House Gecko). Predation. Herpetological Review 44(3). N 159 8 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 179 Kluge, A.G. (1969): The evolution and geographical origin of the New World 180 Hemidactylus 181 Publications Museum of Zoology, University of Michigan 138: 1-78. 182 Rocha, C.F.D.,Vrcibradic, D. (1998): Reptiles as predators and as preys in a restinga 183 habitat of Southeastern Brazil. Ciência e Cultura 50: 364-368. 184 Rocha, C.F.D., Bergallo, H.G., Alves, M.A.S., Van Sluys, M. (2003): A biodiversidade 185 nos grandes remanescentes florestais do Estado do Rio de Janeiro e nas restingas dos 186 corredores da Mata Atlântica. São Carlos: Rima Editora. 187 Rocha, C.F.D., Anjos, L.A. (2007): Feeding ecology of a nocturnal invasive alien lizard 188 species, Hemidactylus mabouia Moreau de Jonnès, 1818 (Gekkonidae), living in an 189 outcrop rocky area in southeastern Brazil. Brazilian Journal of Biology 67: 485-491. 190 Rocha, C.F.D., Anjos, L.A., Bergallo, H.G. (2011): Conquering Brazil: the invasion by 191 the exotic gekkonid lizard Hemidactylus mabouia (Squamata) in Brazilian natural 192 environments. Zoologia 28: 747-754. 193 Rose,W.. (1950): The Reptiles and Amphibians of South Africa: General Characteristics 194 of Reptiles. The Standard Press Ltd. 195 Silva, L., Land, L., Luengo, L.J.L.R. (2008). Flora e Fauna Terrestre Invasora na 196 Macaronésia. TOP 100 nos Açores, Madeira e Canárias. ARENA, Ponta Delgada, no 197 âmbito do programa INTERREG III B – BIONATURA (2007-2008). Thesis.. 198 Telles, F.B.S., Militão, C.M., Bergallo, H. G. Rocha, C.F.D. (2015): Invasion of the alien 199 gecko Hemidactylus mabouia (Moureau de Jonnès, 1818) in natural habitat at Praia do complex (Gekkonidae, Sauria). Miscellaneous N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y mabouia-brookii 200 Sul Biological Reserve, Ilha Grande, RL. Brazil. Brazilian Journal of Biology. 201 Vanzolini, P.E. (1968): Lagartos Brasileiros da Familia Gekkonidae (Sauria). Arquivos 202 de Zoologia 17: 1-84. 9 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Vanzolini, P.E. (1978): On South American Hemidactylus (Sauria, Gekkonidae). Papéis 204 Avulsos de Zoologia 31: 307-343. 205 Vanzolini, P.E., Ramos-Costa, A.M.M., Vitt, L.J. (1980). Répteis das Caatingas. Rio de 206 Janeiro: Anais da Academia Brasileira de Ciências. o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 203 207 208 209 210 211 212 213 214 215 216 217 218 219 220 Table and Figure captions 221 Table 1. Categories of habitat degradation recorded in five restinga habitats along the 223 Espírito Santo state in Souheastern Brazil. N 222 224 225 Table 2. Number of adult individuals of Hemidactylus mabouia and eggs recorded in 226 five sandy coastal plains areas (Praia das Neves, Paulo Cesar Vinha State Park, 227 Comboios Biological Reserve, Conceição da Barra Environmental Protection Area and 10 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 228 Itaúnas State Park) along Southeastern of Espírito Santo State Brazil, including 229 vegetation type and microhabitats used 230 Figure 1. Frequency of disturbances recorded in each Restinga area studied in coastal 232 Espírito Santo State. (A) Praia das Neves; (B) Paulo Cesar Vinha State Park; (C) 233 Comboios Biological Reserve; (D) Conceição da Barra Environmental Protection Area; 234 (E) Itaúnas State Park. Legend: (RV) Removing of vegetation; (TV) Trampling of 235 vegetation; (ER) Establishment of residences; (VT) Vehicular traffic; (EV) Exotic 236 vegetation; (RS) Replacement of substrate; (TD) Trash deposition; (BV) Burst 237 vegetation; (TR) Trail/road/street. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 231 238 11 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 Table 1. Categories of habitat degradation recorded in five restinga habitats along the Espírito Santo state in Souheastern Brazil. Removal of vegetation Trampling od vegetation for beach access Establishment of residences Vehicular traffic on the vegetation or dunes Exotic vegetation (e.g. grass, Eucalyptus spp, among others) Replacement of the original substrate by others (e.g. clay, gravel) Trash deposition Burnt of vegetation Trail/road/street o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y RV TV ER VT EV RS TD BV TR 239 240 241 Table 2. Number of adult individuals of Hemidactylus mabouia and eggs recorded in 242 five sandy coastal plains areas (Praia das Neves, Paulo Cesar Vinha State Park, 243 Comboios Biological Reserve, Conceição da Barra Environmental Protection Area and 244 Itaúnas State Park) along Southeastern of Espírito Santo State Brazil, including 245 vegetation type and microhabitats used . Number of individuals Restinga of Hemidactylus Eggs/Hatched eggs Vegetation Type Microhabitat mabouia recorded 15 4 HP/FR/CR/OS PEPCV 0 0 - - Comboios 0 0 - - APA C. Barra 29 2 OS UT/UB/CT Itaúnas 1 0 OS UB N Praia das Neves UT/SD/TT/UT/UF/BR 246 Legend: (APA C. Barra) Conceição da Barra Environmental Protection Area; (PEPCV) 247 Paulo Cesar Vinha State Park; [Vegatation type]: (HP) halophilous-psammofilous 248 creeper vegetation (OS) open shrubby; (CR) closed rear; (FR) forest. [Microhabitats]: 12 Citation as online first paper: North-western Journal of Zoology (on-first): art.152505 249 (UB); under bush (UT) under trash; (SD) sand; (TT) tree trunk; (UT) under fallen trunk; 250 (UF) under leaf litter (BR) bromeliad (CT) cactaceae. o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y 251 252 N 253 13