Snakes in Urban and Peri-Urban Areas: Encounters and Challenges in the Atlantic Forest Biome, Brazil

doi:10.21203/rs.3.rs-4961003/v1

In global scenarios, the implementation of major structural works, such as highways, railroads and ports, as well as the accelerated growth of urban centers, are processes that can have an impact on local fauna and if conducted without proper planning or focus on mitigating possible interference to fauna, can lead to the destruction of habitats and consequently damage to biodiversity, which also has an impact on society. Studies on herpetofauna and the management of species that appear in urban environments are little explored on the South American continent and research on snakes in these environments has not been carried out in the region investigated. The aim of this study was to identify the occurrences of snakes in urbanized areas of two municipalities in the Atlantic Forest biome, to learn about the spatial distribution and final destination of these animals. Our results found 25 species of snakes divided between the families Boidae (3 sp.), Colubridae (7 sp.), Dipsadidae (12 sp.) Typhlopidae (1 sp.) Viperidae (2 sp.) that circulated in urban and peri-urban areas and were identified using data obtained from the electronic system of the state fauna management agency and additionally from a herpetological collection of the local university, which presented a panorama of the return of animals to the wild as well as revealing animals victimized by trampling in the urbanized stretches. The final destinations of snakes that have appeared in urban areas are still poorly explained because most of the species rescued, despite having been relocated, had poorly detailed information on the management forms, which need to be better documented, from the level of species identification, as well as the final destination of the relocation, for more efficient management of urban wildlife, aiding in the process of conserving species that appear in cities.

Environment

Urban Wildlife

Wildlife relocation

Ophidians

Conflicts between snakes and humans have become an increasing concern worldwide, especially in regions with high species diversity and abundance (Hauptfleisch, Sikongo & Theart, 2020; Lettoof et al., 2023). The fragmentation of natural habitats, often resulting from the expansion of urban centers, exacerbates these conflicts (McKinney, 2002). The expansion of urban areas, necessary to accommodate population growth, presents additional challenges for species such as reptiles, which must adapt to environments with noise, artificial lights, temperature changes, and altered hydrological characteristics. However, these built environments can also offer new habitat options (French et al., 2018), which in turn may lead to incidental encounters and conflicts with the human population (Parkin et al., 2021; Teixeira et al., 2016).

Interactions between snakes and urban populations often result in the persecution and killing of these animals (Balakrishnan, 2010; França; Germano; França, 2012; Hauptfleisch, Sikongo & Theart,2020) or in or snakebite accidents,, which are considered by the World Health Organization to be neglected neotropical diseases (Chippaux,2017). On the other hand, when people spot snakes or other reptiles, they can also call on government agencies, such as the Forest Guard (Parkin et al., 2021), the Environmental Police (Negromonte et al., 2021; Teixeira et al.,2016) or Wild Animal Screening Centers (Bentes, 2013; Viana, 2014), to remove and relocate these animals.

Urbanization, accompanied by the construction of major infrastructure projects such as highways, railways, and ports in areas of high biodiversity like the Atlantic Forest biome, presents a serious challenge to the conservation of local fauna (Güneralp et al., 2021). These land-use changes not only fragment habitats but also create new interfaces of contact between humans and wildlife, increasing the likelihood of unwanted encounters (Bloomfield et al., 2020). If undertaken without adequate planning and the implementation of mitigation measures, these activities can lead to environmental degradation and biodiversity loss, with significant impacts on both fauna and human communities (McKinney, 2002; Balakrishnan, 2010; Hauptfleisch, Sikongo & Theart, 2020).

Brazil, with one of the most diverse reptile faunas in the world, is home to 856 species, distributed among the orders Testudines, Crocodylia, and Squamata (Guedes, Entiauspe-Neto & Costa, 2023; Uetz et al., 2022). However, despite this rich biodiversity, studies on the presence and management of snakes in urban and peri-urban areas are still limited (França & França, 2019). Previous research on snakes in Brazil has focused primarily on rural contexts or conservation areas, with few studies addressing the specific challenges that arise in urban zones (Carvalho & Nogueira, 1998; França et al., 2012). Additionally, there is a lack of data on the occurrence of snakes in urban areas in the southern region of Bahia, where a significant portion of the Atlantic Forest biome is located.

The Atlantic Forest, one of the most biodiverse and threatened biomes on the planet, has been intensely impacted by human activities, particularly by urban and agricultural expansion (Joly, Metzger, & Tabarelli, 2014). The cities of Itabuna and Ilhéus, located in southern Bahia, exemplify these processes, as they are situated in a region recognized as a biodiversity hotspot. Both cities have experienced accelerated urban growth and the implementation of large-scale infrastructure projects, such as a gas pipeline (SEINFRA, 2015), a new state highway (SEINFRA, 2023), the South Port Project (SEINFRA, 2021), and the start of work on the West-East Integration Railway - FIOL (ANTT, 2023). Such interventions, if not carefully managed, can lead to the loss of critical habitats and the displacement of species, increasing the likelihood of encounters with the urban population and resulting in conflicts that need to be managed with effective public policies (Hauptfleisch, Sikongo & Theart, 2020; McKinney, 2002).

In addition to scientific knowledge about wildlife in urban environments, it is important to pay attention to the legal responsibilities for wildlife management at a national level. The Brazilian Constitution states that the protection of wild fauna must be carried out by the public authorities (BRASIL, 1988). In this respect, environmental and public safety agencies at the federal, state and municipal levels make efforts and act to rescue and dispose of wild animals that appear in urban areas, including snakes, sending them for release or to Wild Animal Screening Centers (CETAS) (Bentes, 2013; Silva; Leal, 2020; Negromonte et al., 2021; Viana 2014) or, in the event of death, to herpetological collections (Costa et al, 2010).

However, the occurrence and fate of snakes in urban areas remain poorly documented, especially in the southern region of Bahia. The lack of studies limits the formulation of effective public policies for biodiversity conservation in urbanized areas (Negromonte et al., 2021; Teixeira et al., 2016). In this context, this study aims to identify the occurrence of snakes in urban and peri-urban areas of two municipalities in southern Bahia, located in the Atlantic Forest biome, and to analyze their spatial distribution and final destination. This research seeks to fill gaps in the knowledge about the presence and management of snakes in urban environments, contributing to the development of more effective strategies for the conservation and management of wildlife in urbanized areas.

3.1 Location and general description of the study área

This study was conducted in the urban and peri-urban areas of the municipalities of Itabuna and Ilhéus. Both municipalities are located in the Litoral Sul da Bahia identity territory (SEI Bahia, 2024). With a territory of

401.028 km², Itabuna has a population of 186,708 inhabitants and an average of 465.57 per km2 (IBGE, 2024).

Ilhéus has a larger territory, with 1,588.555 km² and a resident population of 178,649 inhabitants with an average of 112.46 inhabitants per km2 (Fig. 1).

Ilhéus and Itabuna are categorized as cities with a Tropical Forest climate (Af) by Koppen (1931), and have an average monthly rainfall of over 60 mm and an annual rainfall of over 1,500 mm. Summers are long and hot, with temperatures above 22ºC. Both municipalities are part of the Atlantic Forest Biome (IBGE, 2024). The urban area of Itabuna is bordered by the Cachoeira River along its entire length, and its surroundings are made up of cocoa agroforestry (cabrucas), pasture/cabruca transition vegetation and pastures (Requião; Espirito-Santo, 2022) with no conservation units set up by the government. The urban area of the municipality of Ilhéus stands out for being located on an estuary formed by the Cachoeira, Almada, Santana and Fundão rivers, with extensive coastline, mangroves and sandbanks (Oliveira; Cunha, 2007), as well as having protected areas set up by the government, including two fully protected Conservation Units (CU) - Boa Esperança Municipal Park and Ponta da Tulha State Park - PEPT (GEOBAHIA, 2024). To the north of its boundaries, it has territory included in the Environmental Protection Area - APA Lagoa Encantada/Rio Almada - a Conservation Unit for sustainable use (INEMA, 2024).

3.2 Data collection

Data on snake occurrences in urban stretches was obtained from two sources: The Electronic Information System (SEI) of the Institute of the Environment and Water Resources - INEMA as the main source of information and the Herpetological Collection: Zoology Museum of the State University of Santa Cruz - MZUESC, as a source of complementary data.

3.2.1 Electronic Information System - SEI/ INEMA

Complementary Law 140/2011 (Brasil, 2011) gave the states of the union responsibility for implementing public policies aimed at wildlife management. In the state of Bahia, the Institute of the Environment and Water Resources (INEMA) is the body responsible for implementing public environmental policy, including the management and disposal of wildlife, which is outlined in internal ordinances that help technicians make decisions regarding the management and final disposal of wildlife. SEI was implemented in the public bodies of the state of Bahia in March 2017 and, as of May 2018, INEMA began internal negotiations and training to implement its processes (INEMA, 2019). Requests to rescue wild animals are generated by the population or other public security entities (e.g. Environmental Police, Military Firefighters, Municipal Civil Guard) and are included in this system. Data collection was authorized by INEMA's General Directorate through SEI process no.

046.0533.2023.0003721-02. The data obtained was organized according to content analysis (Moraes, 1999) and categorization methods (Parkin et al, 2021). At this stage, the RFs and final destination sheets were checked individually and tabulated in Microsoft Excel 2013 software, according to the criteria described below:

Animal: snake, popular name and scientific name;

Municipality of occurrence: Itabuna and Ilhéus;

Location: urban and peri-urban areas;

Period of occurrence: 01/01/2019 to 31/12/2022 data available in the electronic system;

Record of occurrence: capture and non-capture, with photographs and without photographs; data with georeferencing and without georeferencing;

Destination: final destination information with georeferencing and without georeferencing, release documentation in registered areas, other situations (referral to sorting centers, death, escape, runaway);

Exclusion factors: non-snake animal; municipality not registered; area of occurrence not registered; municipality outside the study area; records in rural areas.

3.2.2 Herpetological Collection - MZUESC

Data was collected from the MZUESC herpetological collection based on the following criteria:

Animal: snake, genus and species;

Municipality of occurrence: Itabuna and Ilhéus;

Locality: urban and peri-urban area;

Period of occurrence: 2000 to 2019 (data available after filtering the areas of interest);

Exclusion factors: non-snake animal; unreferenced area or information of occurrence, municipality outside the study area; records in rural areas.

Photographic records of snakes seen in the urban and peri-urban areas of Ilhéus and Itabuna were obtained from the vouchers examined and, in order to complement the collection of species of interest to the study, photographs were kindly provided by the curator of the MZUESC collection, which are duly referenced below.

3.3 Data analysis

3.3.1 Identification of snakes

The aim of this work was to find out about the richness, abundance, distribution and destination of snake species, obtained from occurrence records in the wildlife management agency's electronic system, related to urban and peri-urban areas. The data, accompanied by photographs, enabled the taxa to be identified at genus and species level, supported by the literature which points to the viability of using photographs for comparison (Costa et al., 2021; Guedes; Entiauspe-Neto; Costa, 2023). Comparative identification was carried out by consulting specialists and up-to-date literature in relation to the data obtained from SEI/INEMA for the 2019–2022 period, and these were observed by municipality individually, where it became clear that no records of snakes in urban areas were computed for Ilhéus between 2019 and 2020.

In addition, data and specimens from the MZUESC Herpetological Collection, incorporated there between 2000 and 2019, were examined. The voucher numbers are listed in Appendix 1. In addition, the taxonomic nomenclature was checked in Uetz et al. (2022), Costa et al.(2021) and Guedes; Entiauspe-Neto; Costa, 2023 (2023) and the presence of endangered species was consulted in the Brazilian Red List (MMA,2022) and the State List of Endangered Species (SEMA,2017).

A dominance calculation was carried out based on the data obtained from the SEI system and the MZUESC collection (genus/species identified), considering the occurrences in each municipality/period and following the model adapted by Mesquita et al. (2013) (apud Abreu; Nogueira, 1989; Luiselli, 2006). The species dominance calculation was applied using the following formula:

$$\:\text{D}=\frac{number\:of\:snakes\:of\:the\:target\:species\:}{total\:number\:of\:snakes\:in\:the\:sample}x\:100$$

The calculation results are categorized as: accidental (0%-2.5%), accessory (2.5%-5%) and dominant (5%- 100%).

3.3.2 Final disposal of snakes - Ilhéus and Itabuna

The destination/translocation of snakes that passed through the municipalities studied was analyzed using the SEI/INEMA database, using a quantitative descriptive approach, where the final destination and variables related to the management of these occurrences in the period 2019–2022 were verified.

3.3.3 Landscape analysis

Snakes were checked in the landscape of the municipalities studied using the geographical coordinates available in the database. The images were created by overlaying the occurrence data (geolocation) with the land use and land cover data contained in the MapBiomas platform, and using the QGIS 3.24 software. In this analysis, it was possible to verify that of the total of 181 occurrences, 45 remained without geographic coordinates associated with the Itabuna database, reducing the total mapping and distribution in the land use table for this municipality to 136 points. The Ilhéus data showed that of the 201 occurrences, 87 points had no defined geolocation, reducing the mapping to 114 points plotted on the map.

4.1 Snake occurrences in Itabuna and Ilhéus - urban and peri-urban areas

The data revealed 211 snake specimens that were documented in Itabuna and Ilhéus using the SEI/INEMA electronic system. However, 148 records could not be identified due to the lack of photographs associated with the occurrences and were classified as "unidentified" species (N.id). In addition, 171 specimens were examined in the MZUESC collection, making a total of 382 snakes that passed through the urban and peri-urban areas of Itabuna and Ilhéus (Table 1).

Tabela 1 - Species of snakes that have passed through the urban and peri-urban areas of Itabuna and Ilhéus. Number of species sighted in Ilhéus and Itabuna from the MZUESC museum (NMz) and number of specimens from Ilhéus and Itabuna from occurrences in the SEI/INEMA system (NS). Conservation status SEMA-BA (2017) and Ministry of the Environment - MMA (2022), respectively: LC = Least Concern; VU = Vulnerable.

Tabela 2 - Evaluation of the degree of dominance applied only to the species identified (Genus and species), that passed through urban and peri-urban areas, considering the total number of occurrences in the period 2000–2022 per municipality. Number of species identified based on MZUESC (NMz) and SEI/INEMA (NS), Dominance (D).

Genus/species	ILHEUS		ITABUNA
Genus/species	(NMz/NS)	D(%)	(NMz/NS)	D(%)
Amerotyphlops brongersmianus (Vanzolini, 1976)	3	2	3	3.61
Atractus guentheri (Wucherer, 1861)	6	4	-
Boa atlantica Gonzales, Lima, Passos, Silva, 2024	8	5.33	39	46.7
Bothrops leucurus Wagler in Spix, 1824	2	1.33	7	8.43
Chironius carinatus (Linnaeus 1758)	29	19.33	4	4.82
Chironius laevicollis (Wied-Neuwied, 1824)	6	4	-
Clelia plumbea (Wied, 1820)	-	-	5	6.02
Corallus hortulana (Linnaeus, 1758)	2	1.33	1	1.20
Dipsas neuwiedi (Ihering, 1911)	3	2.67	-
Drymarchon corais (Boie, 1827)	1	0.66	1	1.20
Epicrates cenchria (Linnaeus, 1758)	11	7.34	-
Erythrolamprus miliaris (Linnaeus, 1758)	17	11.33	6	7.23
Erythrolamprus taeniogaster (Jan, 1863)	2	1.33	-
Imantodes cenchoa (Linnaeus, 1758)	2	1.33	-
Lachesis muta (Linnaeus, 1766)	10	6.67	-
Leptophis liocercus (Wied, 1824)	8	5.33	-
Oxybelis aeneus (Wagler, 1824)	1	0.66	-
Oxyrhopus guibei Hoge & Romano, 1977	3	2	-
Oxyrhopus petolarius (Linnaeus, 1758)	13	8.67	5	6.02
Palusophis bifossatus (Raddi,1820)	1	0.66	6	7.23
Philodryas olfersii (Lichtenstein, 1823)	9	6	2	2.41
Pseudoboa nigra (Duméril, Bibron & Duméril, 1854)	8	5.33	2	2.41
Siphlophis leucocephala (Laurenti, 1768)	1	0.66	-
Tantilla melanocephala (Linnaeus, 1758)	-	-	2	2.41
Xenopholis scalaris (Wucherer, 1861)	3	2	-
Total General	150		83

Legend: Dominance = accidental (0%-2.5%), accessory (2.5%-5%) and dominant (5%-100%).

4.2 Distribution of snakes in urban and peri-urban areas - Itabuna and Ilhéus

The data showed snakes distributed in various locations in the urban and peri-urban areas of the municipalities studied. Ilhéus stood out, as it revealed the appearance of snakes in different contexts, such as

animals that had been run over on stretches of road that cut through urban areas, such as BA 001 and BR 415, occurrences on the campuses of the State University of Santa Cruz - UESC and the headquarters of the Executive Commission of the Cocoa Plantation Plan - CEPLAC, as well as in villages and residential neighborhoods, unlike Itabuna, whose records were only found in residential areas and some peri-urban stretches.

4.3 Distribution of snakes: Itabuna-Bahia landscape.

In Itabuna, 181 occurrences of snakes promoted encounters with the population in 35 residential neighborhoods and the industrial center. Of the occurrences observed, 22.52% had no information on the specific neighborhood/location. Among the neighborhoods identified, the following stand out: Jaçanã, with 9.34%, Pedro Gerônimo and São Judas, with 4.94% and João Soares and Parque Verde, with 4.39% of the occurrences (Table 4).

Tabela 3 - Distribution locations of snakes that passed through the urban and peri-urban areas of Itabuna. Number of occurrences given by MZUESC (NMz) and SEI/INEMA (NS) from 2000–2022.

Locality/neighborhood	NMz/MS	Locality/neighborhood	NMz/MS
Banco Raso	1	Monte Líbano	1
Califórnia	2	Não informado	40
Castália	4	Nossa Senhora das Graças	4
Centro	5	Nova Ferradas	3
Centro Industrial	1	Nova Itabuna	3
Conceição	3	Novo Jaçanã	2
Fatima	2	Parque Verde	8
Ferradas	3	Pedro Jerônimo	9
Góes Calmon	4	Pontalzinho	2
Jaçanã	13	Santa Catarina	1
Jardim Vitória	4	Santa Inês	1
Jd. Primavera	2	Santo Antônio	1
João Soares	8	São Caetano	7
Jorge Amado	2	São Judas	9
Lomanto	7	São Pedro	7
Lot. Santa Tereza	1	São Roque	4
Mangabinha	6	Vale do Sol	2
Manoel Leão	5	Vila Anália	3
Maria Pinheiro	1
Total General	181

Below are the results of the number of occurrences compared with information on land use and land cover. The areas identified were classified as Urbanized Area (UA), Mosaic of Uses (MU) and Pasture (P) (Fig. 3 and Table 4).

Table 4 - Distribution of snakes that traveled through the urban and peri-urban areas of Itabuna according to data from land use and cover Mapbiomas. Types of use: Urbanized area (AU), Mosaic of uses (MU), Pasture (P). Occurrence of snakes in %. Database MZUESC(NMz) and SEI/INEMA (NS).

Family / Snake

Data NMz/NS

AU(%)

MU(%)

P(%)

Boidae

Boa atlantica (Gonzales, Lima, Passos, Silva, 2024)	21.32	1.47	2.20
Corallus hortulana (Linnaeus, 1758)	0.7	-	-

Colubridae

Chironius carinatus (Linnaeus 1758)	0.7	-	-
Drymarchon corais (Boie, 1827)	0.7	-	-

Family / Snake	Data NMz/NS
Family / Snake	AU(%)	MU(%)	P(%)
Palusophis bifossatus (Raddi,1820)	2.94	-	-
Tantilla melanocephala (Linnaeus, 1758)	0.7	-	-

Dipsadidae

Clelia plumbea (Wied, 1820)	0.7	-	1.48
Erythrolamprus miliaris (Linnaeus, 1758)	1.47	-	-
Oxyrhopus petolarius (Linnaeus, 1758)	1.47	-	-
Pseudoboa nigra (Duméril, Bibron & Duméril, 1854)	0.7	-	-
Thamnodynastes sp.	0.7	-	-
N. id	46.32	4.41	8.1

Typhlopidae

Amerotyphlops brongersmianus (Vanzolini, 1976)

1.47

-

Viperidae

Bothrops leucurus Wagler in Spix, 1824	0.7	0.7	0.7
Total by use (%)	80.6	6.6	12.5

Legend: N.id = Unidentified snake. AU = Areas with a significant density of buildings and roads, including areas free of buildings and infrastructure. MU = Areas of agricultural use where it was not possible to distinguish between pasture and agriculture. P = Areas of predominantly planted pasture, directly related to agricultural activity. Natural pasture areas, on the other hand, are predominantly characterized as grasslands or flooded fields, and may or may not be subject to grazing practices.

Table 4 shows that most of the snakes recorded in Itabuna do not seem to avoid the urban landscape, with the majority of the taxa confirmed as being present in urbanized areas (UA), with Boa atlantica standing out with 21.32% of appearances, having transited through other categories of land use, followed by Palusophis bifossatus with 2.94% of appearances in urban areas. The "N.id" snakes (species that were not identified by the SEI/INEMA system due to lack of photographs) also represented a high incidence in urbanized areas, with 46.32% (Figure 10).

4.4 Distribution of snakes: Ilhéus-Bahia landscape

In Ilhéus, 201 snake encounters were recorded in different areas. This includes 27 residential neighborhoods, 07 villages, and one district further away from the urban core, such as Sambaituba. In addition, there were encounters on two portions of highways, one under state jurisdiction and the other federal, which cross urbanized areas that are in the process of expansion. In addition, the incidence of these reptiles on the UESC campus and CEPLAC's regional headquarters stands out, both of which have urban infrastructure. Of all the occurrences observed, 4.48% had no information on the specific neighborhood. Among the localities identified, the following stand out: Salobrinho, with 4.97%; Nossa Senhora da Vitória, Iguape and Jardim Savóia, with 3.5%; and Olivença and Banco da Vitória, with 2.3% (Table 5).

Tabela 5 - Distribution locations of snakes that traveled through the urban and peri-urban areas of Itabuna and promoted encounters with the population. Number of occurrences given by MZUESC (NMz) and SEI/INEMA (NS) from 2002-2022.

Locality/neighborhood	NMz/ NS	Locality/neighborhood	NMz/ NS
Banco da Vitória	6	Cururupe	3
Barra	2	Esperança	4
Basílio	2	Hernani Sá	2

Boa Vista (“Pacheco”)	3	Iguape	7
Sede regional CEPLAC	1	Ilhéus II	1
Campus UESC	28	Jardim Atlântico	1
Centro	1	Jardim Savóia	7
Ceplus	2	Joia do Atlântico	1
Conquista	2	Malhado	1
Mamoan	2	Rodovia Estadual BA 001	23
Não informado	9	Rodovia Federal BR 415	43
Nelson Costa	5	Salobrinho	10
Nossa Senhora da Vitória	7	Sambaituba	1
Novo Ilhéus	1	São Miguel	2
Olivença	6	Sapetinga	2
Outeiro	1	Tapera	1
Ponta da Tulha	3	Teotônio Vilela	2
Ponta do Ramo	1	Vila Areias	3
Pontal	4	Vila Cachoeira	1
Princesa Isabel	1	Vila Juerana	1
Total	87		114
Total General	201

In relation to the highways that cross the urban and peri-urban stretches of the municipality, there were 32.8% of incidents, 11.44% of which were on the BA 001 state highway and 21.4% on the BR 415 federal highway, also known as the Jorge Amado Highway, which resulted in the snakes being run over and killed (Fig. 5).

Below are the results of the occurrences compared with the land use and land cover information. The areas identified were classified as Urbanized Area (UA), Forest Formation (FF), Mosaic of Uses (MU). Other non- vegetated areas (OANV) and Pasture (P) (Table 6).

Table 6 - Distribution of snakes that passed through the urban and peri-urban areas of Ilhéus according to Mapbiomas land use and land cover data. Types of use: Urbanized area (AU), Forest formation (FF), Mosaic of uses (MU), Other non-vegetated areas (OANV), Pasture (P). Occurrence of snakes in %. Database MZUESC(NMz) and SEI/INEMA (NS).

Taxon

Data NMz/ NS

AU(%)

FF(%)

MU(%)

OANV(%)

P(%)

Boidae

Boa atlantica Gonzales, Lima, Passos, Silva, 2024	0.88	-	1.75	-	0.88
Corallus hortulana (Linnaeus, 1758)	-	-	-	-	0.88
Epicrates cenchria (Linnaeus, 1758)	0.88	0.88	-	-	0.88
Colubridae
Chironius carinatus (Linnaeus 1758)	4.38	1.75	3.51	-	3.51
Chironius laevicollis (Wied-Neuwied, 1824)	-	-	0.88	-	1.75
Drymarchon corais (Boie, 1827)	-	-	0.88	-	-
Imantodes cenchoa (Linnaeus, 1758)	-	-	0.88	-	-
Leptophis ahaetulla (Linnaeus, 1758)	2.63	-	-	-	-
Oxybelis aeneus (Wagler, 1824)	-	-	0.88	-	-

Dipsadidae

Atractus guentheri (Wucherer, 1861)	0.88	0.88	-	-
Dipsas sp.	-	-	-	-	0.88
Dipsas neuwiedi (Ihering, 1911)	0.88	-	-	-	-
Erythrolamprus miliaris (Linnaeus, 1758)	3.51		0.88	0.88	-
Oxyrhopus guibei Hoge & Romano, 1977	-	-	0.87	-	-
Oxyrhopus petolarius (Linnaeus, 1758)	-	-	2.63	-	0.88
Philodryas olfersii (Lichtenstein, 1823)	-	-	0.87	-	-
Pseudoboa nigra (Duméril, Bibron & Duméril, 1854)	1.75	-	-	0.88	1.75
Siphlophis leucocephalus (Günther, 1863)	-	-	0.88	-	-
N. id	39.48	-	3.51	-	1.75

Typhlopidae

Amerotyphlops brongersmianus (Vanzolini, 1976)

0.88

-

Viperidae

Bothrops leucurus Wagler in Spix, 1824	-	-	0.87	-	-
Lachesis muta (Linnaeus, 1766)	1.75	2.63	0.87	-	0.88
Total by use (%)	57.9	6.14	20.16	1.76	14.04

Legend: N.id = Unidentified snake. AU = Areas with a significant density of buildings and roads, including areas free of buildings and infrastructure. FF = Atlantic Forest: Dense, Open and Mixed Ombrophilous Forest and Semi- Deciduous Seasonal Forest, Deciduous Seasonal Forest and Pioneer Tree Formation MU = Areas of agricultural use where it was not possible to distinguish between pasture and agriculture.

Table 6 shows that the majority of snakes moved through the urban landscape, with 57.9% of confirmed occurrences, with Chironius carinatus standing out, moving through most categories of land use, including forest formation, and the species Erythrolamprus miliaris, recorded in three categories of land use (Pasture, Mosaic of Uses and Urbanized Area). These species had the highest representation in urban areas in the municipality, with 4.38% and 3.51%, respectively. The "N.id" snakes (species that were not identified by the SEI/INEMA system due to lack of photographs) accounted for 39.48% of appearances in the urban landscape (Fig. 12).

4.5 Final disposal of snakes - occurrences in Itabuna and Ilhéus

The data below shows the number of occurrences related to the response of the wildlife management body

- INEMA - to snake encounters with the population and which situations occurred when these animals were spotted and called upon to resolve the conflicts (Table 7).

Table 7

The agency's response to the appearance of snakes that traveled through the urban and peri-urban areas of Itabuna and Ilhéus and promoted encounters with the population. Number of occurrences/specimens from SEI/INEMA system data (NS).
Final destination/Redemption variables	Ilhéus		Itabuna		Total
Final destination/Redemption variables	(NS)	Service status	(NS)	Service status	Total
STATE CETAS	-	-	2	CF	2
PRIVATE CETRAS	1	CF	-	-	1
Escaped after rescue	-	-	2	CNF	2
Not captured	12	CNF	18	CNF	30
Death	1	CF	7	CF	8
Release identified	-	-	18	CF	18
Release not identified	39	CF	111	CF	150
Total General	53		158		211
Caption: CETAS - Wild Animal Screening Center; CETRAS - Wild Animal Treatment Center. CF - Conflict finalized / CNF: Conflict not finalized

Of the 53 incidents recorded for the municipality of Ilhéus, 73.6% did not include information on the destination of the snakes after treatment or the specific place of release. One death was recorded, one snake was sent to the CETRAS of a private enterprise in the Ilhéus region and 22.64% of the incidents resulted in the snake not being captured. In relation to Itabuna, of the 158 records analyzed, it was found that 67.72% of the snakes were captured and returned to the wild, but without specific identification of the location, while only 11.39% of the releases were geolocated. In addition, 1.26% were sent to the State CETAS located in the municipality of Cruz das Almas - Bahia, 4.43% of the occurrences resulted in the death of the snakes and 11.39% of the snakes were not captured. It is worth noting that the status CF (conflict finalized) and CNF (conflict not finalized) are related to care, being finalized with the removal and final destination and not finalized when the snake was not captured (Table 8 and Table 9).

Tabela 8 - Response by the environmental agency to the appearance of snakes that have traveled through the urban and peri-urban areas of Itabuna and Ilhéus and identification of the snakes that have had encounters with the population and have been removed. Number of occurrences/specimens from SEI/INEMA system data (NS).

Final disposal / snake	Popular name given (NS)	Ilhéus (NS)	Itabuna (NS)	Total
STATE CETAS			2	2
Boa atlantica	Jibóia	-	2	2
PRIVATE CETRAS		1		1
Boa atlantica	Jibóia	1		1
DEATH		1	7	8
N. id	Serpente/cobra	1	5	6
Palusophis bifossatus	Jaracussu do brejo		2	2
ASAS I RELEASE			14	14
Boa atlantica	Jibóia		9	9
Clelia plumbea	Mussurana		1	1
Corallus hortulana	Suaçuboia		1	1
Drymarchon corais	Cainana		1	1
N. id	Serpente/cobra		1	1
Palusophis bifossatus	Jaracussu do brejo		1	1
RELEASE FARM. A			3	3
Boa atlantica	Jibóia		3	3
RELEASE FARM. B			1	1
Chironius carinatus	Cainana		1	1
RELEASE NOT IDENTIFIED		39	111	150
Boa atlantica	Jibóia	1	25	26

Final disposal / snake	Popular name given (NS)	Ilhéus (NS)	Itabuna (NS)	Total
Bothrops leucurus	Jararaca/Boca Podre		4	4
Chironius carinatus	Cainana		2	2
Clelia plumbea	Mussurana		4	4
N. id	Serpente/cobra	38	71	109
Oxyrhopus petolarius	Falsa coral		1	1
Palusophis bifossatus	Jaracussu do brejo		3	3
Thamnodynastes sp.	Cobra corre campo		1	1
Total Geral		41	138	179

Caption: ASAS I - Wild Animal Release Area registered by the State of Bahia; Farm. A - Release area not formalized as an ASAS; Farm. B - Release area not formalized as an ASAS.

Table 9

-Destination of identified releases. Number of occurrences/specimens from SEI/INEMA system data (NS).
Release identified	Snake origin	Final destination			Distance (Km)
Release identified	Snake origin	Barro Preto (NS)	Ilhéus (NS)	Total (NS)	Distance (Km)
ASAS I -a	Itabuna	9	-	9	25
ASAS I -b	Itabuna	5	-	5	25
FARM. A	Itabuna	-	3	3	25
FARM. B	Itabuna	1		1	35
Total		15	3	18

Caption: ASAS - Release area registered by the state; FARM. A - Release area not formalized as ASAS; FARM. B - Release area not formalized as ASAS.

According to Tables 8 and 9, of the 18 snake relocations identified, 77.8% took place in Wild Animal Release Areas (ASAS) type I, recognized by the environmental agency. Releases on rural properties not registered for this purpose accounted for 22.2% of the relocations.

Our data showed 25 species passing through the urban environments of the cities of Itabuna and Ilhéus, and the total number of species recorded is 18.25% of the known snakes in the state of Bahia (Guedes; Entiauspe- Neto; Costa, 2023), with seven species dominating the dataset, divided between the families Boidae (Boa atlantica, Epicrates cenchria), Colubridae (Chironius Carinatus), Dipsadidae (Erytrolamprus miliaris, Oxyrhopus petolarius) and Viperidae (Lachesis muta and Bothrops leucurus). The species Chironius carinatus D = 19.33, Erythrolamprus miliaris D = 11.33, Oxyrhopus petolarius D = 8.67, Epicrates cenchria D = 7.34 and Lachesis muta

D = 6.67, were dominant in the urban occurrences of Ilhéus and the species Boa atlantica D = 46.42 and Bothrops leucurus D = 8.33 in the urban occurrences of Itabuna.

In the municipality of Ilhéus, the semi-aquatic species Erytrolamprus miliaris and the terrestrial species Chironius carinatus showed the highest rates of sucking in urban and peri-urban areas. These species are not considered to be of medical importance and their physical size allows them to be easily seen by the population, unlike the Amerotyphlops brongersmianus species, which, as well as being considered a small species, is fossorial and was identified in urbanized stretches of Ilhéus, possibly in residential backyards, making it an interesting find. In Itabuna, the new species Boa atlantica (Gonzales et al.,2024), had the highest abundance of all the snakes identified in the urban areas of this study. These animals are characterized by their large size, which allows snakes to be seen more frequently (Letooff et al.,2023). In our study, B. atlantica showed an abundance of 12.1% of the total sample in urban areas and according to the distribution of the species between the states of Rio de Janeiro and Rio Grande do Norte (Gonzales et al.,2024), it showed a high number of appearances in urban and peri-urban areas in the capital of Bahia (Rodamilans et al., 2020), in the capital and metropolitan cities of Pernambuco (Negromonte et al., 2021) and in natural restinga areas (Sampaio et al.,2018). In addition to the urbanized areas in this study, this species was also identified passing through open stretches of pasture or agriculture (Table 5).

The distribution of snakes in the municipalities studied revealed that 25 species had direct encounters with the population, requiring removal and relocation, or indirect encounters, such as being run over (Balakrishnan, 2010). The snakes were found to be distributed in different categories of land use in urban and peri-urban areas, including residential neighborhoods and outlying areas of the municipalities. In Itabuna, some neighborhoods where the occurrences prevailed have native vegetation and pasture areas around them (Requião; Espirito-Santo, 2022) and the municipality of Ilhéus has a distribution of restinga fragments, mangroves and coastal stretches distributed throughout the municipality (Oliveira; Cunha, 2007).It is important to note that both municipalities are in the process of urban expansion to areas further away from the city center and these stretches of native vegetation or pasture have been giving way to the implementation of new infrastructures such as residential condominiums, for example. These factors can promote the encounter of snakes with the population in these locations, known in other countries as suburban areas (Hauptfleisch, Sikongo & Theart,2020; Mckinney,2002).

In the results presented in Ilhéus, it is important to note that the UESC campus was responsible for 13.46% of the occurrences in this municipality, where 15 species were observed circulating around the campus, but even with a low level of dominance in the sample (mostly accidental), it showed a higher diversity of species than the urban occurrences in Itabuna, which showed 13 species. This diversity in this urbanized environment may be

associated with the existence of the cabruca agroforestry system and its biodiversity of snakes (Argôlo, 2004), which is adjacent to the concrete structures of the institution.

Non-permeable structures such as two highways that cross urban and peri-urban stretches of the municipality of Ilhéus, accounted for 34.13% of the occurrences in the municipality, which resulted in being run over, a type of human action that causes snake deaths (Balakrishnan, 2010). The snakes Chironius carinatus and Lachesis muta were the most common to appear on these roads, culminating in being run over. However, unlike C. carinatus, the species Lachesis muta, which has a conservation status of VU - Vulnerable (SEMA, 2017), did not appear in direct contact with people in this investigation. This species seems to frequent more preserved vegetation environments such as primary forests and riparian forests (Marques et al., 2016), although it can eventually be recorded in secondary forests and agroforestry systems such as cacao cabruca (Argôlo, 2004) and their surroundings, such as the BA 001 and BR 415 highways, which cross some peri-urban and urban expansion areas in Ilhéus. The other snake species identified in this study (24 sp.) fall into the conservation status LC = of little concern.

Under Brazilian law, killing, chasing, hunting, catching and using specimens of wild fauna, whether native or on a migratory route, without the proper permission, license or authorization is characterized as an environmental crime (BRASIL,1998) and those who practice it can be held administratively and criminally liable, which is a major challenge for the bodies involved in the management of wild fauna, especially snakes, taking into account people's fear and aversion (Parkin et al., 2021), who may sacrifice these animals when they encounter them or suffer accidents (Carvalho; Nogueira, 1998; França; Germano; França, 2012), unlike other taxa that are pleasant to the urban population, such as bird species (Mckinney, 2002).

The numbers of occurrences and final destination of the snakes identified in this study revealed that the vast majority of specimens that appeared in the urban areas of Itabuna and Ilhéus were returned to the wild (see Table 8), certainly because they had physical characteristics that made them suitable for release, such as the absence of injuries, in accordance with current legislation (Brazil, 2014; INEMA, 2021); however, there is a need to better document the final destination of these animals. The lower number of incidents in the municipality of Ilhéus observed in the SEI/INEMA data may be under-represented due to the ostensive actions carried out by the Environmental Protection Police Company (CIPPA), which has a platoon at the municipality's headquarters. It should also be noted that INEMA's headquarters in Itabuna received a greater number of snake cases in the system. Species that have appeared in Itabuna and have the potential to cause accidents, such as Bothrops leucurus,

have been released in areas not identified by the agency and apparently are not wanted by the owners of the areas registered for official release. When observing the species that were released in ASAS, it was noted that 100% of

the snakes, such as the boids Boa atlantica, Corallus hortulana and the colubrids Drymarchon corais and Palusophis bifossatus, do not cause snakebite accidents considered to be of medical importance. It is thought that the large number of releases without identification can be justified by inferring the following hypotheses: 1. The existence of vegetation fragments outside of WSAs and close to urban areas made it possible to carry out a quick release and thus reduce the time the snake had to be confined or traveled to a registered WSA; 2. High temperatures and waiting times can decrease the life span of ectothermic animals in confined environments (e.g. transport boxes) and motivated the quicker release without destination data; 3. Fuel savings were considered in order to avoid long journeys; 4. Factors related to management have influenced the decision to release, such as the lack of trained staff, which can lead to the animal being "dumped" in unsuitable places, such as grazing areas for venomous species like cattle or horse farms (personal ob.) or even near houses, thus promoting new conflicts.

The snakes that had their destination identified were not venomous and were relocated at an average distance of 27.5 km from the municipal limits of occurrence, a much greater distance than that adopted by snake capturers in Australia, who relocate species at a distance of no more than 20 km (Shine; Koenig, 2001), with non-venomous snakes at distances of 500 m from the capture site and venomous species in more distant forest fragments (Parkin et al., 2021). In order to adopt these actions, it is necessary to know the basic identification characteristics of the species involved.

Final considerations

The SEI/INEMA electronic system databases enabled the collection and identification of snakes and the analysis of their distribution in urban and periurban zones, successfully meeting the objectives of this research. The data provided valuable insights into the environmental agency's response to snake occurrences in urban areas and the translocation processes following rescues conducted by the agency. However, 70.1% of the snakes recorded in urbanized areas could not be fully analyzed due to the absence of photographs associated with the handled animals.

Data from UESC's herpetological collection supplemented this research by providing information on other species that moved through the urbanized areas of the municipalities studied, thus filling the gap left by the limitations of the SEI/INEMA system data. This issue is consistent with findings from other studies in Brazil, which also pointed to a lack of species identification in official data (Negromonte et al., 2021; Silva & Leal, 2020; Teixeira et al., 2016; Viana, 2014). Additionally, the absence of geographical information regarding relocation sites created further gaps in understanding snake translocation in urban areas, leading to the formulation of several hypotheses on the subject.

These findings are significant for this pioneering research in the region, as they highlight the need for improvements in the environmental agency's electronic system. It is essential to propose the standardization of the format and the minimum quantity of photographs required for each record, including geographical coordinates of the rescue and relocation sites, to enhance internal management processes and provide a solid foundation for future studies.

The results also emphasized the necessity of registering new Wildlife Release Areas (ASAS) on rural properties closer to urban areas in the studied municipalities. This would improve wildlife management by reducing travel time for relocations, increasing the frequency of releases, and ensuring more accurate documentation. Such initiatives would contribute significantly to the fauna management efforts in southern Bahia.

Environmental education initiatives focused on institutions that manage snakes are crucial for minimizing conflicts and preventing accidents that could harm both people and the species appearing in urban areas. The information obtained from this study will facilitate the creation of educational materials, as it has enhanced our understanding of snake species that commonly inhabit urban environments in the region and their potential to cause accidents. This knowledge will also be instrumental in guiding decision-making regarding snake relocation.

Understanding the composition, abundance, and distribution of snakes in urbanized areas is a vital starting point for assessing how the expansion of local infrastructure might influence wildlife encounters in the urban zones of the municipalities studied. The observed abundance of Boa atlantica in this study underscores the need for further research into the ecology and behavior of this species, which is endemic to the Atlantic Forest Biome (Gonzales et al., 2024) and has demonstrated a remarkable tolerance for urbanized areas. The species richness identified in the urban stretches of this study may encourage additional research on snakes in natural areas amidst urban expansion, particularly in Ilhéus, where two fully protected conservation units—Boa Esperança Municipal Park and Ponta da Tulha State Park—are bordered by urban structures.

Acknowledgements

We would like to thank the Instituto do Meio Ambiente e Recursos Hídricos - INEMA (Institute of the Environment and Water Resources) for authorizing and making available the snake occurrence and management data in the electronic information system, as well as the Univiersidade Estadual de Santa Cruz (Santa Cruz State University) for providing access to the Zoology Museum's collection and its technical team to help identify the snakes.

Financing

The authors declare that no funds, grants or other support were received during the preparation of this manuscript

Competitive interests

The authors have no relevant financial or non-financial interests to declare.

Author contributions

All the authors contributed to the conception and design of the study. Material preparation, data collection and analysis were carried out by André Nascimento de Souza, Sofia Campiolo, Antônio Jorge Suzart Argôlo, Rafaela Candido de França and Nathalia Ribeiro Santos. The first draft of the manuscript was written by André Nascimento de Souza and all authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.

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No competing interests reported.

APPENDICES.docx

Snakes in Urban and Peri-Urban Areas: Encounters and Challenges in the Atlantic Forest Biome, Brazil

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Abstract

Figures

Introduction

Material and Methods