UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” Instituto de Biociências Câmpus do Litoral Paulista Natan Gonçalo dos Santos Anjos LAND GASTROPODS ALONG AN ALTITUDINAL GRADIENT ON THE COAST OF SÃO PAULO, BRAZIL SÃO VICENTE 2024 2 UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” Instituto de Biociências Câmpus do Litoral Paulista NATAN GONÇALO DOS SANTOS ANJOS LAND GASTROPODS ALONG AN ALTITUDINAL GRADIENT ON THE COAST OF SÃO PAULO, BRAZIL Trabalho de Conclusão de Curso apresentado como requisito parcial para obtenção do título de bacharel em Ciências Biológicas – Habilitação em Gerenciamento Costeiro – pela Universidade Estadual Paulista “Júlio de Mesquita Filho”. Orientador: Profº Dr. Marcos Ricardo Bornschein SÃO VICENTE 2024 3 Resumo: Fatores ambientais afetam como as espécies se espalham pelo globo. A regra de Rapoport dita que um maior número de espécies é encontrado próximo ao Equador, diminuindo em direção aos polos, e o mesmo pode ser dito, de uma altitude menor, para uma maior. Gastrópodes terrestres são o grupo animal com a maior taxa de extinção, e um dos grupos que podem seguir esta regra. Os gastrópodes terrestres da Serra do Mar, coberta pela Floresta Atlântica, são subestudados; este trabalho busca descrever as comunidades de gastrópodes terrestres de duas áreas protegidas (Parque Estadual da Serra do Mar e Parque Natural Municipal Nascentes de Paranapiacaba) e saber se eles seguem a regra de Rapoport altitudinal. Amostramos quatro pontos em diferentes altitudes, duas em cada área. Coletamos serapilheira e fizemos busca ativa de conchas e indivíduos vivos. Calculamos índices de diversidade α e β, e de equitabilidade. Nós encontramos 1559 indivíduos de 40 espécies; não houve muita mudança de riqueza de espécies em relação à altitude. A diversidade β foi principalmente explicada pelo turnover de espécies. As comunidades de gastrópodes terrestres do Parque Estadual da Serra do Mar e do Parque Natural Municipal Nascentes de Paranapiacaba não seguem a regra de Rapoport altitudinal. Palavras-chave: Diversidade, ecologia, comunidades, caracol, Paranapiacaba, Serra do Mar, Floresta Atlântica 5 Abstract: Environmental factors affect how species are scattered across the globe. Rapoport’s rule states that a greater number of species are found near the Equator, diminishing in direction to the Poles, and the same can be said, from a lower altitude, to a higher one. Land gastropods are the animal group with the highest extinction rate, and one of the groups that can fit under this rule. The land gastropods of Serra do Mar, covered by the Atlantic Rainforest, are understudied; this work seeks to describe the land gastropod communities of two protected areas (Parque Estadual da Serra do Mar and Parque Natural Municipal Nascentes de Paranapiacaba), and to know if they follow altitudinal Rapoport’s rule. We sampled at four points in different altitudes, two on each area. We collected leaf litter and did active search of shells and living individuals. We calculated α-diversity, evenness and β-diversity indices. We found 1559 individuals of 40 species; there was not much change in species richness with altitude, changes in α- diversity also did not change with altitude. β-diversity was mainly explained by species turnover. The land gastropod communities of Parque Estadual da Serra do Mar and Parque Natural Municipal Nascentes de Paranapiacaba do not follow altitudinal Rapoport’s rule. Keywords: Diversity, ecology, communities, land snail, Paranapiacaba, Serra do Mar, Atlantic Rainforest 6 Land gastropods along an altitudinal gradient on the coast of São Paulo, Brazil1 Natan Gonçalo dos Santos Anjos*; Marcos Ricardo Bornschein * corresponding author: natan.gs.anjos@unesp.br ABSTRACT Environmental factors affect how species are scattered across the globe. Raapoport’s rule states that a greater number of species are found near the Equator, diminishing in direction to the Poles, and the same can be said, from a lower altitude, to a higher one. Land gastropods are the animal group with the highest extinction rate, and one of the groups that can fit under this rule. The land gastropods of Serra do Mar, covered by the Atlantic Rainforest, are understudied; this work seeks to describe the land gastropod communities of two protected areas (Parque Estadual da Serra do Mar and Parque Natural Municipal Nascentes de Paranapiacaba), and to know if they follow altitudinal Rapoport’s rule. We sampled at four points in different altitudes, two on each area. We collected leaf litter and did active search of shells and living individuals. We calculated α-diversity, evenness and β-diversity indices. We found 1559 individuals of 40 species; there was not much change in species richness with altitude, changes in α-diversity also did not change with altitude. β-diversity was mainly explained by species turnover. The land gastropod communities of Parque Estadual da Serra do Mar and Parque Natural Municipal Nascentes de Paranapiacaba do not follow altitudinal Rapoport’s rule. KEYWORDS: Diversity, ecology, communities, land snail, Paranapiacaba, Serra do Mar, Atlantic Rainforest INTRODUCTION The way organisms and species are scattered across the globe depends on the environmental factors that affect them, such as changes in temperature 1 O manuscrito foi formatado segundo a revista: Malacologia 7 or precipitation along an altitudinal gradient (Walsh 1979; Pellegatti & Galvani). Eduardo H. Rapoport (Rapoport 1975 apud Stevens 1989) proposed that the distribution of animal species across the globe is uneven, with a greater amount of species found at the Equator, diminishing with increasing latitude, reaching its lowest values at the poles; what became known as Rapoport’s rule. This rule was adapted and expanded to cover changes in altitude, in addition to in latitude (Stevens 1992). Rapoport’s rule may or may not affect different groups of organisms, and when it does affect them, the results may vary in scale, in terrestrial invertebrates, peaks of abundance and species richness are sometimes expected (Olson 1994). Land snails and slugs are the only molluscs that can live outside water and not depend on being submerged or under splash. Because of their high sensitivity to the surrounding environment, coupled with their need of high humidity, they are severely threatened, being the animal group with the highest extinction rate, and the taxonomic group with the highest number of documented extinctions, in addition to the problem, Brazilian malacofauna is severely understudied; in Brazil, there are 748 known species of land snails (Lydeard et al. 2004; Salvador 2019; Salvador et al. 2024). The Atlantic Rainforest is a biome found on the Eastern Coast of Brazil, which used to cover the coastal areas from Rio Grande do Norte to Rio Grande do Sul, and most of São Paulo, Paraná, and Santa Catarina states. Today, only 11,73% of its original coverage remains, mostly in fragments with less than 0,5 km² (Ribeiro et al. 2009). The coast of São Paulo state has the largest contiguous strip of protected Atlantic Rainforest, mainly inside the Parque Estadual da Serra do Mar (PESM); with other protected areas nearby: (ex.:Parque Estadual do Xixová-Japuí, Parque Estadual da Restinga de Bertioga). This work seeks to study the land gastropod communities of Parque Estadual da Serra do Mar and Parque Natural Municipal das Nascentes de Paranapiacaba, and to test the application of elevational Rapoport’s rule to it. MATERIAL AND METHOD The work was done on the centre-east part of the Serra do Mar, on four points in four different altitudes: the upper two at Parque Natural Municipal 8 Nascentes de Paranapiacaba, and the lower two at Parque Estadual da Serra do Mar – Núcleo Itutinga-Pilões. We sampled between March and April 2023. Sampling was always done by at least two people trained in gastropod- collecting. Study area Parque Natural Municipal Nascentes de Paranapiacaba (Paranapiacaba Headwaters Natural Municipal Park; PNMNP) is a conservation unit on the municipality of Santo André, São Paulo, Brazil. It is home to over 300 vascular plant species, in 47 families and 103 genera, 27 of them being threatened and 9 are exotic (Santo André 2015). Its phytophysiognomy is dense ombrophilous forest, montane and high-montane, in different regeneration states, ranging from primary succession, restricted to two areas, to advanced secondary succession (Santo André 2015). Parque Estadual da Serra do Mar (Serra do Mar State Park; PESM) is a state-administered conservation unit spanning over 20 municipalities. We sampled on the Itutinga-Pilões nucleus, near its Guariúma base, that is located on the municipality of Praia Grande, São Paulo, Brazil. Over 500 plant species can be found in it, 61 of them are threatened; exotic species are usually fructiferous or ornamental species, tied to human occupation, sometimes being a common sight (Instituto Florestal 2008). PESM also harbours over 600 species of terrestrial vertebrates (Instituto Florestal 2008). We sampled on four points (Figure 1), two on each locality. At PNMNP, we sampled at 1185 m (point H) and also at a lower altitude (point MH). At PESM, we sampled at 351 m (point ML) and at 70 m (point L). Points ML, MH and H are covered by montane dense ombrophilous forest, while point L is covered by lowlands dense ombrophilous forest (Instituto Florestal 2008; Santo André 2015). Sampling methodology We sampled using two methods: litter leaf collection and active search. For the leaf litter collection, we collected all the leaf litter of 15 50 cm x 50 cm plots using a square, every two metres, along a 30 m tape measure, starting from the 0th metre. During the active search, we looked for shells and living 9 individuals, on three 36 m² plots, alongside a 30 m tape measure, for half an hour, in pairs, from the 10th metre. We searched through micro-habitats (ex.: below leaves, inside bromeliads), up to 2m in height. At the laboratory, we searched for living individuals and shells through the leaf litter; then the leaf litter was dried, sifted, and we looked for micromollusc shells. The individuals found were euthanised in water, and conserved in alcohol 70%, while the shells were preserved dry. From each sampled place, we measured the soil pH (with SONDATERRA PH-2500), variation of air humidity and temperature (with a digital thermohygrometer) during sampling. We took the weather conditions (ex.: rainfall and wind) and descriptions of the environment, including soil covering, epiphyte presence, ground covering, and epiphyte bromeliads. Geographic coördinates of initial sampling points were taken with an Etrex 10 GPS. Species identification Taxonomic ordering followed Bouchet et al. (2017), while species are according to MolluscaBase (2023). Data analysis We used the software R (R Core Team 2024) to calculate rthe diversity analyses. To analyse α-diversity, we used Simpson (D) and Shannon (H’) indices, calculated with the library vegan (Oksanen et al. 2024). We used Sørensen’s β index (βSOR) for β-diversity analysis, calculated with the library betapart (Baselga et al. 2023). We also calculated the equitability using Pielou’s index (J). RESULTS Environmental data We covered 1115 metres of altitude (Table 1), from 70 m at the lowest height to 1185 m at the highest. Soil pH was always slightly acidic, ranging from 6,4 to 6,8 (Table 2). For logistic reasons, we did litter leaf collection and active search on different dates on Paranapiacaba. We collected the leaf litter of the highest point on the 1st of March, alongside the first two plots of active search, on the 20th, we finished the active search of the highest point, and collected the leaf 10 litter of point MH, and finally on the 25th, we did the active search on point MH. The litter leaf collection and active search of the respective heights at PESM Itutinga-Pilões was done on the same day. The last sampling occurred a month and 8 days after the autumnal aequinox. Abundance We found 51 living individuals (21 by active search and 30 by leaf litter collection) and 1508 shells (5 by active search and 1503 by leaf litter collection); giving a total of 1559 gastropods (Table 3). The most abundant families were Helicinidae, Charopidae and Scolodontidae. The most abundant species was Alcadia cf. iheringi Wagner, 1911, with 632 individuals. The most abundant family found trough active search was Simpulopsidae. The most abundant species were Simpulopsis sp.1 and cf. Scolodontidae sp.15. The most abundant family found by litter leaf collection was Helicinidae. The most abundant species were Alcadia cf. iheringi, Radiodiscus sp.2 and Radiodiscus sp.3 (Fig. 2). At point L, the most abundant species was Radiodiscus sp.1. At point ML, the most abundant species was Scolodontidae sp.7. At point MH, the most abundant species was Radiodiscus sp.2. At point H, the most abundant species was Alcadia cf. iheringi, accounting near two thirds of the collected individuals. Richness We have found 40 species, included in 10 families. Only seven species were found by active search (Scolodontidae sp.10, cf. Scolodontidae sp.15, Alcadia cf. iheringi, Simpulopsis sp.1, Euconulidae sp., cf. Lilloiconcha sp.1, cf. Cystopeltidae sp.5), belonging to five families. By litter leaf collection, we found 39 species, with Lilloiconcha sp.1 being the only absence of the total species on the present study. We found a richness of 18 on the highest point. At point L we found 21 species. We encountered 20 species at point MH, but only 10 at point ML. The most speciose family was Scolodontidae, with 15 species, but only 2 genera were identified, with 12 species not assigned to any (table 3). The genus with the greatest species richness was Radiodiscus Pilsbry, 1906, with four species. 11 Diversity Alpha-diversity was at its highest at point ML in both Shannon and Simpson indices (H’=2,4317; D=0,8783; Table 4). Individuals of Alcadia cf. iheringi were responsible for near two thirds of point H’s abundance, to avoid skewing and biasing the data, we decided to calculate point H’s α-diversity indices with and without A. cf. iheringi (with: H’=1,3203; D=0,5416; J=0,4568; without: H’=2,0013; D=0,8073; J=0,7064). Overall Sørensen β-diversity was 0,6723. Pairwise differences consistently had much higher species turnover component in comparison to the nestedness component, except for points ML-MH (βSNE=0,2333; βSIM=0,3000). DISCUSSION Soil pH did not show much variation with altitude, being slightly acidic, around 6,5. It also did not show an increasing or decreasing trend. The vegetation had suffered anthropic impact before the study area got turned into a conservation unit (Instituto Florestal 2008; Santo André 2015). We have found 40 species. Perez and Hausdorf (2022) have found 80 species in Ecuador, but only 510 individuals. Our results are closer to the range of 21-33 species of previous studies done on (Southern) South America (Santos & Monteiro 2001; Oroño et al. 2007; Miranda & Cuezzo 2010; Nunes & Santos 2012). The most abundant species was Alcadia cf. iheringi, with 632 individuals (Fig. 2; 40% of all individuals), 601 of them at point H; Helicinidae was also the most abundant family, with a single species. Charopidae and Scolodontidae were the second and third most abundant families, with respectively 330 and 306 individuals. In Southern South America, Charopidae seems to be the most dominant family, while in Northern South America, Scolodontidae seems to dominate (Oroño et al. 2007). If the high abundance of A. cf. iheringi were caused by a disturb event (like a fallen tree or an abnormal concentration of leaves on the ground), then the current study fits into the expected pattern, if not, the mountaintops of Paranapiacaba might have a unique community profile; either case could only be demonstrated if the area were to be sampled again. Differently from Leme and Indrusiak (1990), we did not find any specimens of Megalobulimus parafragilior Leme & Indrusiak, 1990 nor of Megalobulimus fragilior (Ihering, 1901), if they are actually distinct species. Helicodiscus 12 parallelus (Say, 1921) is the same species as H. theresa Thiele, 1927 (Silva et al. 2020). Two species, H. parallelus and Deroceras laeve (Müller, 1774), are nonnative to Brazil. H. parallelus has been known to occur in Brazil for nearly a century, first thought to be a native species, although its invasive potential is unclear, and the species may have become nativized. D. laeve is an agricultural pest (Landal et al. 2019; Farias et al. 2023) and known to be a host of parasitic worms (e.g.: Maurer et al. 2002). Values of α-diversity given by Shannon’s index were similar to the ones found by Oroño et al. (2007), and by Miranda and Cuezzo (2010). The diversity and evenness indices showed a great decline at point H (Table 4), which disappeared if the indices were calculated after removing one outlier species; specially Simpson’s and Pielou’s indices. The closeness of species richness between each sampling point’s communities and the absence of a clear trend on diversity, does not corroborate the application of elevational Rapoport’s rule, as proposed by Stevens (1989, 1992), to the gastropods of PNMNP and PESM. Sørensen’s β-diversity index (Fig. 3) indicates that pair-to-pair community changes were more influenced by species turnover, with Simpson’s dissimilarity index values being consistently higher than the values of the nestedness component. Nestedness was higher than 0,2 between points ML-L and ML-MH; the nestedness component was 0,1714 between points ML-H, being lower than 0,05 on all other pairs. This means that the changes along altitude are more influenced by changes in species presence, than by changes in species richness. The higher values of nestedness involving point ML are probably related to the fact that it has the lowest species richness between all points. CONCLUSION The gastropods of PESM and PNMNP do not exhibit a distribution pattern in relation altitude. We recommend that more studies be made on the status of H. parallelus, to assess if it has been “nativized”, and the extent to which it can be found. Furthermore, we urge that more research be done on land gastropods of the Atlantic Rainforest, mainly descriptive and biogeographic works. ACKNOWLEDGEMENTS 13 This work was conducted with permission from SISBio, licence number 85923-1. Larissa Teixeira gave assistance in designing the study, helped with fieldwork and looking for shells in dried leaf litter. Bárbara Amaral, Gabriel Alves, Maria Fernanda Rivas, and Gustavo Adati helped with fieldwork. Katarina Adriélly A. Dantas, Bárbara Amaral, and Gabriel Souza helped look for individuals and shells in wet leaf litter. CITED LITERATURE Baselga, A., D. Orme, S. Villeger, J. de Bortoli, F. Leprieur, M. Logez, S. Martínez-Santalla, R. Martin-Devasa, C. Gomez-Rodríguez, R. M. 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Cabridge University Press, Cambridge, United Kingdom, pp. 17 TABLES TABLE 1: Point coördinates and fieldwork weather condition. Locality Weather Point Start/End time Reference Coördinates Date Paranapiacaba Clear sky H 7:10/11:00 23°46’43” S 46°17’14” W 2023 III- 01 7:18/8:23 2023- III- 20 Clear sky MH 12:27/12:00 23°45’52” S 46°17’04” W 9:56/11:08 2023-III- 25 Guariúma Clear sky L 10:20/12:00 24°00’37” S 46°34’06” W 2023- III- 30 Overcast ML 9:00/11:13 24°00’10” S 46°34’18” W 2023-IV- 28 TABLE 2: Soil pH, air humidity, temperature, altitude, and presence of epiphytes at each point. Locality pH Humidity Temperature (°C) Epiphytes Point Altitude Paranapiacaba 6,7 53% – 76% 25,5 – 28,7 Present H 1185 m 6,4 57% – 66% 22,7 – 24,3 Present MH 910 m Guariúma 6,8 53% – 76% 25,6 – 30,2 Present L 70 m 6,7 51% – 70% 20,1 – 24,9 Present ML 351 m TABLE 3: Land gastropod abundance: total, by point, and by species. Species Point H Point MH Point ML Point L Total Shells Shells Shells Shells Scolodontidae cf. Happiella sp.1 0 0 1 1 0 0 0 0 2 cf. Happiella sp.2 5 4 0 0 0 0 0 0 9 Miradiscops sp.1 22 0 7 1 1 0 47 0 78 Scolodontidae sp.4 6 0 9 0 6 0 0 0 21 Scolodontidae sp.5 0 0 10 0 0 0 14 0 24 Scolodontidae sp.6 0 0 4 0 0 0 3 0 7 Scolodontidae sp.7 1 0 21 0 44 0 25 0 91 Scolodontidae sp.8 0 0 0 0 0 0 3 0 3 Scolodontidae sp.9 0 0 0 0 4 0 0 0 4 Scolodontidae sp.10 0 0 0 0 0 0 4 0 4 Scolodontidae sp.11 27 0 0 0 0 0 0 0 27 19 cf. Scolodontidae sp.12 0 0 6 0 0 0 15 0 21 cf. Scolodontidae sp.13 0 0 3 0 2 0 0 0 5 cf. Scolodontidae sp.14 0 0 0 0 0 0 4 0 4 cf. Scolodontidae sp.15 0 0 0 0 0 0 1 5 6 Streptaxidae cf. Streptaxidae sp.1 0 0 3 0 0 0 0 0 3 Charopidae Radiodiscus sp.1 0 0 31 0 0 0 70 0 101 Radiodiscus sp.2 43 0 65 0 2 0 0 0 110 Radiodiscus sp.3 61 0 34 0 16 0 1 0 112 Radiodiscus sp.4 2 0 1 0 0 0 0 0 3 Rotadiscus sp.1 0 0 0 0 0 0 1 0 1 Charopidae sp.6 0 0 0 0 0 0 3 0 3 Cystopeltidae cf. Zilchogyra sp.1 0 0 1 0 0 0 0 0 1 cf. Zilchogyra sp.2 0 0 15 0 0 0 0 0 15 cf. Zilchogyra sp.3 1 0 0 0 0 0 0 0 1 20 cf. Zilchogyra sp.4 0 0 0 0 39 0 14 0 53 cf. Cystopeltidae sp.5 106 0 0 0 0 0 0 0 106 cf. Lilloiconcha sp.1 0 0 0 0 0 0 0 1 1 Helicodiscidae Helicodiscus parallelus 0 0 0 0 2 0 18 0 20 Helicinidae Alcadia cf. iheringi 588 13 3 0 18 0 11 1 634 Euconulidae Euconulidae sp.1 4 0 0 0 0 0 0 0 4 Euconulidae sp.2 3 2 0 0 0 0 0 0 5 Euconulidae sp.3 2 0 0 0 0 0 0 0 2 Agriolimacidae Deroceras laeve 0 1 0 0 0 0 0 0 1 Simpulopsidae Simpulopsis sp.1 9 2 10 5 0 0 0 10 36 Simpulopsis sp.2 4 0 2 2 0 0 0 0 8 cf. Rhinus sp.1 0 0 3 0 0 0 1 0 4 21 Simpulopsidae sp.4 1 0 0 0 0 0 1 0 2 Simpulopsidae sp.5 0 0 0 0 0 0 1 0 1 Diplommatinidae Adelopoma sp.1 0 0 23 0 0 0 0 0 23 Total 910 259 134 256 1559 TABELA 4: Species richness, abundance, evenness, and α-diversity indices for each sampling point. Point S Abundance H’ D J H 18 910 1,3203 0,5416 0,4568 MH 20 259 2,4317 0,8783 0,8117 ML 10 134 1,7170 0,7716 0,7457 L 21 256 2,3486 0,8602 0,7714 FIGURES FIG. 1: Location of the four sampling points, with some nearby municipalities indicated. Point H: 1185 m. Point MH: 910 m. Point ML 351 m. Point L: 70 m. 23 FIG. 2: Total abundance of land gastropods obtained by the leaf litter collection method. FIG. 3: Graphical representation of Sørensen’s β-diversity index and its components, nestedness and species turnover, for each pair of sampling points. 24 25 26 27 28