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Natural History of Snakes in Forests in the Manaus

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Natural History of Snakes in Forests in the Manaus M. Martins and M. E. Oliveira 1 NATURAL HIS TORY OF S NAKES IN of visually searching for snakes, ca. 1600 of FORES TS IN THE MANAUS REGION, which during time constrained search. Tempera- CENTRAL AMAZONIA, BRAZIL* ture and relative humidity in Manaus are high and the amount of annual rainfall (2075 mm/yr) is relatively small, with a long dry season (4–7 Marcio Martins mo). Of the 65 species for which information is available, 28 (42%) are primarily terrestrial, 20 Departamento de Ecologia Geral, Instituto de (30%) fossorial and/or cryptozoic, 13 (20%) Biociências, Universidade de São Paulo, Caixa arboreal, and four (6%) aquatic, although many Postal 11.461, 05422-970 São Paulo SP, species use more than one microhabitat when Brazil active. Nearly all inactive snakes were found on vegetation. In relation to time of activity, of the 62 species for which information is available 26 M . Ermelinda Oliveira species (41%) seem to be strictly diurnal, 13 (21%) strictly nocturnal, and 23 (38%) both Departamento de Parasitologia, Instituto de diurnal and nocturnal. The five prey types most Ciências Biológicas, Universidade do Amazo- commonly consumed by snakes in the Manaus nas, Av. Rodrigo Otávio 3.000, 69077-000 region are vertebrates: lizards (consumed by 58% Manaus AM, Brazil of the species), frogs (39%), mammals (23%), birds (18%), and snakes (16%). A cluster analy- _____________________________________ sis combining data on microhabitat use, diel ac- *This study is dedicated to O.R. Cunha and tivity, and diet resulted in several groups of spe- F.P. Nascimento (both now retired from Mu- cies with similar habits. All these "guilds" in- seu Goeldi, Belém) for their unparalleled con- cluded closely related species, as well as dis- tributions to the knowledge of Brazilian Ama- tantly related ones that converge in habits. These zonian snakes, including natural history, and combined results indicate that besides current the immense collection of snakes at the ecological factors (e.g., predation pressure; dif- MPEG, an invaluable source of natural his- ferential prey availability in different microhabi- tory information for years to come. tats), historical factors (phylogeny and bio- geography) may have played and important role in determining the current natural history pat- terns of this snake assemblage. A high diversity Abstract. We present natural history infor- of defensive tactics was found in the assemblage, mation on 66 species of snakes found in the and phylogeny may be a strong determinant fac- forests of the Manaus region, Central Amazo- tor for the occurrence of defensive tactics in each nia, Brazil. For each species, we provide in- species. Contradicting generalizations on the formation on size, color pattern, habitat and timing and length of reproductive season in microhabitat, feeding habits, reproduction, and Amazonian snakes, juvenile recruitment seems to defense. We also include a partial summary of occur mainly during the rainy season in most the information available in the literature for species from the Manaus region, although some Amazonian localities. Our results are based on species seem to breed throughout the year. This nearly 800 captures or sightings of snakes may be a consequence of the prolonged dry sea- made from 1990–1995 at localities around son that occurs in the region, during which time Manaus, mostly at a primary forest reserve some resources occur in limited supplies. 25 km north of Manaus. Field data at this reserve were obtained during over 2600 man-h M. Martins and M. E. Oliveira 2 Key Words. Serpentes; Amazonia; M icro- "guildas" incluem espécies filogeneticamente habitat; Feeding; Defense; Reproduction. próximas, bem como espécies distantes que con- vergem em hábitos. Estes resultados combinados Resumo. São apresentadas informações sobre indicam que, além de fatores ecológicos correntes a história natural de 66 espécies de serpentes (e.g., pressão de predação; disponibilidade difer- encontradas em matas na região de Manaus, encial de presas em diferentes microhabitats), Amazônia central, Brasil. Para cada espécie fatores históricos (filogenia e biogeografia) devem são fornecidas informações sobre tamanho, ter tido um papel importante na determinação coloração, habitat e microhabitat, hábitos ali- dos padrões atuais de história natural desta co- mentares, reprodução e defesa. Também é munidade de serpentes. Foi encontrada uma fornecida uma revisão parcial das informações grande diversidade de táticas defensivas na co- disponíveis para outras localidades amazôni- munidade e a filogenia deve ser um importante cas. Os resultados são baseados em quase 800 fator determinante na ocorrência de táticas defen- capturas ou avistamentos de serpentes reali- sivas em cada espécie. Contradizendo generaliza- zados entre 1990 e 1995 em localidades ao ções sobre o período e a duração da estação re- redor de Manaus, principalmente em uma produtiva em serpentes amazônicas, o recruta- reserva de floresta primária localizada a 25 km mento de jovens na região de Manaus parece ao norte de Manaus. Os dados de campo nesta ocorrer principalmente durante a estação chuvosa reserva foram obtidos durante mais de 2.600 na maioria das espécies, embora algumas se re- horas-homem de procura visual, cerca de produzam ao longo de todo o ano. Esse padrão 1.600 durante procura limitada por tempo. As deve ser conseqüência da estação seca prolongada temperaturas e a umidade relativa em M anaus que ocorre na região, período no qual alguns re- são altas e a quantidade anual de chuvas cursos ocorrem em quantidades limitadas. (média 2075 mm/ano) é relativamente pe- quena, com estação seca prolongada (4–7 me- ses). Entre 65 espécies para as quais existe Good natural history information (cf. informação, 28 (42%) são primariamente ter- Greene 1993) forms the essential raw data for restres, 20 (30%) fossórias e/ou criptozóicas, studies on evolutionary biology and ecology (see 13 (20%) arborícolas e quatro (6%) aquáticas, Greene 1986 1993 1994a,b, for further discus- embora várias espécies uilizem mais de um sions). The few available studies that provide microhabitat quando ativas. Quase todas as good natural history data on Amazonian snakes serpentes inativas foram encontradas sobre a (especially Beebe 1946; Duellman 1978; and vegetação. Com relação ao período de ativi- Dixon and Soini 1986) have been widely used in dade, das 62 espécies para as quais esta in- reviews on snake diversity and community formação está disponível, 26 (41%) parecem structure (e.g., Duellman 1989 1990; Cadle and ser estritamente diurnas, 13 (21%) estrita- Greene 1993). Amazonian habitats are shrinking mente noturnas e 23 (38%) tanto diurnas relatively rapidly, threatening snake populations como noturnas. As cinco presas mais comuns with extinction; thus, the accumulation of de- consumidas pelas serpentes de mata da região tailed natural history data on Amazonian snakes de Manaus foram: lagartos (consumidos por is crucial for future conservation and manage- 58% das espécies), anuros (39%), mamíferos ment (see Greene 1993). (23%), aves (18%) e serpentes (16%). Uma The snake fauna of Central Amazonia is análise de agrupamento combinando dados still poorly known compared to its western (e.g., sobre uso de microhabitat, período de ativi- Dixon and Soini 1986; Duellman 1978; Fugler dade e dieta resultou em vários grupos de 1986; Lescure and Gasc 1986; Rodríguez and espécies com hábitos similares. Todas estas Cadle 1990; Vanzolini 1986), eastern (see Cunha M. Martins and M. E. Oliveira 3 and Nascimento 1993, and references therein), Martins and Oliveira 1993). We consider the and northern (e.g., Beebe 1946; Chippaux Manaus region to be a somewhat triangular area 1986; Gasc and Rodrigues 1980; Hoogmoed limited on the west by an arbitrary straight line 1979 1982b; Lancini 1979; Roze 1966; Test et from the Anavilhanas archipelago (close to the al. 1966) portions. The available information mouth of the Rio Negro) to the Rio Pitinga (ca. on the snakes of Central Amazonia is scarce 250 km north of Rio Amazonas), on the north- (Martins and Oliveira 1993), and the few ref- east by the Rio Uatumã, and on the south by the erences to this fauna (Egler et al. 1996; Hoge Rio Amazonas. This large area has about 35.000 and Nina 1969; Martins 1993; Martins and km2 (3.5 million ha). However, most of our col- Gordo 1993; Martins and Oliveira 1993; lecting effort was made in a few scattered locali- Schmidt and Inger 1951; Vanzolini 1985) deal ties within this large area (see below and Fig. 1 in with one or a few species. The only relatively Martins and Oliveira 1993). Biogeographically, it detailed study on the snakes of Central Ama- is important to stress that our sample is re- zonia is that by Zimmermann and Rodrigues stricted to the northern banks of the Rio Negro (1990), which provides an analysis of the and the Rio Amazonas; if we had expanded our herpetofaunal community in some reserves samplings to the southern banks of these two located about 70 km north of Manaus. For major rivers, some additional species would be snakes, these authors provided short descrip- included in our list. tions of resource use and abundance data, Most of our field data (552 snake sight- based on 226 captures or sightings. ings of 52 species) resulted from a regular snake- Herein we present detailed natural searching program (see Materials and Methods) history data on 62 species of snakes found in that operated from October 1991–March 1993 at the forests of the Manaus region, based on the Reserva Florestal Adolpho Ducke (RFAD; about 800 snake captures or sightings, most of Figs. 1–3). Results from fieldwork before and them (552 sightings) made during a long-term after this period are also included. The RFAD is study at Reserva Ducke, a primary forest a 100 km2 tract of forest, mostly undisturbed, reserve 25 km north of Manaus. Additionally, located at Km 26 on Highway AM-010 (con- we examined several museum specimens necting Manaus to Itacoatiara), north of Manaus.
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