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Bradypus Variegatus, Bradypodidae) in Amazonian Black-Water floodplain Forest (Igapó)

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Bradypus Variegatus, Bradypodidae) in Amazonian Black-Water floodplain Forest (Igapó) Canadian Journal of Zoology Cathemeral activity by sloths (Bradypus variegatus, Bradypodidae) in Amazonian black-water floodplain forest (igapó) Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0177.R2 Manuscript Type: Note Date Submitted by the 13-Mar-2021 Author: Complete List of Authors: Castro, Matheus; Instituto Nacional de Pesquisas da Amazonia Dias-Silva, Renann; Universidade Federal do Amazonas, Zoology Barnett, Adrian; University of Roehampton, Life Sciences; Instituto Nacional deDraft Pesquisas da Amazonia, Biodiversity Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Xenarthra, Cathemeral, Activity cycle, Flooded forest, Igapó, Sloth, Keyword: Bradypus variegatus © The Author(s) or their Institution(s) Page 1 of 31 Canadian Journal of Zoology 1 Cathemeral activity by sloths (Bradypus variegatus, Bradypodidae) in Amazonian black- 2 water floodplain forest (igapó) 3 1M.J. Castro-Saa, R.H.P. Dias-Silvab, A.A. Barnettc,d 4 a Ecology Post-graduate Program, National Amazon Research Institute, Av. André Araújo, 2.936 5 - Petrópolis, Manaus, Amazonas, Brazil, [email protected] 6 b Zoology Post-graduate Program, Universidade Federal do Amazonas, Av. Gal. Rodrigo Otávio 7 Jordão Ramos, 3000, Sector South Manaus, Amazonas, Brazil, [email protected] 8 c Amazon Mammals Research Group, National Amazon Research Institute, Av. André Araújo, 9 2.936 - Petrópolis, Manaus, Amazonas, DraftBrazil, 10 d Zoology Department, Federal University of Pernambuco, Recife, Pernambuco, Brazil 11 [email protected] 1Correspondence author Matheus José de Castro Sa, MSc, Ecology Post-graduate Program, National Amazon Research Institute, Av. André Araújo, 2.936 - Petrópolis, Manaus, Amazonas, Brazil. Email: [email protected] Telephone number (Brazil): +55 92 9315-0543 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 31 12 Cathemeral activity by sloths (Bradypus variegatus, Bradypodidae) in Amazonian black-water 13 floodplain forest (igapó) 14 M.J. Castro-Sa, R.H.P. Dias-Silva, A.A. Barnett 15 16 Abstract 17 Both biotic and abiotic factors are important for maintaining the activity cycles of animals, and 18 may determine the most advantageous periods for eating, moving and sleeping. While the solar 19 day-night cycle is among the most central of abiotic variables, a number of species are active 20 both day and night. Three-toed sloth populationsDraft (Bradypus, Linnaeus 1758) across the 21 Neotropics show this pattern, with activity occurring at various points across the 24-hour cycle. 22 In the current study, we used radio tracking techniques to investigate the daily temporal 23 patterning of sloth displacement in Amazonian igapó flooded forest, and compared the results 24 with populations studied in other habitats. We concluded that igapó sloths are cathemeral, and 25 discussed that environmental temperature, nutritional needs and the presence of predators may be 26 the main factors influencing their activity pattern. 27 28 Key words: Sloth, Bradypus variegatus, Cathemeral, Activity cycle, Flooded forest, Igapó. 2 © The Author(s) or their Institution(s) Page 3 of 31 Canadian Journal of Zoology 29 Introduction 30 Animals adopt behavioral strategies that reflect their biological needs and define their 31 activity cycles. Among mammals, there are species that concentrate their activities in well- 32 defined periods and, consequently, can be classified as diurnal, nocturnal or crepuscular. For 33 these organisms the alternation of light and dark across the 24 hour diel period is the main factor 34 determining their activity cycles (Enright 1970). Others do not follow a circadian rhythm 35 synchronized by light-dark phases, and will, instead, display significant amounts of activity 36 during both diurnal and nocturnal periods. In such cases, there may be little or no synchrony 37 between the activity patterns of conspecifics in the same population, or between different 38 populations of the same species. This hasDraft been reported for a variety of mammal species 39 (Eulemur Simons and Rumpler, 1988 and Hapalemur Saint-Hilaire, 1851: Curtis et al. 1999; 40 Donati et al. 2009; Cryptoprocta ferox Bennett, 1833: Colquhoun 1998; Aotus Illiger, 1811: 41 Fernandez-Duque 2003; Alouatta Lacépède, 1799: Dahl and Hemingway 1988; Varecia 42 variegata Kerr, 1792: Wright 1999). Such animals are known as cathemeral, and may have their 43 activity cycles influenced by environmental factors related to temperature, nutritional needs and 44 predation risk, rather than the light/dark cycle (Charles-Dominique 1975; Donati and 45 Borgognini-Tarli 2006). 46 47 In taxa with broad ranges, it is common for the activity cycle to vary geographically in 48 accordance with local conditions (Daan and Aschoff 1975; Halle and Stenseth 2000). Such 49 patterns might be expected in the genus Bradypus Linnaeus, 1758 (three-toed sloths), given that 50 this taxon has a geographical distribution that includes a variety of different tropical forests types 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 31 51 within Central and South America, including rainforest, mangroves, and montane forest (de 52 Moraes-Barros et al. 2011). At the few sites where they have been studied, Bradypus sloths have 53 demonstrated great variation in spatial and temporal activity patterns, both between and within 54 populations (Table 1). In function of low average temperature, in highland forests at 1,500 m 55 altitude (Urbani and Bosque 2007), and at an altitude of 1000 m asl in the forests of the of 56 Atlantic coastal mountains (Chiarello 1998), three-toed sloths were reported to concentre their 57 activities to the warmer daylight hours, and preferentially use the upper, sunnier, strata of trees. 58 However, in the Amazon and in tropical forests of Central America at altitude of 35 m asl, where 59 the temperature of the upper canopy can reach 34 ºC during the day (Sommer et al. 2002), 60 nocturnal activity by sloths has been recorded, with Bradypus sloths reported to be active 61 throughout the 24-hour period, but feedingDraft and locomoting more at night, and generally doing so 62 mostly in the forest mid-strata (Sunquist and Montgomery 1973; Queiroz 1995; Castro-Vásquez 63 et al. 2010). 64 65 Predation risk and nutritional needs may also be important for the activity cycle of three- 66 toed sloths. In the Amazon, while plants species richness is high (Wittmann et al. 2006), there is 67 a diverse assembly of diurnal and nocturnal, sloth predators, both aerial and terrestrial: 68 spectacled owls, Pulsatrix perspicillata Latham, 1790 (Voirin and Kays 2009) and jaguars: 69 Panthera onca Linnaeus, 1758 (Ramalho and Magnusson 2009) (nocturnal), plus harpy eagles: 70 Harpia harpyja Linnaeus, 1758 (Aguiar-Silva et al. 2014), and tayra, Eira barbara Linnaeus, 71 1758 (Bezerra et al. 2009), (diurnal). In such locations, brown-throated three-toed sloths (B. 72 variegatus Schinz, 1825) demonstrate cathemeral behavior and more nocturnal displacement 4 © The Author(s) or their Institution(s) Page 5 of 31 Canadian Journal of Zoology 73 (Queiroz 1995). However in the Atlantic forest, a biome with a long history of anthropic impacts 74 resulting in local extinctions of large predators (Oliveira-Santos and Tizianel 2008; Santos et al. 75 2008; Mendes Pontes et al. 2016), the Bradypus sloths adopt a mainly diurnal pattern (Chiarello 76 1998; Giné et al. 2015; Oliveira Bezerra et al. 2020). This indicates that sloths can change their 77 activity cycle depending on the different environmental pressures imposed by each habitat or 78 ecosystem. Given that sloths in flooded forests have barely been studied, we conducted a study 79 to examine how sloths in Amazonian black-water floodplain forest behave in terms of the 80 temporal patterning of their displacement, as a proxy of activity. 81 82 Here, we present the results of aDraft study of a population of brown-throated three-toed sloth 83 (B. variegatus) monitored for six months in igapó forest, one of many Amazonian habitat types 84 where these animals are abundant but not previously studied. We used data on the time and 85 extent of movement, and a review of activity cycle studies of sloths in other habitats to respond 86 to the following question: Are igapó-living brown-throated three-toed sloth diurnal, nocturnal or 87 cathemeral? As well as using data from the literature to discuss: which potential factors could 88 influence changes in the activity (and displacement) patterns of the brown-throated three-toed 89 sloth in igapó forest. 90 Material and Methods 91 The study was conducted in igapó, an Amazonian forest ecosystem in which sloths have 92 never been studied previously. Igapó is a seasonally-flooded riparian-forest type that covers 93 some 119,000 km2 of the Amazon Basin (Melack and Hess 2010). Annual flooding may exceed 5 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 6 of 31 94 200-days and floodwaters reach 10 m (Wittmann et al. 2006). The study was conducted at 95 Açutuba (ca. 1,840 ha; 3°05´S, 60°18’W), an igapó conservation area within the municipality of 96 Iranduba, some 25 km south of Manaus, the capital of Amazonas State, central Amazonian 97 Brazil (Fig. 1). The annual temperature range is from 23 °C to 36 °C, with no thermal contrast of 98 notably hot and cold months. It rains all year round in Iranduba, with annual precipitation around 99 2.100 mm in two distinct periods: very rainy (between November to May, with maximum 100 rainfall in March, 249 mm), and less rainy (June to October, with minimum rainfall in August, 101 45 mm). Due to proximity to the equator, variation across the year in the times of sunrise and 102 sunset were slight, varying between 05.37-06.08 (sunrise) and 17.51-18.21 (sunset) (Rodrigues et 103 al.
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