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Activity pattern, budget and diurnal rhythmicity of the brown-throated three-toed sloth (Bradypus variegatus) in northeastern Brazil

Abstract

Previous studies exploring the rhythmic activity of sloths of the Bradypus genus in undisturbed forests revealed cathemeral patterns of activity. In the current study we wished to examine sloth behavior in a highly disturbed secondary forest habitat. We evaluated activity pattern, time budget and rhythmic activities of brown-throated three-toed sloths (B. variegatus) living in the border of a highly disturbed forest fragment in northeastern Brazil. Three adults (2 females and 1 male) and 2 infants were studied over 29 days. Observational data were collected in 15 min increments over the 24-h day in the following categories: resting, moving, travelling, eating and grooming. Time series data were subjected to X2 periodogram, Fourier (Fast Fourier Transformation, FFT), cosinor and CircWave circadian rhythm analysis, and revealed significant 24-h rhythms in all behaviors in most circumstances. Unlike sloths located in an undisturbed forest, this population exhibited primarily diurnal activity patterns of behavior, with the center of gravity for each behavior occurring in the middle of the day. Furthermore, several behaviors were expressed in a bimodal pattern, with a morning and a late afternoon peak of activity. These data suggest that with decreased predator presence and with a more ubiquitous food source, sloths adjust their temporal niche to daytime.

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Abbreviations

CG:

Center of gravity

FFT:

Fast Fourier Transformation

ZT:

Zeitgeber time

References

  1. Alanara A, Burns MD, Metcalfe NB (2001) Intraspecific resource partitioning in brown trout: the temporal distribution of foraging is determined by social rank. J Anim Ecol 70:980–986

    Google Scholar 

  2. Altmann J (1974) Observational study of behavior: sampling methods. Behavior 49:227–267

    CAS  Google Scholar 

  3. Beebe W (1926) The three-toed sloth Bradypus cuculliger cuculliger Wagler. Zoologica 7:1–67

    Google Scholar 

  4. Britton SW, Kline RF (1939) On deslothing the sloth. Science 90:16–17

    CAS  PubMed  Google Scholar 

  5. Carmo NAD (2002) Distribuição, densidade, padrão de atividades, dieta e parasitas de Bradypus tridactylus (Mammalia, Xenarthra) em fragmento florestal na Amazonia Central. MPhil thesis, Universidade Federal do Amazonas, Amazonas, Brazil

  6. Cassano CR (2006) Ecologia e conservação da preguiça-de-coleira (Bradypus torquatus Illiger, 1811) no sul da Bahia. MPhil thesis, Universidade Estadual de Santa Cruz, Bahia, Brazil

  7. Castro-Vásquez L, Meza M, Plese T, Moreno-Mora S (2010) Activity patterns, preference and use of floristic resources by Bradypus variegatus in a tropical dry forest fragment, Santa Catalina, Bolívar, Colombia. Edentata 11:62–69

    Google Scholar 

  8. CHESF (2004) Relatório Final da Fase I do Programa de Monitoramento da Fauna, na área de Influência da linha de transmissão 230 kV Recife II/ Pau Ferro. Brasilconsult, Recife

    Google Scholar 

  9. Chiarello AG (1998) Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J Zool 246:1–10

    Google Scholar 

  10. Chiarello AG (2008) Sloth ecology: an overview of field studies. In: Vizcaíno SF, Loughry WJ (eds) The biology of Xenarthra. Florida University Press, Gainesville, pp 269–280

    Google Scholar 

  11. Consentino LN (2004) Aspectos do comportamento da preguica comum, Bradypus variegatus (Xenarthra, Bradypodidae) em uma área de semi-cativeiro no município de Valença—Rio de Janeiro. MPhil thesis, Universidade Federal de Rio de Janeiro, Rio de Janeiro, Brazil

  12. Donati G, Borgognini-Tarli SM (2006) From darkness to daylight: cathemeral activity in primates. J Anthropol Sci 84:7–32

    Google Scholar 

  13. Duarte DPF, Costa CP, Huggins SE (1982) The effects of posture on blood pressure and heart rate in the three-toed sloth Bradypys tridactylus. Comp Biochem Physiol 73(4):697–702

    CAS  Google Scholar 

  14. Duffield GE, Robles-Murguia M, Watson NP, Mantani A, Peirson SN, Loros JJ, Israel MA, Dunlap JC (2009) A role for the Id2 gene in regulating photic entrainment of the mammalian circadian system. Curr Biol 19:297–304

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Ensing EP, Ciuti S, de Wijs FALM, Lentferink DH, ten Hoedt A, Boyce MS, Hut RA (2014) GPS based daily activity patterns in European red deer and North American elk (Cervus elaphus): indication for a weak circadian clock in ungulates. PLoS ONE 9(9):e106997. https://doi.org/10.1371/journal.pone.0106997

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Fenn MGP, MacDonald DW (1995) Use of middens by red foxes: risk reverses rhythms of rats. J Mamm 76:130–136

    Google Scholar 

  17. Freitas BLM (2012) Inventário de mamíferos e o efeito do tamanho e forma dos fragmentos sobre a mastofauna de médio e grande porte em fragmentos florestais isolados do Centro de Endemismo Pernambuco. Undergraduate thesis, Universidade Federal de Pernambuco, Pernambuco, Brazil

  18. Gandavo PM (1980) Tratado da terra do Brasil; história da província Santa Cruz. Fundação Biblioteca Nacional, Rio de Janeiro, Brazil (original edition by Gandavo, 1576)

  19. Giné GAF, Cassano CR, Almeida SS, Faria D (2015) Activity budget, pattern and rhythm of maned sloths (Bradypus torquatus): responses to variations in ambient temperature. Mamm Biol 80:459–467

    Google Scholar 

  20. Glanz WE (1982) The terrestrial mammal fauna of Barro Colorado Island: censuses and long-term changes. In: Leigh EG, Rand AS, Windsor D (eds) The ecology of a tropical forest, seasonal rhythms and long-term changes. Oxford University Press, Oxford, pp 455–468

    Google Scholar 

  21. Goffart M (1971) Function and form in the sloth. Pergamon Press, Oxford

    Google Scholar 

  22. Halle S (2006) Polyphasic activity patterns in small mammals. Folia Primatol 77:15–26

    PubMed  Google Scholar 

  23. Hut RA, Kronfeld-Schor N, Van Der Vinne V, De La Iglesia H (2012) In search of a temporal niche: environmental factors, Chapter 17. Prog Brain Res 199:281–304

    PubMed  Google Scholar 

  24. Kredel FE (1928) Note on the temperature of the sloth. J Mamm 9:48–51

    Google Scholar 

  25. Lockard RB (1978) Seasonal change in the activity pattern of Dipodomys spectabilis. J Mamm 59:563–568

    Google Scholar 

  26. McNab BK (1963) Bioenergetics and the determination of home range size. Am Nat 97:133–140

    Google Scholar 

  27. McNab BK (1978) Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on a ubiquitous food supply. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 153–162

    Google Scholar 

  28. Mendes Pontes AR, Soares ML (2005) Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. J Zool 266:1–9

    Google Scholar 

  29. Mendes Pontes AR, Normande IC, Fernandes ACA, Ribeiro PFR, Soares ML (2007) Fragmentation causes rarity in common marmosets in the Atlantic forest of northeastern Brazil. Biodivers Conserv 16:1175–1182

    Google Scholar 

  30. Mendes Pontes AR, Beltrão ACM, Normande IC, Malta AJR, Silva Júnior AP, Santos AMM (2016) Mass extinction and the disappearance of unknown mammal species: scenario and perspectives of a biodiversity hotspot’s hotspot. PLoS ONE 11(5):e0150887. https://doi.org/10.1371/journal.pone.0150887

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Mendes Pontes AR, Mariz Beltrão AC, Melo Santos AM (2019) Reconsidering mammal extinctions in the Pernambuco Endemism Center of the Brazilian Atlantic Forest: a critique. Anim Biodivers Conserv 42(1):69–77

    Google Scholar 

  32. Montgomery GG, Sunquist ME (1978) Habitat selection and use by two-toed and three-toed sloths. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 329–359

    Google Scholar 

  33. Nagy KA, Montgomery GG (1980) Field metabolic rate, water flux, and food consumption in three-toed sloths (Bradypus variegatus). J Mamm 61:465–472

    Google Scholar 

  34. Oliveira AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in southeastern Brazil and the influence of climate. Biotropica 32:793–810

    Google Scholar 

  35. Oliveira MA, Grillo AS, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx 3(4):389–394

    Google Scholar 

  36. Pepin D, Cargnelutti B (1994) Individual variations of daily activity patterns in radiotracked European hares during winter. Acta Theriol 39:399–409

    Google Scholar 

  37. Pinder L (1985) Observações preliminares sobre a preguiça de coleira (Bradypus torquatus) (Illiger, 1811) (Edentata, Bradypodidae). XII Congresso Brasileiro de Zoologia. Universidade Estadual de Campinas, Campinas, pp 290–291

    Google Scholar 

  38. Pinheiro HLN, Mendes Pontes AR (2015) Home range, diet, and activity patterns of common marmosets (Callithrix jacchus) in very small and isolated fragments of the Atlantic forest of northeastern Brazil. Int J Ecol. https://doi.org/10.1155/2015/685816

    Article  Google Scholar 

  39. Queiroz HL (1995) Preguiças e guaribas. Os mamíferos folívoros arborícolas do Mamirauá. Sociedade Civil Mamirauá, Amazonas

    Google Scholar 

  40. Roxburgh L, Perrin MR (1994) Temperature regulation and activity pattern of the round-eared elephant shrew Macroscelides proboscideus. J Therm Biol 19:13–20

    Google Scholar 

  41. Salvador FV (1975) História do Brasil: 1500 a 1627 (original edition by Salvador, 1627). Editora Melhoramentos, Brasília

    Google Scholar 

  42. Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141:249–260

    Google Scholar 

  43. Sick H (1993) Birds in Brazil: a natural history. Princeton University Press, Princeton

    Google Scholar 

  44. Silva AP Jr, Mendes Pontes AR (2008) The effect of a mega-fragmentation process on large mammal assemblages in the highly-threatened Pernambuco Endemism Centre, north-eastern Brazil. Biodivers Conserv 17:1455–1464

    Google Scholar 

  45. Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeastern Brazil. Nature 404:72–74

    Google Scholar 

  46. Slater PJB (1981) Individual differences in animal behavior. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology, advantages of diversity, IV. Plenum Press, London, pp 35–49

    Google Scholar 

  47. Souza D, Borges O (2004) Todas as aves do Brazil: Guia de campo para identificação. DALL Press, Feira de Santana

    Google Scholar 

  48. Sunquist ME, Montgomery GG (1973) Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J Mamm 54:946–954

    CAS  Google Scholar 

  49. Tabarelli M, Silva JMC, Gascon C (2004) Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodivers Conserv 13:1419–1425

    Google Scholar 

  50. Tachinardi P, Tøien Ø, Valentinuzzi VS, Buck CL, Oda GA (2015) Nocturnal to diurnal switches with spontaneous suppression of wheel-running behavior in a subterranean rodent. PLoS ONE 10(10):e0140500. https://doi.org/10.1371/journal.pone.0140500

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Terborgh J, Wright SJ (1994) Effects of mammalian herbivores on plant recruitment in two Neotropical forests. Ecology 75:1829–1833

    Google Scholar 

  52. Urbani B, Bosque C (2007) Feeding ecology and postural behaviour of the three-toed sloth (Bradypus variegates flaccidus) in northern Venezuela. Mamm Biol 72:321–329

    Google Scholar 

  53. Van der Veen DR, Mulder EGA, Oster H, Gerkema MP, Hut RA (2008) SCN-AVP release of mPer1/mPer2 double-mutant mice in vitro. J Circadian Rhythms 6(5):89. https://doi.org/10.1186/1740-3391-6-5

    CAS  Article  Google Scholar 

  54. Van der Vinne V, Riede SJ, Gorter JA, Eijer WG, Sellix MT, Menaker M, Daan S, Pilorz V, Hut RA (2014) Cold and hunger induce diurnality in a nocturnal mammal. Proc Natl Acad Sci USA 111(42):15256–15260

    PubMed  Google Scholar 

  55. Van Der Vinne V, Gorter JA, Riede SJ, Hut RA (2015) Diurnality as an energy-saving strategy: energetic consequences of temporal niche switching in small mammals. J Exp Biol 218(16):2585–2593

    PubMed  Google Scholar 

  56. Veloso HP, Rangel-Filho ALR, Lima JCA (1991) Classificação da Vegetação Brasileira Adaptada a um Sistema Universal. IBGE, Rio de Janeiro

    Google Scholar 

  57. Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of populations inside protected areas. Science 280:2126–2128

    CAS  PubMed  Google Scholar 

  58. Zhou P, Ross RA, Pywell CM, Liangpunsakul S, Duffield GE (2014) Disturbances in the murine hepatic circadian clock in alcohol-induced hepatic steatosis. Sci Rep 4:3725. https://doi.org/10.1038/srep03725

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the head of the Condomínio Luzanópolis for granting permission to carry out the research in its premises, and Department of Zoology, Universidade Federal de Pernambuco for provision of equipment for fieldwork.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors

Contributions

DOB: Collected and analyzed the data, and wrote the article; LRRL: Analyzed the data; GED and DJA: Analyzed the data and wrote the article; ARMP: Designed the experiment, analyzed the data and wrote the article.

Corresponding author

Correspondence to Antonio Rossano Mendes Pontes.

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Electronic supplementary material

Below is the link to the electronic supplementary material.

42991_2020_47_MOESM1_ESM.pdf

Supplementary file1 Proportions of day/night activity of male BV2 in the Atlantic forest of northeastern Brazil (PDF 410 kb)

42991_2020_47_MOESM2_ESM.pdf

Supplementary file2 Proportions of day/night activity of female BV3 in the Atlantic forest of northeastern Brazil (PDF 409 kb)

42991_2020_47_MOESM3_ESM.pdf

Supplementary file3 Proportions of day/night activity of infant F1 in the Atlantic forest of northeastern Brazil (PDF 408 kb)

42991_2020_47_MOESM4_ESM.pdf

Supplementary file4 Proportions of day/night activity of infant F2 in the Atlantic forest of northeastern Brazil (PDF 408 kb)

42991_2020_47_MOESM5_ESM.pdf

Supplementary file5 Activity records of each of the five behavior categories for male BV2 are shown in double-plotted format. Each horizontal line represents a 48 hr period, and the second 24 hr period is plotted to the right and below the first. Vertical bars represent the occurrence of a behavioral observation. Data are concatenated allowing for 12 days of activity to be analyzed as a continuum. The timing of the light-dark (diel) cycle is indicated by the white-and-black bars below the records. Time is provided as local clock time (PDF 43 kb)

42991_2020_47_MOESM6_ESM.pdf

Supplementary file6 Activity records of each of the five behavior categories for female BV3 are shown in double-plotted format (PDF 36 kb)

42991_2020_47_MOESM7_ESM.pdf

Supplementary file7 Activity records of each of the five behavior categories for infant F1 are shown in double-plotted format (PDF 36 kb)

42991_2020_47_MOESM8_ESM.pdf

Supplementary file8 Activity records of each of the five behavior categories for infant F2 are shown in double-plotted format (PDF 24 kb)

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Oliveira Bezerra, D.d., de Lucena, L.R.R., Duffield, G.E. et al. Activity pattern, budget and diurnal rhythmicity of the brown-throated three-toed sloth (Bradypus variegatus) in northeastern Brazil. Mamm Biol 100, 337–353 (2020). https://doi.org/10.1007/s42991-020-00047-5

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Keywords

  • Bradypus variegatus
  • Circadian rhythm
  • Diurnal rhythm
  • Forest fragmentation
  • Sloth behavior
  • Time budget