Advertisement

Moving forward on the sampling efficiency of neotropical small mammals: insights from pitfall and camera trapping over traditional live trapping

  • Ana Filipa PalmeirimEmail author
  • Maíra Benchimol
  • Carlos A. Peres
  • Marcus Vinícius Vieira
Methods Paper

Abstract

The Neotropical region hosts one of the highest levels of small non-volant mammal species diversity worldwide, but sampling therein is often intractable due to high logistic and labour costs. While most common sampling methods include live trapping (LT) and pitfall trapping (PT), camera trapping (CT) is potentially a useful technique. Studies assessing data acquisition efficiency for neotropical small mammals are mostly limited to LT and PT, and no small mammal study to date included CT. We provide a comparative assessment of the efficiency of LT (Sherman and wire-mesh traps), PT and CT in surveying small mammal species across 25 sites in an Amazonian archipelagic landscape. Based on 26,184 trap nights, we obtained 782 small mammal records representing at least 18 species. Most species were detected by both LT (72.2%) and PT (83.3%), but each of these methods exclusively recorded additional species, whereas CT detected only nearly one-fourth (N = 4) of all species recorded. Nevertheless, for nearly all species detected by CT, the probability of detecting individual species was similar or higher than that of LT. Species detected by CT represented the largest-bodied rodents and marsupials (> 200 g). Pitfall traps are an important complement to LT, and CT comprises an efficient technique to sample large-bodied small mammals. Improvements in the efficiency of camera traps in recording and identifying small-bodied species are both needed and possible, but we recommend the combination of LT and PT methods to enhance the completeness of community-wide small mammal sampling in neotropical forests.

Keywords

Amazon Land-bridge islands Marsupials Rodents Sherman Tomahawk 

Notes

Acknowledgements

We are grateful to all 19 volunteers and field assistants who helped during field campaigns and to M. N. da Silva for helping with species identification.

Funding information

Funding was provided by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro–FAPERJ (grant Cientistas do Nosso Estado to MVV), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Grant to MVV), Natural Environment Research Council (NERC; grant NE/J01401X/1 to CAP) and the Post-Graduate Program in Ecology of the Federal University of Rio de Janeiro. The Uatumã Biological Reserve provided logistic support during fieldwork, and additional resources or equipment were provided by The Rufford Small Grants Foundation, RFP-Wildlife Conservation Society, The Conservation, Food and Health Foundation, and Idea Wild. AFP and MB were funded by the Coordenação de Aperfeiçoamento Pessoal de Nível Superior scholarship from the Brazilian Ministry of Education.

Supplementary material

13364_2019_429_MOESM1_ESM.docx (167 kb)
ESM 1 (DOCX 167 kb)

References

  1. Adler GH, Lambert TD (1997) Ecological correlates of trap response of a neotropical forest rodent Proechimvs semispinosus. J Trop Ecol 13:59–68CrossRefGoogle Scholar
  2. Ahumada JA, Silva CEF, Gajapersad K, Hallam C, Hurtado J, Martin E, McWilliam A, Mugerwa B, O’Brien T, Rovero F, Sheil D, Spironello WR, Winarni N, Andelman SJ (2011) Community structure and diversity of tropical forest mammals: data from a global camera trap network. Philos Trans R Soc Lond Ser B Biol Sci 366:2703–2711CrossRefGoogle Scholar
  3. American Veterinary Medical Association (2013) AVMA guidelines for the euthanasia of animals. https://www.avma.org/KB/Policies/Documents/euthanasia.pdf. Accessed Jan 2014
  4. Ardente NC, Ferreguetti AC, Gettinger D, Leal P, Martins-Hatano F, Bergallo HG (2017) Differential efficiency of two sampling methods in capturing non-volant small mammals in an area in eastern Amazonia. Acta Amazon 47:123–132CrossRefGoogle Scholar
  5. Benchimol M, Peres CA (2015) Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in lowland Amazonia. PLoS One 10:e0129818CrossRefGoogle Scholar
  6. Boonstra R, Krebs CJ (1978) Pitfall trapping of Microtus townsendii. J Mammal 59:136–148CrossRefGoogle Scholar
  7. Bovendorp RS, McCleery RA, Galetti M (2017) Optimising sampling methods for small mammal communities in Neotropical rainforests. Mammal Rev 47:148–158CrossRefGoogle Scholar
  8. Buckner CH (1964) Preliminary trials of a camera recording device for the study of small mammals. Can Field Nat 78:77–79Google Scholar
  9. Castleberry SB, Mengak MT, Menken TE (2014) Comparison of trapping and camera survey methods for determining presence of allegheny woodrats. Wildl Soc Bull 38:414–418CrossRefGoogle Scholar
  10. Comissão de Ética, BioÉtica e Bem-Estar Animal/CFMV (2012) Guia Brasileiro de Boas Práticas em Eutanásia em Animais - Conceitos e Procedimentos Recomendados. Brasília, Brazil. http://portal.cfmv.gov.br/uploads/files/Guia%20de%20Boas%20Práticas%20para%20EEutanasi.pdf. Accessed Jan 2014
  11. De Bondi N, White JG, Stevens M, Cooke R (2010) Comparison of the effectiveness of camera trapping and live trapping for sampling terrestrial small-mammal communities. Wildl Res 37:456–465CrossRefGoogle Scholar
  12. Emmons L, Feer F (1997) Neotropical rainforest mammals: a field guide. University of Chicago Press, ChicagoGoogle Scholar
  13. FUNCATE/INPE/ANEEL (2000) Mapeamento por satélite das áreas inundadas por reservatórios de hidrelétricas brasileiras. Unpublished Report. Convênio FUNCATE/INPE/ANEEL, São PauloGoogle Scholar
  14. Gardner TA, Barlow J, Araujo IS, Ávila-Pires TCS, Bonaldo AB, Costa JE, Espósito MC, Ferreira LV, Hawes J, Hermandez MI, Hoogmoed M, Leite RN, Lo-Man-Hung NF, Malcolm JR, Martins MB, Mestre LAM, Miranda-Santos R, Nunes-Gutjahr A, Oveal WL, Parry LTW, Peters SL, Ribeiro-Júnior MA, Silva MNF, Silva-Motta C, Peres CA (2008) The cost-effectiveness of biodiversity surveys in tropical forests. Ecol Lett 11:139–150CrossRefGoogle Scholar
  15. Glen AS, Cockburn S, Nichols M, Ekanayake J, Warburton B (2013) Optimising camera traps for monitoring small mammals. PLoS One 8:e67940CrossRefGoogle Scholar
  16. Hannibal W, Caceres NC (2010) Use of vertical space by small mammals in gallery forest and woodland savannah in South-Western Brazil. Mammalia 74:247–255CrossRefGoogle Scholar
  17. Hice CL, Schmidly DJ (2002) The effectiveness of pitfall traps for sampling small mammals in the Amazon basin. Mastozool Neotrop 9:85–89Google Scholar
  18. Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419CrossRefGoogle Scholar
  19. Hobbs MT, Brehme CS (2017) An improved camera trap for amphibians, reptiles, small mammals, and large invertebrates. PLoS One 12:e0185026CrossRefGoogle Scholar
  20. IBAMA (1997) Plano de manejo fase 1: Reserva Biológica do Uatumã. Eletronorte/Ibama. Brasília/DF. http://www.icmbio.gov.br/portal/images/stories/docs-planos-de-manejo/rebio_uatuma_pm.pdf. Accessed 10 Sept 2017
  21. Jones KE, Bielby J, Cardillo M, Fritz SA, O'Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster CA, Price SA, Rigby EA, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648–2648CrossRefGoogle Scholar
  22. Krebs CJ (1966) Demographic changes in fluctuating populations of Microtus californicus. Ecol Monogr 36:239–273CrossRefGoogle Scholar
  23. Larrucea ES, Brussard PF (2008) Efficiency of various methods used to detect presence of pygmy rabbits in summer. West N Am Nat 68:303–310CrossRefGoogle Scholar
  24. Larsen TH (2016) Core standardized methods for rapid biological field assessment. Conservation International, ArlingtonGoogle Scholar
  25. Laurance WF (1992) Abundance estimates of small mammals in Australian tropical rainforest: a comparison of four trapping methods. Wildl Res 19:651–655CrossRefGoogle Scholar
  26. Macedo J, Loretto D, Vieira MV, Cerqueira R (2006) Classes de desenvolvimento em marsupiais: um método para animais vivos. Mastozool Neotrop 13:133–136Google Scholar
  27. Malcolm JR (1991) The small mammals of Amazonian forest fragments: pattern and process. PhD thesis, University of FloridaGoogle Scholar
  28. Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammals in a panamanian could forest. J Mammal 81:563–570CrossRefGoogle Scholar
  29. McClearn D, Kohler J, McGowan KJ, Cedeno E, Carbone LG, Miller D (1994) Arboreal and terrestrial mammal trapping on Gigante peninsula, Barro Colorado nature monument, Panama. Biotropica 26:208–213CrossRefGoogle Scholar
  30. McCleery RA, Zweig CL, Desa MA, Hunt R, Kitchens WM, Percival HF (2014) A novel method for camera-trapping small mammals. Wildl Soc Bull 38:887–891CrossRefGoogle Scholar
  31. Norris D, Michalski F, Peres CA (2010) Habitat patch size modulates terrestrial mammal activity patterns in Amazonian forest fragments. J Mammal 91:551–560CrossRefGoogle Scholar
  32. O’Connell AF, Nichols JD, Karanth KU (2010) Camera traps in animal ecology: methods and analyses. Springer, LondonGoogle Scholar
  33. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2007) Vegan: the community ecology package. R package version 2, pp 4–2Google Scholar
  34. Oliveira-Santos LG, Tortato MA, Graipel ME (2008) Activity pattern of Atlantic Forest small arboreal mammals as revealed by camera traps. J Trop Ecol 24:563–567CrossRefGoogle Scholar
  35. Palmeirim AF, Benchimol M, Vieira MV, Peres CA (2018) Small mammal responses to Amazonian forest islands are modulated by their forest dependence. Oecologia 187:1–14.  https://doi.org/10.1007/s00442-018-4114-6 CrossRefGoogle Scholar
  36. Patton JL, Da Silva MNF, Malcolm JR (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull Am Mus Nat Hist 244:1–306CrossRefGoogle Scholar
  37. R Core Team (2015) A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  38. Ribeiro-Júnior MA, Rossi RV, Miranda CL, Ávila-Pires TC (2011) Influence of pitfall trap size and design on herpetofauna and small mammal studies in a Neotropical Forest. Zoologia (Curitiba) 28:80–91CrossRefGoogle Scholar
  39. Ripley B, Canty A (2017) Boot: bootstrap functions. R package version 1, pp 3–19Google Scholar
  40. Santos-Filho M, Silva DJ, Sanaiotti TM (2006) Efficiency of four trap types in sampling small mammals in forest fragments. Mato Grosso, Brazil Mastozool Neotrop 13:217–225Google Scholar
  41. Santos-Filho MD, Lázari PRD, Sousa CPFD, Canale GR (2015) Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amaz 45:187–194CrossRefGoogle Scholar
  42. Sikes RS (2016) 2016 guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688CrossRefGoogle Scholar
  43. Silveira L, Jácomo ATA, Diniz-Filho JAF (2003) Camera trap, line transect census and track surveys: a comparative evaluation. Biol Conserv 114:351–355CrossRefGoogle Scholar
  44. Terborgh J, Lopez L, Nuñes PV, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926CrossRefGoogle Scholar
  45. Tilman D (2000) Causes, consequences and ethics of biodiversity. Nature 405:208–211CrossRefGoogle Scholar
  46. Umetsu F, Naxara L, Pardini R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. J Mammal 87:757–765CrossRefGoogle Scholar
  47. Vieira EM, Monteiro-Filho ELA (2003) Vertical stratification of small mammals in the Atlantic rain forest of South-Eastern Brazil. J Trop Ecol 19:501–507CrossRefGoogle Scholar
  48. Villette P, Krebs CJ, Jung TS (2017) Evaluating camera traps as an alternative to live trapping for estimating the density of snowshoe hares (Lepus americanus) and red squirrels (Tamiasciurus hudsonicus). Eur J Wildl Res 63(1):7Google Scholar
  49. Voss RS, Lunde DP, Simmons NB (2001) The mammals of Paracou, French Guiana: a neotropical lowland rainforest fauna part 2. Nonvolant species. Bull Am Mus Nat Hist 263:3–236CrossRefGoogle Scholar
  50. Welbourne DJ, MacGregor C, Paull D, Lindenmayer DB (2015) The effectiveness and cost of camera traps for surveying small reptiles and critical weight range mammals: a comparison with labour-intensive complementary methods. Wildl Res 42:414–425CrossRefGoogle Scholar
  51. Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz W (2014) EltonTraits 1.0: species-level foraging attributes of the world's birds and mammals. Ecology 95:2027–2027CrossRefGoogle Scholar
  52. Woodman N, Timm RM, Slade NA, Doonan TJ (1996) Comparison of traps and baits for censusing small mammals in Neotropical lowlands. J Mammal 77:274–281CrossRefGoogle Scholar
  53. Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2019

Authors and Affiliations

  1. 1.Laboratório de Vertebrados, Departamento de EcologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.School of Environmental SciencesUniversity of East AngliaNorwichUK
  3. 3.Laboratório de Ecologia Aplicada à ConservaçãoUniversidade Estadual de Santa CruzIlhéusBrazil

Personalised recommendations