Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Thermal imaging outshines spotlighting for detecting cryptic, nocturnal mammals in tropical rainforests

Avril H. Underwood https://orcid.org/0000-0001-5845-1574 A * , Mia A. Derhè https://orcid.org/0000-0002-5364-2766 B and Susan Jacups C
+ Author Affiliations
- Author Affiliations

A College of Science and Engineering, James Cook University, McGregor Road, Smithfield, Qld 4878, Australia.

B Lancaster Environment Centre, Lancaster University, Bailrigg, Lancaster, LA1 4YQ UK.

C The Cairns Institute, James Cook University, McGregor Road, Smithfield, Qld 4878, Australia.

* Correspondence to: avril.underwood@my.jcu.edu.au

Handling Editor: Rafael Villafuerte

Wildlife Research 49(6) 491-499 https://doi.org/10.1071/WR21130
Submitted: 30 August 2021  Accepted: 13 November 2021   Published: 28 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Context: Thermal imaging has been shown to be a valuable technique for detecting a range of terrestrial mammals across different environments. The limited studies looking at its effectiveness in detecting arboreal mammals in rainforest ecosystems have had mixed success due to the complexity of the environment and limitations of the technology itself.

Aims: We investigated whether using a hand-held thermal imaging device would detect more individuals of six species of nocturnal arboreal mammal in tropical rainforests than the most-used detection method of spotlighting. We determined whether environmental variables effecting either equipment operation or mammal behaviour would influence these results.

Methods: We surveyed eight transects across the Wet Tropics of northern Queensland for six species of arboreal mammals using both a hand-held thermal imager and a spotlight. We used a measure of underestimation to compare counts of individual species, and then modelled total mammal counts with detection method and environmental variables to find the best approximating model.

Key results: Spotlighting underestimated the total number of each species by between 33 and 100% when compared with thermal imaging. Detection method alone without any environmental interaction term provided the best approximating model (AICc = 275.58, marginal pseudo R2 = 0.286), with thermal imaging technology detecting almost double the number of our target individuals (12.3 ± 1.76) compared with spotlighting (6.7 ± 1.02).

Conclusions: Despite recorded operational limitations, thermal imaging technology greatly improved our ability to locate both small and large nocturnal, arboreal mammals, including a species that is rarely observed in the wild.

Implications: The potential to not only improve detection of nocturnal, arboreal mammals but also improve cryptic species distribution and abundance measures suggests thermal imaging technology is an important tool for use globally across rainforests environments.

Keywords: cryptic, detection methods, infrared technology, mammals, nocturnal, possums, spotlighting, thermal imaging, tree kangaroos, tropical rainforests.


References

Amstrup, SC, York, G, McDonald, TL, Nielson, R, and Simac, K (2004). Detecting denning polar bears with forward-looking infrared (FLIR) imagery. BioScience 54, 337–344.
Detecting denning polar bears with forward-looking infrared (FLIR) imagery.Crossref | GoogleScholarGoogle Scholar |

Bates, D, Mächler, M, Bolker, B, and Walker, S (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Boonstra, R, Krebs, CJ, Boutin, S, and Eadie, JM (1994). Finding mammals using far-infared thermal imaging. Journal of Mammalogy 75, 1063–1068.
Finding mammals using far-infared thermal imaging.Crossref | GoogleScholarGoogle Scholar |

Bowler, MT, Tobler, MW, Endress, BA, Gilmore, MP, and Anderson, MJ (2017). Estimating mammalian species richness and occupancy in tropical forest canopies with arboreal camera traps. Remote Sensing in Ecology and Conservation 3, 146–157.
Estimating mammalian species richness and occupancy in tropical forest canopies with arboreal camera traps.Crossref | GoogleScholarGoogle Scholar |

Burnham KP, Anderson DR (2002) ‘Model Selection and Multimodel Inference: a Practical Information–theoretic Approach.’ (Springer-Verlag: New York, NY)

Butler, DA, Ballard, WB, Haskell, SP, and Wallace, MC (2006). Limitations of thermal infrared imaging for locating neonatal deer in semiarid shrub communities. Wildlife Society Bulletin 34, 1458–1462.
Limitations of thermal infrared imaging for locating neonatal deer in semiarid shrub communities.Crossref | GoogleScholarGoogle Scholar |

Collier, BA, Ditchkoff, SS, Raglin, JB, and Jorgan, MS (2007). Detection probability and sources of variation in white-tailed deer spotlight surveys. The Journal of Wildlife Management 71, 277–281.
Detection probability and sources of variation in white-tailed deer spotlight surveys.Crossref | GoogleScholarGoogle Scholar |

Coudrat, C, Rogers, L, and Nekaris, K (2011). Abundance of primates reveals samkos wildlife sanctuary, cardamom mountains, cambodia as a priority area for conservation. Oryx 45, 427–434.
Abundance of primates reveals samkos wildlife sanctuary, cardamom mountains, cambodia as a priority area for conservation.Crossref | GoogleScholarGoogle Scholar |

Das, N, Biswas, J, Das, J, Ray, P, Sangma, A, and Bhattacharjee, P (2009). Status of Bengal slow loris Nycticebus bengalensis (Primates: Lorisidae) in gibbon wildlife sanctuary, Assam, India. Journal of Threatened Taxa 1, 558–561.
Status of Bengal slow loris Nycticebus bengalensis (Primates: Lorisidae) in gibbon wildlife sanctuary, Assam, India.Crossref | GoogleScholarGoogle Scholar |

Ditchkoff, SS, Raglin, JB, Smith, JM, and Collier, BA (2005). From the field: capture of white-tailed deer fawns using thermal imaging technology. Wildlife Society Bulletin 33, 1164–1168.
From the field: capture of white-tailed deer fawns using thermal imaging technology.Crossref | GoogleScholarGoogle Scholar |

Duckworth, J (1998). The difficulty of estimating population densities of nocturnal forest mammals from transect counts of animals. Journal of Zoology 246, 443–486.
The difficulty of estimating population densities of nocturnal forest mammals from transect counts of animals.Crossref | GoogleScholarGoogle Scholar |

Dymond, JR, Trotter, CM, Shepherd, JD, and Wilde, H (2000). Optimizing the airborne thermal detection of possums. International Journal of Remote Sensing 21, 3315–3326.
Optimizing the airborne thermal detection of possums.Crossref | GoogleScholarGoogle Scholar |

Focardi, S, De Marinis, AM, Rizzotto, M, and Pucci, A (2001). Comparative evaluation of thermal infrared imaging and spotlighting to survey wildlife. Wildlife Society Bulletin 29, 133–139.

Franke, U, Goll, B, Hohmann, U, and Heurich, M (2012). Aerial ungulate surveys with a combination of infrared and high–resolution natural colour images. Animal Biodiversity and Conservation 35, 285–293.

Fryxell JM, Sinclair AR, Caughley G (2014) ‘Wildlife Ecology, Conservation, and Management,’ 3rd edn. (John Wiley & Sons: Chichester, West Sussex, UK)

Gill, R, Thomas, M, and Stocker, D (1997). The use of portable thermal imaging for estimating deer population density in forest habitats. Journal of Applied Ecology , 1273–1286.
The use of portable thermal imaging for estimating deer population density in forest habitats.Crossref | GoogleScholarGoogle Scholar |

Goldingay, RL, and Sharpe, DJ (2004). How effective is spotlighting for detecting the squirrel glider? Wildlife Research 31, 443–449.
How effective is spotlighting for detecting the squirrel glider?Crossref | GoogleScholarGoogle Scholar |

Goudberg NJ (1990) The feeding ecology of three species of north Queensland upland rainforest ringtail possums, Hemibelideus lemuroides, Pseudocheirus herbertensis and Pseudocheirus archeri (Marsupialia: Petauridae). PhD Thesis, James Cook University, Townsville, Qld, Australia.

Guisan, A, and Thuiller, W (2005). Predicting species distribution: offering more than simple habitat models. Ecology Letters 8, 993–1009.
Predicting species distribution: offering more than simple habitat models.Crossref | GoogleScholarGoogle Scholar | 34517687PubMed |

Haigh, A, Butler, F, and O’Riordan, RM (2012). An investigation into the techniques for detecting hedgehogs in a rural landscape. Journal of Negative Results 9, 15–26.

Harding, EK, and Gomez, S (2006). Positive edge effects for arboreal marsupials: an assessment of potential mechanisms. Wildlife Research 33, 121–129.
Positive edge effects for arboreal marsupials: an assessment of potential mechanisms.Crossref | GoogleScholarGoogle Scholar |

Havens KJ, Sharp E (1996). The use of thermal imagery in the aerial survey of panthers (and other animals) in the Florida Panther National Wildlife Refuge and the Big Cypress National Preserve. Virginia Institute of Marine Science. Virginia Institute of Marine Science, Gloucester Point, VA, USA.

Havens, KJ, and Sharp, EJ (1998). Using thermal imagery in the aerial survey of animals. Wildlife Society Bulletin 26, 17–23.

Hodnett E (2005) Thermal imaging applications in urban deer control. In ‘Proceedings of the 11th Wildlife Damage Management Conference’. (Eds DL Nolte, KA Fagerstone) pp. 141–148. (Internet Center for Wildlife Damage Management: Traverse City, MI, USA)

Kanowski, J, Hopkins, MS, Marsh, H, and Winter, JW (2001). Ecological correlates of folivore abundance in north Queensland rainforests. Wildlife Research 28, 1–8.
Ecological correlates of folivore abundance in north Queensland rainforests.Crossref | GoogleScholarGoogle Scholar |

Kanowski, J, Winter, JW, and Catterall, CP (2008). Impacts of cyclone Larry on arboreal folivorous marsupials endemic to upland rainforests of the Atherton Tableland, Australia. Austral Ecology 33, 541–548.
Impacts of cyclone Larry on arboreal folivorous marsupials endemic to upland rainforests of the Atherton Tableland, Australia.Crossref | GoogleScholarGoogle Scholar |

Kays, R, and Allison, A (2001). Arboreal tropical forest vertebrates: current knowledge and research trends. Plant Ecology 153, 109–120.
Arboreal tropical forest vertebrates: current knowledge and research trends.Crossref | GoogleScholarGoogle Scholar |

Kays, R, Sheppard, J, McLean, K, Welch, C, Paunescu, C, Wang, V, Kravit, G, and Crofoot, M (2019). Hot monkey, cold reality: surveying rainforest canopy mammals using drone-mounted thermal infrared sensors. International Journal of Remote Sensing 40, 407–419.
Hot monkey, cold reality: surveying rainforest canopy mammals using drone-mounted thermal infrared sensors.Crossref | GoogleScholarGoogle Scholar |

Laurance, WF (1990a). Comparative responses of five arboreal marsupials to tropical forest fragmentation. Journal of Mammalogy 71, 641–653.
Comparative responses of five arboreal marsupials to tropical forest fragmentation.Crossref | GoogleScholarGoogle Scholar |

Laurance, WF (1990b). Effects of weather on marsupial folivore activity in a north Queensland upland tropical rainforest. Australian Mammalogy 13, 41–47.

Laurance, WF, and Laurance, SGW (1996). Responses of five arboreal marsupials to recent selective logging in tropical Australia. Biotropica 28, 310–322.
Responses of five arboreal marsupials to recent selective logging in tropical Australia.Crossref | GoogleScholarGoogle Scholar |

Laurance, SG, and Laurance, WF (1999). Tropical wildlife corridors: use of linear rainforest remnants by arboreal mammals. Biological Conservation 91, 231–239.

Laurance, WF, Laurance, SG, and Hilbert, DW (2008). Long-term dynamics of a fragmented rainforest mammal assemblage. Conservation Biology 22, 1154–1164.
Long-term dynamics of a fragmented rainforest mammal assemblage.Crossref | GoogleScholarGoogle Scholar | 18637907PubMed |

Lenth, RV (2016). Least-squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.

Lim, NTL, and Ng, PKL (2010). Population assessment methods for the Sunda colugo Galeopterus variegatus (Mammalia: Dermoptera) in tropical forests and their viability in Singapore. Raffles Bulletin of Zoology 58, 157–164.

Loretto, D, and Vieira, MV (2011). Artificial nests as an alternative to studies of arboreal small mammal populations: a five-year study in the Atlantic Forest, Brazil. Zoologia 28, 388–394.
Artificial nests as an alternative to studies of arboreal small mammal populations: a five-year study in the Atlantic Forest, Brazil.Crossref | GoogleScholarGoogle Scholar |

Lüdecke, D, Ben-Shachar, MS, Patil, I, Waggoner, P, and Makowski, D (2021). performance: an R package for assessment, comparison and testing of statistical models. Journal of Open Source Software 6, 1–8.
performance: an R package for assessment, comparison and testing of statistical models.Crossref | GoogleScholarGoogle Scholar |

Matthews, TJ, and Whittaker, RJ (2015). REVIEW: on the species abundance distribution in applied ecology and biodiversity management. Journal of Applied Ecology 52, 443–454.
REVIEW: on the species abundance distribution in applied ecology and biodiversity management.Crossref | GoogleScholarGoogle Scholar |

Mazerolle MJ (2017) Package ‘AICcmodavg’. R package 281. R Foundation for Statistical Computing, Vienna, Austria.

McCafferty, DJ (2013). Applications of thermal imaging in avian science. Ibis 155, 4–15.
Applications of thermal imaging in avian science.Crossref | GoogleScholarGoogle Scholar |

McGregor, H, Moseby, K, Johnson, CN, and Legge, S (2021). Effectiveness of thermal cameras compared to spotlights for counts of arid zone mammals across a range of ambient temperatures. Australian Mammalogy 22, .
Effectiveness of thermal cameras compared to spotlights for counts of arid zone mammals across a range of ambient temperatures.Crossref | GoogleScholarGoogle Scholar |

Mills, CA, Godley, BJ, and Hodgson, DJ (2016). Take only photographs, leave only footprints: novel applications of non-invasive survey methods for rapid detection of small, arboreal animals. PLoS One 11, e0146142.
Take only photographs, leave only footprints: novel applications of non-invasive survey methods for rapid detection of small, arboreal animals.Crossref | GoogleScholarGoogle Scholar | 26789632PubMed |

Mutalib, AHA, Ruppert, N, Akmar, S, Kamaruszaman, FLFJ, and Rosely, NFN (2019). Feasibility of thermal imaging using unmanned aerial vehicles to detect Bornean orangutans. Journal of Sustainability Science and Management 14, 182–194.

Nekaris, KAI, Blackham, GV, and Nijman, V (2008). Conservation implications of low encounter rates of five nocturnal primate species (Nycticebus spp.) in Asia. Biodiversity and Conservation 17, 733–747.
Conservation implications of low encounter rates of five nocturnal primate species (Nycticebus spp.) in Asia.Crossref | GoogleScholarGoogle Scholar |

Pahl, L, Winter, J, and Heinsohn, G (1988). Variation in responses of arboreal marsupials to fragmentation of tropical rainforest in north eastern Australia. Biological Conservation 46, 71–82.

Pocknee, CA, Lahoz-Monfort, JJ, Martin, RW, and Wintle, BA (2021). Cost-effectiveness of thermal imaging for monitoring a cryptic arboreal mammal. Wildlife Research , .
Cost-effectiveness of thermal imaging for monitoring a cryptic arboreal mammal.Crossref | GoogleScholarGoogle Scholar |

Rader, R, and Krockenberger, A (2006). Does resource availability govern vertical stratification of small mammals in an Australian lowland tropical rainforest? Wildlife Research 33, 571–576.
Does resource availability govern vertical stratification of small mammals in an Australian lowland tropical rainforest?Crossref | GoogleScholarGoogle Scholar |

R Core Team (2021) ‘R: A Language and Environment for Statistical Computing.’ (Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/

Read, D, and Fox, B (1991). Viability of using faecal pellet counts for estimating parma wallaby, Macropus parma (Marsupialia: Macropodidae) density. Australian Mammalogy 14, 29–32.

Rovero, F, and Marshall, AR (2004). Estimating the abundance of forest antelopes by line transect techniques: a case from the Udzungwa Mountains of Tanzania. Tropical Zoology 17, 267–277.
Estimating the abundance of forest antelopes by line transect techniques: a case from the Udzungwa Mountains of Tanzania.Crossref | GoogleScholarGoogle Scholar |

Russell R (1980) ‘Spotlight on Possums.’ (University of Queensland Press: Brisbane, Qld, Australia)

Sharp EJ, Havens KJ (2015) ‘Thermal Imaging Techniques to Survey and Monitor Animals in the Wild: a Methodology.’ (Elsevier Science & Technology: London, UK)

Sousa-Silva, R, Alves, P, Honrado, J, and Lomba, A (2014). Improving the assessment and reporting on rare and endangered species through species distribution models. Global Ecology and Conservation 2, 226–237.
Improving the assessment and reporting on rare and endangered species through species distribution models.Crossref | GoogleScholarGoogle Scholar |

Stanton JP, Stanton DJ (2005) ‘Vegetation of the Wet Tropics of Queensland Bioregion.’ (Wet Tropics Management Authority: Cairns, Qld, Australia)

Starr, C, Nekaris, K, Streicher, U, and Leung, LK-P (2011). Field surveys of the vulnerable pygmy slow loris Nycticebus pygmaeus using local knowledge in Mondulkiri Province, Cambodia. Oryx 45, 135–142.
Field surveys of the vulnerable pygmy slow loris Nycticebus pygmaeus using local knowledge in Mondulkiri Province, Cambodia.Crossref | GoogleScholarGoogle Scholar |

Stobo-Wilson, AM, Murphy, BP, Cremona, T, and Carthew, SM (2019). Contrasting patterns of decline in two arboreal marsupials from northern Australia. Biodiversity and Conservation 28, 2951–2965.
Contrasting patterns of decline in two arboreal marsupials from northern Australia.Crossref | GoogleScholarGoogle Scholar |

Strahan R (Ed.) (2004) ‘The Mammals of Australia.’ (Reed New Holland: Sydney, NSW, Australia)

Svensson, MS, Samudio, R, Bearder, SK, and Nekaris, KAI (2010). Density estimates of Panamanian owl monkeys (Aotus zonalis) in three habitat types. American Journal of Primatology 72, 187–192.
Density estimates of Panamanian owl monkeys (Aotus zonalis) in three habitat types.Crossref | GoogleScholarGoogle Scholar | 19852005PubMed |

Vinson, SG, Johnson, AP, and Mikac, KM (2020). Thermal cameras as a survey method for Australian arboreal mammals: a focus on the greater glider. Australian Mammalogy 42, 367–374.
Thermal cameras as a survey method for Australian arboreal mammals: a focus on the greater glider.Crossref | GoogleScholarGoogle Scholar |

Wayne, A, Cowling, A, Ward, C, Rooney, J, Vellios, C, Lindenmayer, D, and Donnelly, C (2006). A comparison of survey methods for arboreal possums in Jarrah forest, Western Australia. Wildlife Research 32, 701–714.
A comparison of survey methods for arboreal possums in Jarrah forest, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Whitworth, A, Braunholtz, LD, Huarcaya, RP, MacLeod, R, and Beirne, C (2016). Out on a limb: arboreal camera traps as an emerging methodology for inventorying elusive rainforest mammals. Tropical Conservation Science 9, 675–698.
Out on a limb: arboreal camera traps as an emerging methodology for inventorying elusive rainforest mammals.Crossref | GoogleScholarGoogle Scholar |

Wilson RF (2000) The impact of anthropogenic disturbance on four species of arboreal folivorous possums in the rainforest of north eastern Queensland, Australia. PhD Thesis, James Cook University, Cairns, Queensland, Australia.