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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE (Open Access)

Does the photoluminescence of rat fur influence interactions in the field?

Linda M. Reinhold https://orcid.org/0000-0002-1168-9160 A * , David T. Wilson https://orcid.org/0000-0001-5047-0711 B and Tasmin L. Rymer https://orcid.org/0000-0002-9963-6345 A C *
+ Author Affiliations
- Author Affiliations

A College of Science and Engineering, James Cook University, PO Box 6811, Cairns, Qld 4870, Australia.

B Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Qld 4878, Australia.

C Centre for Tropical Environmental and Sustainability Sciences, James Cook University, PO Box 6811, Cairns, Qld 4870, Australia.


Handling Editor: Laura Wilson

Australian Journal of Zoology 71, ZO23021 https://doi.org/10.1071/ZO23021
Submitted: 25 May 2023  Accepted: 12 December 2023  Published: 9 January 2024

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC)

Abstract

While the photoluminescence of mammal fur is widespread, any potential function based on its optical properties remains speculative. Using paired photoluminescent and non-photoluminescent real-fur rat models in a field experiment, we aimed to test whether nocturnal vertebrates reacted differently to blueish-white photoluminescent fur than to non-photoluminescent fur. Remote cameras were set out in three different habitats (farmland, rainforest and woodland) in the Wet Tropics of Far North Queensland, Australia, over three full moon and three new moon phases. We recorded what species interacted with the models and counted the number of interactions with each model to calculate pair-wise differences of interactions with photoluminescent and non-photoluminescent models. No animal group (marsupial, placental mammal or avian) showed a preference for either model, on either new or full moon, suggesting that they either cannot detect a difference, or that preference is not based on photoluminescent properties. These findings do not support a hypothesis of selective pressure from nocturnal vertebrates acting on the trait of blueish-white photoluminescence in mammal fur.

Keywords: fluorescence, hair, mammal, moon, nocturnal, phosphorescence, terrestrial, visual function.

References

Akcali CK, Adan Pérez-Mendoza H, Salazar-Valenzuela D, Kikuchi DW, Guayasamin JM, Pfennig DW (2019) Evaluating the utility of camera traps in field studies of predation. PeerJ 7, e6487.
| Crossref | Google Scholar | PubMed |

Anich PS, Anthony S, Carlson M, Gunnelson A, Kohler AM, Martin JG, Olson ER (2021) Biofluorescence in the platypus (Ornithorhynchus anatinus). Mammalia 85, 179-181.
| Crossref | Google Scholar |

Arnold KE, Owens IPF, Marshall NJ (2002) Fluorescent signaling in parrots. Science 295, 92.
| Crossref | Google Scholar | PubMed |

Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002) Trichromacy in Australian marsupials. Current Biology 12, 657-660.
| Crossref | Google Scholar | PubMed |

Arrese CA, Beazley LD, Neumeyer C (2006) Behavioural evidence for marsupial trichromacy. Current Biology 16, R193-R194.
| Crossref | Google Scholar | PubMed |

Bergman TJ, Kitchen DM (2009) Comparing responses to novel objects in wild baboons (Papio ursinus) and geladas (Theropithecus gelada). Animal Cognition 12, 63-73.
| Crossref | Google Scholar | PubMed |

Brown GE, Crane AL, Demers EE, Chivers DP, Ferrari MCO (2022) Uncertain foraging opportunities and predation risk exert additive effects on induced neophobia in cichlids. Animal Behaviour 186, 21-28.
| Crossref | Google Scholar |

Caro T (2013) The colours of extant mammals. Seminars in Cell & Developmental Biology 24, 542-552.
| Crossref | Google Scholar | PubMed |

Carvalho LdS, Cowing JA, Wilkie SE, Bowmaker JK, Hunt DM (2006) Shortwave visual sensitivity in tree and flying squirrels reflects changes in lifestyle. Current Biology 16, R81-R83.
| Crossref | Google Scholar | PubMed |

Clarke JA (1983) Moonlight’s influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behavioral Ecology and Sociobiology 13, 205-209.
| Crossref | Google Scholar |

Clulow S, Peters KL, Blundell AT, Kavanagh RP (2011) Resource predictability and foraging behaviour facilitate shifts between nomadism and residency in the eastern grass owl. Journal of Zoology 284, 294-299.
| Crossref | Google Scholar |

Czarnecki C, Manderino R, Parry D (2022) Reduced avian predation on an ultraviolet-fluorescing caterpillar model. The Canadian Entomologist 154, e10.
| Crossref | Google Scholar |

Dolan PG, Carter DC (1977) Glaucomys volans. Mammalian Species 78, 1-6.
| Crossref | Google Scholar |

Douglas RH, Jeffery G (2014) The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals. Proceedings of the Royal Society B: Biological Sciences 281, 20132995.
| Crossref | Google Scholar |

Douglas HD, III, Ermakov IV, Gellermann W (2021) Brighter is better: bill fluorescence increases social attraction in a colonial seabird and reveals a potential link with foraging. Behavioral Ecology and Sociobiology 75, 144.
| Crossref | Google Scholar |

Endler JA (1992) Signals, signal conditions, and the direction of evolution. The American Naturalist 139, S125-S153.
| Crossref | Google Scholar |

Endler JA (1993) The color of light in forests and its implications. Ecological Monographs 63, 1-27.
| Crossref | Google Scholar |

Gálvez D, Nieto C, Samaniego P (2020) Test of the prey-attraction hypothesis for the scorpion fluorescence. Neotropical Biodiversity 6, 172-177.
| Crossref | Google Scholar |

Gerlach T, Sprenger D, Michiels NK (2014) Fairy wrasses perceive and respond to their deep red fluorescent coloration. Proceedings of the Royal Society B: Biological Sciences 281, 20140787.
| Crossref | Google Scholar |

Gillespie GR, Brennan K, Gentles T, Hill B, Low Choy J, Mahney T, Stevens A, Stokeld D (2015) A guide for the use of remote cameras for wildlife survey in northern Australia. National Environmental Research Program, Northern Australia Hub, Charles Darwin University, Casuarina, NT.

Hammond BR (2012) The visual effects of intraocular colored filters. Scientifica 2012, 424965.
| Crossref | Google Scholar |

Harvey EN (1957) ‘A history of luminescence from the earliest times until 1900. Memoirs of the American Philosophical Society 44.’ (The American Philosophical Society: Philadelphia)

Hunt DM, Carvalho LS, Cowing JA, Parry JWL, Wilkie SE, Davies WL, Bowmaker JK (2007) Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochemistry and Photobiology 83, 303-310.
| Crossref | Google Scholar | PubMed |

Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biological Reviews of the Cambridge Philosophical Society 68, 413-471.
| Crossref | Google Scholar | PubMed |

Johnsen S, Kelber A, Warrant E, Sweeney AM, Widder EA, Lee RL, Jr, Hernández-Andrés J (2006) Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. Journal of Experimental Biology 209, 789-800.
| Crossref | Google Scholar | PubMed |

Kloock CT (2005) Aerial insects avoid fluorescing scorpions. Euscorpius – Occasional Publications in Scorpiology 2005 1-7.
| Crossref | Google Scholar |

Kohler AM, Olson ER, Martin JG, Anich PS (2019) Ultraviolet fluorescence discovered in New World flying squirrels (Glaucomys). Journal of Mammalogy 100, 21-30.
| Crossref | Google Scholar |

Kuznetsova A, Brockhoff PB, Christensen RHB, Jensen SP (2022) Package ‘lmerTest’. Available at https://cran.r-project.org/web/packages/lmerTest/lmerTest.pdf

Lenth R, Buerkner P, Giné-Vázquez I, Herve M, Jung M, Love J, Miguez F, Riebl H, Singmann H (2022) Package ‘emmeans’. Available at https://cran.r-project.org/web/packages/emmeans/emmeans.pdf

Lim MLM, Land MF, Li D (2007) Sex-specific UV and fluorescence signals in jumping spiders. Science 315, 481.
| Crossref | Google Scholar | PubMed |

Linley GD, Pauligk Y, Marneweck C, Ritchie EG (2021) Moon phase and nocturnal activity of native Australian mammals. Australian Mammalogy 43, 190-195.
| Crossref | Google Scholar |

Marshall J, Johnsen S (2017) Fluorescence as a means of colour signal enhancement. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160335.
| Crossref | Google Scholar | PubMed |

Martin GR (1974) Color vision in the tawny owl (Strix aluco). Journal of Comparative and Physiological Psychology 86, 133-141.
| Crossref | Google Scholar | PubMed |

McDonald B, Geiger B, Vrla S (2020) Ultraviolet vision in Ord’s kangaroo rat (Dipodomys ordii). Journal of Mammalogy 101, 1257-1266.
| Crossref | Google Scholar |

McFarland WN, Munz FW (1975) The visible spectrum during twilight and its implications to vision. In ‘Light as an ecological factor: II’. (Eds GC Evans, R Bainbridge, O Rackham) pp. 249–270. (Blackwell Science Publications: Oxford)

Nicholls EM, Rienits KG (1971) Tryptophan derivatives and pigment in the hair of some Australian marsupials. International Journal of Biochemistry 2, 593-603.
| Crossref | Google Scholar |

O’Carroll DC, Warrant EJ (2017) Vision in dim light: highlights and challenges. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160062.
| Crossref | Google Scholar | PubMed |

Olson ER, Carlson MR, Ramanujam VMS, Sears L, Anthony SE, Anich PS, Ramon L, Hulstrand A, Jurewicz M, Gunnelson AS, Kohler AM, Martin JG (2021) Vivid biofluorescence discovered in the nocturnal springhare (Pedetidae). Scientific Reports 11, 4125.
| Crossref | Google Scholar | PubMed |

Pellis SM, Officer RCE (1987) An analysis of some predatory behaviour patterns in four species of carnivorous marsupials (Dasyuridae), with comparative notes on the eutherian cat Felis catus. Ethology 75, 177-196.
| Crossref | Google Scholar |

Penteriani V, Delgado MdM (2017) Living in the dark does not mean a blind life: bird and mammal visual communication in dim light. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160064.
| Crossref | Google Scholar | PubMed |

Peterson RA (2022) Package ‘bestNormalize’. Available at https://cran.r-project.org/web/packages/bestNormalize/bestNormalize.pdf

Pohland G (2007) Spectral data of avian plumage. PhD thesis, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn.

Potier S, Mitkus M, Kelber A (2020) Visual adaptations of diurnal and nocturnal raptors. Seminars in Cell & Developmental Biology 106, 116-126.
| Crossref | Google Scholar | PubMed |

Pynne JT, Castleberry SB, Conner LM, Piper CW, Parsons EI, Gitzen RA, Duncan SI, Austin JD, McCleery RA (2021) Ultraviolet biofluorescence in pocket gophers. The American Midland Naturalist 186, 150-155.
| Crossref | Google Scholar |

Range F, Huber L (2007) Attention in common marmosets: implications for social-learning experiments. Animal Behaviour 73, 1033-1041.
| Crossref | Google Scholar |

Rebell G (1966) Kynurenine in rat hair. Nature 209, 913-914.
| Crossref | Google Scholar | PubMed |

Rebell G, Mahvi A, Lamb JH (1956) Paper chromatographic separation of fluorescent materials in normal rat hair. Journal of Investigative Dermatology 27, 259-262.
| Crossref | Google Scholar |

Rebell G, Lamb JH, Mahvi A, Lee HR (1957) The identification of L-kynurenine as the cause of fluorescence of the hair of the laboratory rat. Journal of Investigative Dermatology 29, 471-477.
| Crossref | Google Scholar | PubMed |

Reinhold L (2021) Mammals with fluorescent fur: observations from the Wet Tropics. North Queensland Naturalist 51, 1-8.
| Google Scholar |

Reinhold L (2023) Photoluminescence in fur. MPhil thesis, James Cook University, Cairns, Australia. Available at https://doi.org/10.13140/RG.2.2.12146.48325

Reinhold LM, Rymer TL, Helgen KM, Wilson DT (2023) Photoluminescence in mammal fur: 111 years of research. Journal of Mammalogy 104, 892-906.
| Crossref | Google Scholar | PubMed |

R Core Team (2020) R: a language and environment for statistical computing (Version 4.1.2). R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org

RStudio Team (2020) RStudio: integrated development for RStudio (Version 1.0.153). PBC, Boston, Massachusetts, United States of America. Available at https://www.rstudio.com

Tomalia DA, Klajnert-Maculewicz B, Johnson KA-M, Brinkman HF, Janaszewska A, Hedstrand DM (2019) Non-traditional intrinsic luminescence: inexplicable blue fluorescence observed for dendrimers, macromolecules and small molecular structures lacking traditional/conventional luminophores. Progress in Polymer Science 90, 35-117.
| Crossref | Google Scholar |

Toussaint SLD, Ponstein J, Thoury M, Métivier R, Kalthoff DC, Habermeyer B, Guilard R, Bock S, Mortensen P, Sandberg S, Gueriau P, Amson E (2023) Fur glowing under ultraviolet: in situ analysis of porphyrin accumulation in the skin appendages of mammals. Integrative Zoology 18, 15-26.
| Crossref | Google Scholar | PubMed |

Udall SL, Briggs FP, Pautzke CF, Janzen DH (1964) Fluorescence studies. In ‘Wildlife research: problems programs progress 1963. Activities of the branch of wildlife research in the Bureau of Sport Fisheries and Wildlife for the calendar year 1963. Circular 188’. p. 64. (United States Department of the Interior, Fish and Wildlife Service and Bureau of Sport Fisheries and Wildlife: Washington DC). Available at https://spo.nmfs.noaa.gov/sites/default/files/legacy-pdfs/CIRC188.pdf

Viitala J, Korplmäki E, Palokangas P, Koivula M (1995) Attraction of kestrels to vole scent marks visible in ultraviolet light. Nature 373, 425-427.
| Crossref | Google Scholar |

Warrant E (2004) Vision in the dimmest habitats on earth. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural and Behavioral Physiology 190, 765-789.
| Crossref | Google Scholar | PubMed |

Wells-Gosling N, Heaney LR (1984) Glaucomys sabrinus. Mammalian Species 229, 1-8.
| Crossref | Google Scholar |

Yolton RL, Yolton DP, Renz J, Jacobs GH (1974) Preretinal absorbance in sciurid eyes. Journal of Mammalogy 55, 14-20.
| Crossref | Google Scholar | PubMed |