Content uploaded by Ronald H Pine
Author content
All content in this area was uploaded by Ronald H Pine on Apr 08, 2018
Content may be subject to copyright.
Labile pigments and fluorescent pelage in didelphid marsupials
Abstract
Mise en evidence d'une fluorescence du pelage apres avoir ete mis en peau chez les Didelphidae. Chez certaines especes les substances fluorescentes paraissent etre a l'interieur des poils et non a leur surface. L'acide 3-hydroxyanthranilique parait etre en grande partie responsable de cette fluorescence, en meme temps que d'autres produits de degradation du tryptophane
... Photoluminescence (fluorescence and/or phosphorescence) is an inherent property of most biological tissues (Stübel, 1911;Niyangoda et al., 2017;Chen et al., 2018), whereby if the excitation light is ultra violet and the re-emission is in the visible spec trum, the organism can appear to glow (Baird, 2015). Although best known from marine environ ments (Sparks et al., 2014), fluorescence and/or phosphorescence is also a trait of many terrest rial invertebrates (Lawrence, 1954), amphibians (Hadjioloff & Zvetkova, 1978), reptiles (Prötzel et al., 2021), birds (Pohland, 2007) and mammals (Pine et al., 1985). ...
... Other Australian mammals are also known to fluoresce, with Bolliger (1944) describing the trait as "not uncommon". Pine et al. (1985) examined museum specimens of Australian mammals for fluorescence but found it to be mild in comparison to American didelphid marsupials. Fluorescence in Australian mammals was then largely forgotten until recently (Reinhold, 2020(Reinhold, , 2021Anich et al., 2021). ...
... My observations of some species differed from some in the literature. For example, the fluorescence of the monotremes examined here and by Pine et al. (1985) and Reinhold (2020) was only subtle. However, both Anich et al. (2021) and Toussaint et al. (2023) reported conspicuous green/ cyan fluorescence in dry-preserved platypus specimens, although relative brightness would need to be compared in the same conditions. ...
The sporadic reporting of fluorescent mammal discoveries has led to the trait being considered atypical. However, this perception may be misleading considering that most mammal species have not been examined. Therefore, I made a targeted attempt to assess the scope of fur fluorescence within one bioregion, the Wet Tropics of Far North Queensland, Australia. A series of 148 fresh, old and frozen wild mammals, mostly roadkill, were examined for the presence of fluorescence in their fur. Two species of monotreme, 20 of marsupial and 22 of placental were collected. Torches of various excitation wavelengths revealed that 95% of all mammal species I was able to examine from the Australian Wet Tropics had at least a low level of fluorescence visible in the fur. Fifty per cent of the mammal species had noticeably mid-to-bright fluorescent fur: 16% had strong pink fluorescence; 43% had strong blueish or other coloured fluorescence; and 9% had both. These observations recalibrate our understanding of mammalian fluorescence to be a somewhat ubiquitous feature of fur chemistry.
... Museum collections are a readily accessible source of mammal material, and an increasing number of studies of photoluminescence have been using them in recent years. Most studies have established the presence of photoluminescence in living or fresh individuals to confirm larger-scale conclusions based on photoluminescence in dry-preserved museum specimens (Udall et al. 1964;Pine et al. 1985;Kohler et al. 2019;Olson et al. 2021;Tumlison and Tumlison 2021). Other studies have relied solely on dry-preserved, or dry-and wet-preserved museum specimens Toussaint et al. 2023), or material whose method of taxidermy was not stated (although likely tanned) of the sole zoo-bred specimen examined (Morandi et al. 2023). ...
... (Toussaint et al. 2023). Pine et al. (1985) previously documented that opossums have more vivid photoluminescence than the other species of mammal they examined, and Hamchand et al. (2021) described the red photoluminescence of fresh European hedgehog, E. europaeus, spines as weak. Therefore, it is improbable that preservation in alcohol was the cause of higher intensity photoluminescence retentino in the wet-preserved opossums. ...
... Therefore, it is improbable that preservation in alcohol was the cause of higher intensity photoluminescence retentino in the wet-preserved opossums. Conversely, Pine et al. (1985) examined dry-preserved skins of opossums that retained hues such as purple, lavender, blue, orange, rose, pink and maroon. Toussaint et al. (2023) recorded the pelage photoluminescence of three of the same species, though different specimens, preserved in alcohol and they were only pink or pink/red, without the blue and purple. ...
Museum specimens have been used as a convenient alternative to live or fresh animals in an increasing number of studies on fur photoluminescence. Although effects of chemical preservation on specimens have been noted, they have not been experimentally tested. I used a series of experiments to answer whether fixation and wet preservation, or tanning, alters the expression of fur photoluminescence in museum specimens. The photoluminescence of northern brown bandicoot, Isoodon macrourus, fur survived initial fixation, but the photoluminescence of both bandicoot and laboratory rat, Rattus norvegicus, fur was severely compromised by longer-term preservation in ethanol. Both chemical and alum tanning eliminated the blue-white photoluminescence of rat fur, but not the pink photoluminescence of bandicoot fur. The results of these small-scale tests indicate that museum-based studies using wet-preserved specimens are likely to be an underestimate of natural photoluminescence in live animals.
... The recent increase in media reports and articles on photoluminescence in biology suggests that photoluminescence in mammals is a rare and exciting new phenomenon (Kohler et al. 2019;Giaimo 2020;Main 2020;Olson et al. 2021). However, research from the last 111 years indicates that the fur of most mammals is likely photoluminescent to some degree, at least at the microscopic level, due to presence of the protein keratin (Rebell et al. 1956;Pine et al. 1985;Toussaint et al. 2023). Photoluminescent pelage occurs in numerous mammal taxa, from rats and bats (Udall et al. 1964), sheep and humans (Millington 2020), to tree-kangaroos (Nicholls and Rienits 1971) and flying squirrels (Kohler et al. 2019). ...
... Photoluminescence in the pelage of mammals is most well-known from opossums in the Americas (Pine et al. 1985). However, the discovery of mammalian photoluminescence predates the work on opossums, with historical publications documenting photoluminescence in a range of species and the isolation of some of the luminophores involved. ...
... Although the extent of brightly photoluminescent fur across mammalian taxa has not been comprehensively documented, the phenomenon has been sporadically recorded across 14 of 28 extant mammal orders (Table 2.1). Figure 2.1 is a timeline of discovery, dividing these orders into the mammal families in which species with luminescent pelage have been found. Pine and Abravaya 1978;Pine et al. 1985;Toussaint et al. 2023Dasyuromorphia Reinhold 2020Peramelemorphia Reinhold 2020Reinhold 2021Diprotodontia Bolliger 1944Nicholls and Rienits 1971;Reinhold 2021Primates Stübel 1911Daly et al. 2009;Millington 2020Lagomorpha Stübel 1911Tumlison 2021 Rodentia Rebell et al. 1956;Kohler et al. 2019;Olson et al. 2021 Eulipotyphla Derrien andTurchini 1925;Hamchand et al. 2021Artiodactyla Hirst 1927Smith et al. 1994;Millington 2020Chiroptera Udall et al. 1964Reinhold 2022 Perissodactyla Posudin 2007 Pholidota (scales) Jeng 2019 Carnivora Latham 1953;Millington 2020;Tumlison and Tumlison 2021 In this review, I convey the historical extent of research on photoluminescence in mammals, filling the gap left by recent reviews (e.g. Lagorio et al. 2015;Jeng 2019;Macel et al. 2020). ...
Photoluminescence (encompassing both fluorescence and phosphorescence) is the absorption and re-emission of light, usually converting photons from lower to higher wavelengths. Since this phenomenon occurs vividly in some, but not all, mammals, the question emerges of whether fur photoluminescence is optically meaningful for those species that possess it. Despite sporadic accounts of photoluminescent mammal species in the literature, there have been no dedicated studies of the prevalence of this trait in any region of Australia. The photoluminescent characteristics of fur have never been examined for most mammal species worldwide. Only a handful of fur luminophores (fluorophores and/or phosphors) have been identified to date, with more suspected to be present in fur. The nature of photoluminescence in fur is also little understood, but has been noted as brighter in live and recently dead animals, with recent museum-based studies flagging, but not accounting for, the chemical changes that fur undergoes in different conditions. Since its detailed documentation in European rabbits (Oryctolagus cuniculus) more than 100 years ago, most studies have assumed that photoluminescence is a dormant by-product of some unknown physiological function. However, potential visual functions have recently been hypothesised because of a resurgence of interest coupled with colour photographs of mammals photoluminescing.
In this thesis, I studied photoluminescence in Australian mammals from the Wet Tropics of Far North Queensland. I addressed gaps in the literature associated with prevalence, the luminophores responsible, retention of photochemical properties, and the function of photoluminescence in the field. Firstly, I investigated how prevalent the phenomenon of photoluminescence is among mammals of the Wet Tropics, Australia, using fresh roadkill animals and frozen specimens from three collections. Although only a subset of Wet Tropics mammal diversity was studied here, I present the most comprehensive account to date of the occurrence of fur photoluminescence across taxa using fresh roadkill animals. Ninety-five per cent of mammals displayed at least a subtle photoluminescence in the fur at some wavelengths. Forty-two per cent of marsupial species and 29% of placental species displayed noticeably bright photoluminescence. Both monotreme species exhibited subtle photoluminescence. There appeared to be no pattern associated with specific diet or lifestyle factors based on species life history characteristics. My findings suggest that photoluminescence is more common than previously known, and that the biochemical basis of fur photoluminescence may be common among mammals.
Secondly, I collected fur samples from seven of these Wet Tropics mammal species to extract and identify the luminophores contributing to photoluminescence. I used high-performance liquid chromatography and liquid chromatography/electrospray ionisation mass spectrometry to identify these luminophores. For two species of bandicoot (the long-nosed bandicoot (Perameles nasuta) and the northern brown bandicoot (Isoodon macrourus)), the northern quoll (Dasyurus hallucatus) and the platypus (Ornithorhynchus anatinus), the work presented here is the first attempt to isolate luminophores from the fur in these genera. I found evidence that supported the presence of coproporphyrin and protoporphyrin, and molecules matching the monoisotopic masses of uroporphyrin and heptacarboxylporphyrin, in the species studied here. These porphyrins had already been identified in the pelage of other mammal species, and exist in a range of organisms from bacteria to birds. Several other photoluminescent molecules extracted from the fur remain to be identified.
Thirdly, I investigated the lability of pink fur photoluminescence in response to light exposure, to ascertain whether observed intraspecies differences can be taken at face value, or whether they may be confounded by environmental conditions. I also tested the effects of wet preservation on both pink and blue fur photoluminescence. I conducted photobleaching experiments using northern brown bandicoot and long-nosed bandicoot pelts and found that pink photoluminescence noticeably fades in as little as two minutes of full sun exposure. These experiments have important implications for researchers working with porphyrin-based photoluminescence. Wet preservation in ethanol nearly extinguished the photoluminescence of both laboratory (Norway) rat (Rattus norvegicus) and bandicoot fur, but initial fixation in formalin partially preserved photoluminescence at a low level. These findings flag the probability of false negatives in studies based solely on museum specimens.
Finally, I investigated the plausibility of a visual function for fur photoluminescence by placing photoluminescent and non-photoluminescent models in the field and assessing the behavioural responses of wild animals to these models over a six-month period. I used remote cameras to observe behaviour under both full moon and new moon cycles to determine whether photoluminescence could be triggered by natural nocturnal lighting conditions. I found that wild nocturnal animals did not show a preference for either model, suggesting either that natural moonlight was not sufficient to stimulate photoluminescence, that wild nocturnal vertebrates were unable to detect photoluminescence in natural conditions, or that these animals do not use this visual property of fur when making behavioural decisions.
... On land, photoluminescence occurs in some fungi (Soop 2005), bacteria (Hurley et al. 2019), and ubiquitously in the chlorophyl of plants ( Krause and Weis 1991). Photoluminescence has also been recorded in terrestrial invertebrates (Kloock 2005), amphibians (Lamb and Davis 2020), reptiles (Prötzel et al. 2021), birds (Derrien and Turchini 1925), and mammals (Bolliger 1944;Pine et al. 1985;Kohler et al. 2019). ...
... Only Jeng (2019) and Croce (2021) mention mammals, with examples beginning in 1985, and many of these studies appear to relate specifically to photoluminescence induced by ultraviolet light (termed UV-induced photoluminescence; Toussaint et al. 2023), although this is not always the case. External UV-induced photoluminescence in the pelage of mammals is most well-known from opossums in the Americas (Pine et al. 1985). However, the discovery of mammalian photoluminescence predates the work on opossums, with historical publications documenting photoluminescence in a range of species and the isolation of some of the luminophores involved. ...
... When metabolized, tryptophan produces a suite of molecules that photoluminesce in various colors. Pine et al. (1985) suspected different tryptophan metabolites to be mostly responsible for the multi-colored photoluminescence in opossums. Tryptophan metabolism can be affected by steroid hormones or an excess of tryptophan in the diet, so the resulting luminophores have the potential to vary with sex, hormone cycles, and diet (Pine et al. 1985). ...
Photoluminescence in the pelage of mammals, a topic that has gained considerable recent research interest, was first documented in the 1700s and reported sporadically in the literature over the last century. The first detailed species accounts were of rabbits and humans, published 111 years ago in 1911. Recent studies have largely overlooked this earlier research into photoluminescent mammalian taxa and their luminophores. Here we provide a comprehensive update on existing research on photoluminescence in mammal fur, with the intention of drawing attention to earlier pioneering research in this field. We provide an overview on appropriate terminology, explain the physics of photoluminescence, and explore pigmentation and the ubiquitous photoluminescence of animal tissues, before touching on the emerging debate regarding visual function. We then provide a chronological account of research into mammalian fur photoluminescence, from the earliest discoveries and identification of luminophores to the most recent studies. While all mammal fur is likely to have a general low-level photoluminescence due to the presence of the protein keratin, fur glows luminously under ultraviolet light if it contains significant concentrations of tryptophan metabolites or porphyrins. Finally, we briefly discuss issues associated with preserved museum specimens in studies of photoluminescence. The study of mammal fur photoluminescence has a substantial history, which provides a broad foundation on which future studies can be grounded.
... Reports of photoluminescence in didelphid marsupials were published in the late 1970 s and early 1980 s (Pine et al., 1985). Since then, there have been few discoveries or studies of this phenomenon in mammalian species. ...
... Since then, there have been few discoveries or studies of this phenomenon in mammalian species. A recent article (Toussaint et al., 2022) confirmed again that Mustela erminea skins can be distinguished from Mustela nivalis by the fluorescence of the former, as was mentioned decades before (Pine et al., 1985). While the phenomenon has been widely reported as biofluorescence in earlier literature, a more recent study suggests that photoluminescence should be used to describe it instead (Toussaint et al., 2022). ...
... The patchy patterns of luminescence in individual springhares seem to suggest that it might serve as camouflage (Olson et al., 2021). Several luminescent porphyrins and tryptophan derivatives have been identified as fluorophores in mammals (Pine et al., 1985;Dooley and Moncrief, 2012;Olson et al., 2021). More recently, it was shown that this photoluminescence may be more widespread in mammals than previously thought and that may not serve a special function but is just a byproduct of physiological processes (Toussaint et al., 2022). ...
Every year, more and more discoveries of photoluminescence in different mammal species are made. The more recent cases thus far have been in duck-billed platypus (Ornithorhyncus anatinus), New World squirrels (Glaucomys spp.) and springhare (Pedetidae). Now we can add another species to the list: the garden dormouse (Eliomys quercinus), an endemic rodent to Europe, currently categorized as Near Threatened (NT) by the IUCN. The fluorescence was described and compared qualitatively in museum specimens, deceased and hibernating animals. The feet and nose of the hibernating dormouse displayed greenish-blue photoluminescence under UV light through a yellow filter, whereas the fur was bright red. The live animal had more vivid red colouring than the museum specimen. The fading and changing of the colour and brightness of photoluminescence was observed in a recently deceased animal and even more strongly in museum specimens.
... Although less UV light is available during the night, most of the biofluorescent mammals identified thus far are nocturnal-crepuscular (Douglas & Jeffery, 2014). Biofluorescence of the pelage under UV light has been documented in marsupial opossums (Didelphids; Meisner, 1983;Pine et al., 1985), the monotreme duck-billed platypus (Ornithorhynchus anatinus; Anich et al., 2021) To the contrary, diurnal squirrels (Sciurus or Tamiasciurus spp.) do not exhibit biofluorescence (Kohler et al., 2019). Thus, the common theme among biofluorescent mammals discovered to-date is that they are active in low-light conditions, such as during dawn, dusk, and night-time or underground. ...
Biofluorescence of mammalian pelage may serve to hide prey from predators sensitive to ultraviolet radiation, among other potential functions. To date biofluorescence has been documented in nocturnal-crepuscular and fossorial mammals that are active under low-light conditions. Giraffes are primarily diurnal, but biofluorescent pelage might offer camouflage from their nocturnal felid predators. Using a full-spectrum camera we qualitatively analyzed UV reflectance and absorption in giraffe pelage from a museum specimen. We found no trace of UV biofluorescence in the giraffe pelage, suggesting that this trait may not be ecologically or biologically relevant in giraffes. The function of biofluorescence in mammals remains elusive, but our study contributes to the growing body of data about biofluorescence, or its lack thereof, in diurnal versus nocturnal-crepuscular or fossorial mammal species.
... Chordate groups are known to comprise at least a single fluorescent organism in their lineages, indicating the evolutionary importance of fluorescence trait (Fig. 3). Fur-based natural fluorescence has been reported in mammals such as Didelphidae marsupials [10], squirrel, Glaucomys spp. [11], platypus, Ornithorhynchus anatinus [12], and springhare, Pedetes surdaster [13]. ...
Since the discovery of the Green fluorescent protein from crystal jellyfish Aequorea victoria, many fluorescent organisms have been identified from different parts of the world. As a result, various fluorescent proteins such as GFP, RFP, and DsRed are discovered and widely used in genetic engineering studies to label a wide range of proteins and genes in mouse models. In bioimaging research, a variety of mouse models are used to visualize fluorescence-based phenotypic variations. In this study, the field mouse, Mus booduga, and common house gecko Hemidactylus frenatus displayed natural blue fluorescence (440–480 nm). The fur of M. booduga and bones of H. frenatus have dis-played blue fluorescence. These organisms may serve as a naturally fluorescent models in bioimaging studies to study phenotypic changes triggered by physico-chemical factors. This study infers that implication of fluorescent terrestrial chordates in evolutionary studies would delineate the origins (ocean to land) and phylogenetic pathways of fluorescent trait in eukaryotes.
Fluorescence induced by ultraviolet light has been observed in many animals, from invertebrates to mammals. Fluorophores (chemical compounds responsible for fluorescence) have been studied in feathers of bird species; for example, porphyrins (one of the most abundant biological pigments) in feathers of some owl species produce red-orange fluorescence. We conducted a fluorescence study on 13 European owl species, and found fluorescence in all of them. Contrary to what was previously reported, we also found fluorescence in the snowy owl (Bubo scandiacus). We also investigated fluorescence of different body and feather areas of the owls, and found similarities between species and some differences depending on occupied landscape, nest and life type, activity period, and plumage colour.
Since the discovery of the Green fluorescent protein from crystal jellyfish Aequorea victoria, many fluorescent organisms have been identified from different parts of the world. As a result, various fluorescent proteins such as GFP, RFP, and DsRed are discovered and widely used in genetic engineering studies to label a wide range of proteins and genes in mouse models. In bioimaging research, a variety of mouse models are used to visualize fluorescence-based phenotypic variations. In this study, the field mouse, Mus booduga, and common house gecko Hemidactylus frenatus dispalyed natural blue fluorescence (440–480 nm). The fur of M. booduga and bones of H. frenatus have displayed blue fluorescence. These organisms may serve as a naturally fluorescent models in bioimaging studies to study phenotypic changes triggered by physico-chemical factors. This study infers that implication of fluorescent terrestrial chordates in evolutionary studies would delineate the origins (ocean to land) and phylogenetic pathways of fluorescent trait in eukaryotes.
Monodelphis emihae (Thomas) generalement considere comme conspecifique avec M. brevicaudata (Erxleben), est une espece distincte sympatrique de M. brevicaudata. D'abord connu seulement de la rive occidentale de Rio Tapagos, M. emiliae existe aussi sur la rive orientale et au Perou. M. emiliae presente comme certains autres didelphides une coloration fugitive qui est en correlation avec sa fluorescence en lumiere ultraviolette
1.1. The red kangaroo and the grey possum have well-defined sternal patches of pigment. The pigment of the patches adheres to the outside of the hairs.2.2. The possum and the tree kangaroo have fluorescent material adhering to the hair, which in the possum is predominantly 3-hydroxyanthranilic acid and in the tree kangaroo is predominantly a mixture of 3-hydroxyanthranilic acid and kynurenine.3.3. Cinnabarinic acid has been shown to be a major component of the free pigment of the red kangaroo.4.4. The free pigment of the possum has characteristics identical with those of pigments synthesized in vitro from dopa and cysteine.5.5. The significance of these observations in relation to the synthesis of hair pigments in mammals is discussed.