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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
... Since the substantial work of Pine et al. 7 on mammals that can glow under UV light, reports are still scarce. Despite this scarcity, biofluorescence is present in all three major groups of mammals [7][8][9][10][11][12][13][14] . ...
... Since the substantial work of Pine et al. 7 on mammals that can glow under UV light, reports are still scarce. Despite this scarcity, biofluorescence is present in all three major groups of mammals [7][8][9][10][11][12][13][14] . These findings indicate that reflectance occurs throughout the visible spectrum, although more frequent at lower wavelengths (blue and violet). ...
... Other chemicals have been isolated from rat fur, such as tryptophan and kynurenine, and they too are fluorescent 20,21 . Aside from pigments, keratin is a fibrous protein found in epidermic structures that glows yellow-green under UV 7,18,22,23 . Keratinised structures seem to resist the wear of digging 24 . ...
Mammals are generally brown in colour, but recent publications are showing that they may not be as uniform as once assumed. Monotremes, marsupials, and a handful of eutherians reflect various colours when lit with UV light, mostly purple. Because of these still scarce records, we aimed to explore UV reflectance among rodent genera, the most diverse mammalian group, and the group of eutherians with the most common records of biofluorescence. Here we report structures like nails and quills reflected green, but for most genera, it was faded. However, Hystrix, Erethizon, and Ctenomys showed intense and contrasting green glow, while Chaetomys presented a vivid orange anogenital. The main available explanation of fluorescence in mammals relies on porphyrin. This explanation applies to the cases like Chaetomys, where specimens showed anogenital orange biofluorescence, but does not apply to the green biofluorescence we observed. In our sample, because the structures that reflected green were all keratinized, we have reasons to believe that biofluorescence results from keratinization and is a structurally-based colouration. However, not all spines/quills equally biofluoresced, so we cannot rule out other explanations. Since Rodentia is the most common mammalian group with reports on biofluorescence, this trait likely serves various functions that match the species diversity of this group.
... Ultraviolet-induced photoluminescence (UV-PL) has been described in the external organs of plants (Lagorio, Cordon & Iriel 2015), 'invertebrates' (Jeng 2019) and in numerous vertebrates including 'fishes', lissamphibians, squamates, birds, and mammals (Prötzel et al. 2021). As far as mammals are concerned, only a handful of observations have been reported, notably in the platypus (Anich et al. 2021), in marsupials including opossums (Meisner 1983;Pine et al. 1985;Tumlison & Tumlison 2021) and bandicoots (Reinhold 2021), in weasels (Latham 1953;Tumlison & Tumlison 2021), in rodents including flying squirrels (Kohler et al. 2019), springhares (Olson et al. 2021) and pocket gophers (Pynne et al. 2021), and in hedgehogs (Hamchand et al. 2021;Mclaughlin, Music & Strunk 2021;Derrien & Turchini 1925). ...
... Interestingly, this UV-PL can occur in different tissues, and its observed colors vary widely within the visible spectrum depending on the species considered. Reported colors include shades of dark blue or violet for bones (Bachman & Ellis 1965;Goutte et al. 2019;Prötzel et al. 2018;Taboada et al. 2017;Moncrief & Dooley 2013), of light blue and green for skin and hair (Prötzel et al. 2021;Taboada et al. 2017;Pine et al. 1985;Anich et al. 2021;Kohler et al. 2019), of yellow for feathers (e.g., (Arnold, Owens & Marshall 2002;McGraw et al. 2007;Pearn, Bennett & Cuthill 2001), and shades of pink to red from feathers as well as from the pelage of most of the photoluminescent mammals (Meisner 1983;Pine et al. 1985;Weidensaul et al. 2011;Olson et al. 2021;Kohler et al. 2019;Reinhold 2021;Hamchand et al. 2021;Mclaughlin, Music & Strunk 2021). This high variability implies that several UV-reactive molecular or structural compounds contribute to this phenomenon. ...
... Interestingly, this UV-PL can occur in different tissues, and its observed colors vary widely within the visible spectrum depending on the species considered. Reported colors include shades of dark blue or violet for bones (Bachman & Ellis 1965;Goutte et al. 2019;Prötzel et al. 2018;Taboada et al. 2017;Moncrief & Dooley 2013), of light blue and green for skin and hair (Prötzel et al. 2021;Taboada et al. 2017;Pine et al. 1985;Anich et al. 2021;Kohler et al. 2019), of yellow for feathers (e.g., (Arnold, Owens & Marshall 2002;McGraw et al. 2007;Pearn, Bennett & Cuthill 2001), and shades of pink to red from feathers as well as from the pelage of most of the photoluminescent mammals (Meisner 1983;Pine et al. 1985;Weidensaul et al. 2011;Olson et al. 2021;Kohler et al. 2019;Reinhold 2021;Hamchand et al. 2021;Mclaughlin, Music & Strunk 2021). This high variability implies that several UV-reactive molecular or structural compounds contribute to this phenomenon. ...
Examples of photoluminescence (PL) are being reported with increasing frequency in a wide range of organisms from diverse ecosystems. However, the chemical basis of this PL remains poorly defined, and our understanding of its potential ecological function is still superficial. Among mammals, recent analyses have identified free-base por-phyrins as the compounds responsible for the reddish ultraviolet-induced photoluminescence (UV-PL) observed in the pelage of springhares and hedgehogs. However, the localization of the pigments within the hair largely remains to be determined. Here, we use photoluminescence multispectral imaging emission and excitation spec-troscopy to detect, map, and characterize porphyrinic compounds in skin appendages in situ. We also document new cases of mammalian UV-PL caused by free-base porphyrins in distantly related species. Spatial distribution of the UV-PL is strongly suggestive of an endogenous origin of the porphyrinic compounds. We argue that reddish UV-PL is predominantly observed in crepuscular and nocturnal mammals because porphyrins are photodegradable. Consequently , this phenomenon may not have a specific function in intra-or interspecific communication but rather represents a byproduct of potentially widespread physiological processes.
... Ultraviolet-induced photoluminescence (UV-PL) has been described in the external organs of plants (Lagorio et al. 2015), "invertebrates" (Jeng 2019), and in numerous vertebrates, including "fishes," lissamphibians, squamates, birds, and mammals (Prötzel et al. 2021). As far as mammals are concerned, only a handful of observations have been reported, notably in the platypus (Anich et al. 2021), in marsupials including opossums (Meisner 1983;Pine et al. 1985;Tumlison & Tumlison 2021) and bandicoots (Reinhold 2021), in weasels (Latham 1953;Tumlison & Tumlison 2021), in rodents including flying squirrels (Kohler et al. 2019), springhares (Olson et al. 2021), and pocket gophers (Pynne et al. 2021), and in hedgehogs (Derrien & Turchini 1925;Hamchand et al. 2021;Silpa et al. 2021). ...
... Interestingly, this UV-PL can occur in different tissues, and its observed colors vary widely within the visible spectrum depending on the species considered. Reported colors include shades of dark blue or violet for bones (Bachman & Ellis 1965;Moncrief & Dooley 2013;Taboada et al. 2017;Prötzel et al. 2018;Goutte et al. 2019), of light blue and green for skin and hair (Pine et al. 1985;Taboada et al. 2017;Kohler et al. 2019;Anich et al. 2021;Prötzel et al. 2021), of yellow for feathers (e.g. Pearn et al. 2001;Arnold et al. 2002;McGraw et al. 2007), and shades of pink to red from feathers as well as from the pelage of most of the photoluminescent mammals (Meisner 1983;Pine et al. 1985;Weidensaul et al. 2011;Kohler et al. 2019;Hamchand et al. 2021;Silpa et al. 2021;Olson et al. 2021;Reinhold 2021). ...
... Reported colors include shades of dark blue or violet for bones (Bachman & Ellis 1965;Moncrief & Dooley 2013;Taboada et al. 2017;Prötzel et al. 2018;Goutte et al. 2019), of light blue and green for skin and hair (Pine et al. 1985;Taboada et al. 2017;Kohler et al. 2019;Anich et al. 2021;Prötzel et al. 2021), of yellow for feathers (e.g. Pearn et al. 2001;Arnold et al. 2002;McGraw et al. 2007), and shades of pink to red from feathers as well as from the pelage of most of the photoluminescent mammals (Meisner 1983;Pine et al. 1985;Weidensaul et al. 2011;Kohler et al. 2019;Hamchand et al. 2021;Silpa et al. 2021;Olson et al. 2021;Reinhold 2021). This high variability implies that several UV-reactive molecular or structural compounds contribute to this phenomenon. ...
Examples of photoluminescence (PL) are being reported with increasing frequency in a wide range of organisms from diverse ecosystems. However, the chemical basis of this PL remains poorly defined, and our understanding of its potential ecological function is still superficial. Amongst mammals, recent analyses have identified free-base porphyrins as the compounds responsible for the reddish ultraviolet-induced photoluminescence (UV-PL) observed in the pelage of springhares and hedgehogs. However, the localization of the pigments within the hair largely remains to be determined. Here we use photoluminescence multispectral imaging emission and excitation spectroscopy to detect, map and characterize porphyrinic compounds in skin appendages in situ . We also document new cases of mammalian UV-PL caused by free-base porphyrins in distantly related species. Spatial distribution of the UV-PL is strongly suggestive of an endogenous origin of the porphyrinic compounds. We argue that reddish UV-PL is predominantly observed in crepuscular and nocturnal mammals because porphyrins are photodegradable. Consequently, this phenomenon may not have a specific function in intra- or interspecific communication but rather represents a byproduct of potentially widespread physiological processes.Co-first authors: Séverine Toussaint and Jasper Ponstein
... Still, little is known about occurrence of fluorescent properties in pelage of mammals, and most reported observations record the phenomenon in marsupials. Meisner (1983) in a published abstract with little detail, mentioned that the North American opossum (Didelphis virginiana) showed complex patterns of fluorescence, and Pine et al. (1985), noted that 24 of 32 species of New World didelphid marsupials fluoresced in UV light. Australian marsupials including Krefft's glider (Petaurus notatus), striped possum (Dactylopsila trivirgata), and long-nosed bandicoot (Perameles nasuta) exhibited different fluorescent colors when exposed to UV light (Reinhold 2021). ...
... The pink glow produced on some opossums was visible on that entire whitish portion of the shaft. Pine et al. (1985) noted the same fluorescent portions for other didelphid marsupials. All 6 of our live adult and juvenile opossums seen during springtime fluoresced dorsally, whereas only 2 of the 8 museum specimens did so (though most fluoresced ventrally). ...
... Time and method of preservation may affect pelage of prepared skins of mammals. Labile pigments in some hairs may change after death (Pine et al. 1985), and if those fluoresced while the animal was alive, studies of museum specimens may not reveal the property. Chemicals used in preparation of wet specimens or tanning solutions may alter pigment structure and remove or reduce fluorescent properties. ...
... There is substantial research on the occurrence of fluorescence in plants [2] and invertebrates [3,4]. There is also increasing evidence to suggest that many vertebrates have fluorescent pigments, including birds [5][6][7], amphibians [8], reptiles [9,10], fish [11] and mammals [1,[12][13][14][15]. Several hypotheses aim to explain an ecological role of fluorescence in vertebrates. ...
... For example, the ability of aromatic molecules to fluoresce is well documented [24,25]. Other molecules that contain an aromatic ring, such as tryptophan and its derivatives are also capable of fluorescence at different wavelengths [13]. The fluorescence of aromatics is dependent on the de-excitation of an electron from the highest occupied molecular orbital (HOMO) to the lowest unoccupied molecular orbital (LUMO), also known as the HOMO-LUMO gap [26,27]. ...
... It is made Historic observations suggested that fluorescence in mammals was limited to the least weasel (Mustela nivalis) and some Australian marsupials such as the red kangaroo (Macropus rufus) and the grey possum (Trichosurus vulpecula) [33,34]. More recent research found no evidence of fluorescence within the least weasel or red kangaroo and therefore fluorescence was believed at one time to be limited to Didelphidae [13,35]. Fluorescence has now been observed in all major taxonomic clades of mammals. ...
While an array of taxa are capable of producing fluorescent pigments, fluorescence in mammals is a novel and poorly understood phenomenon. We believe that a first step towards understanding the potential adaptive functions of fluorescence in mammals is to develop an understanding of fluorescent compounds, or fluorophores, that are present in fluorescent tissue. Here we use Fourier transform-ion cyclotron resonance mass spectrometry (FT-ICR MS) of flying squirrel fur known to fluoresce under ultraviolet (UV) light to identify potentially fluorescent compounds in squirrel fur. All of the potentially fluorescent compounds we identified were either present in non-fluorescent fur or were not present in all species of fluorescent flying squirrel. Therefore, we consider that the compounds responsible for fluorescence in flying squirrels may also be present in non-fluorescent mammal fur. Some factor currently unexplained likely leads to excitation of fluorophores in flying squirrel fur. A recently suggested hypothesis that fluorescence in mammals is widely caused by porphyrins is consistent with our findings.
... Only few mammalian animals are characterized by fluorescence emission from their external surface upon light irradiation. Some ancient reports are recalled by Pine et al. [229], on the changes in color and fluorescence of the fur of wild animals after killing, when introducing its work on the various colors and fluorescence of hair of museal specimens of didelphid marsupials [229]. After that a renewed attention to the phenomenon has indicated that, in general, it seems to apply greatly to some animals with active life under poor light conditions in the crepuscular and nocturnal phases of the day, transversally representing marsupial and placental mammals in Eastern, European, American and African countries [230]. ...
... Only few mammalian animals are characterized by fluorescence emission from their external surface upon light irradiation. Some ancient reports are recalled by Pine et al. [229], on the changes in color and fluorescence of the fur of wild animals after killing, when introducing its work on the various colors and fluorescence of hair of museal specimens of didelphid marsupials [229]. After that a renewed attention to the phenomenon has indicated that, in general, it seems to apply greatly to some animals with active life under poor light conditions in the crepuscular and nocturnal phases of the day, transversally representing marsupial and placental mammals in Eastern, European, American and African countries [230]. ...
... The main fluorophores described in this section are summarized in Table 10. [229][230][231]233] * Excitation/emission ranges may vary depending on measurement conditions. ...
Organisms belonging to all life kingdoms may have the natural capacity to fluoresce. Autofluorescence events depend on the presence of natural biomolecules, namely endogenous fluorophores, with suitable chemical properties in terms of conjugated double bonds, aromatic or more complex structures with oxidized and crosslinked bonds, ensuring an energy status able to permit electronic transitions matching with the energy of light in the UV-visible-near-IR spectral range. Emission of light from biological substrates has been reported since a long time, inspiring unceasing and countless studies. Early notes on autofluorescence of vegetables have been soon followed by attention to animals. Investigations on full living organisms from the wild environment have been driven prevalently by ecological and taxonomical purposes, while studies on cells, tissues and organs have been mainly promoted by diagnostic aims. Interest in autofluorescence is also growing as a sensing biomarker in food production and in more various industrial processes. The associated technological advances have supported investigations ranging from the pure photochemical characterization of specific endogenous fluorophores to their possible functional meanings and biological relevance, making fluorescence a valuable intrinsic biomarker for industrial and diagnostic applications, in a sort of real time, in situ biochemical analysis. This review aims to provide a wide-ranging report on the most investigated natural fluorescing biomolecules, from microorganisms to plants and animals of different taxonomic degrees, with their biological, environmental or biomedical issues relevant for the human health. Hence, some notes in the different sections dealing with different biological subject are also interlaced with human related issues. Light based events in biological subjects have inspired an almost countless literature, making it almost impossible to recall here all associated published works, forcing to apologize for the overlooked reports. This Review is thus proposed as an inspiring source for Readers, addressing them to additional literature for an expanded information on specific topics of more interest.
... Evidence suggests that fluorescence may diminish between live and preserved specimens (Evtukh 2019;Eipper, et al. 2020;Pine, et al. 1985), and also that fluorescence may become present in dead specimens but not in live specimens. To account for this, we noted whether or not the species examined was a live or preserved specimen as a binary (y/n) variable. ...
... These publications led to decades more of short notes and biofluorescence records in arthropods and marine life until the first records of various fluorescent colorations in marsupial mammals (Pine, et al. 1985), and years later the first record of fluorescence in birds (Pearn et al. 2001). After the turn of the millennium, biofluorescent species publications gained new attention, with massive new records of arthropods and marine animals. ...
Biofluorescent animals have become a recent trend in natural history publishing. While the functions and origins of
biofluorescence in fauna remains somewhat controversial, trends in biofluorescence throughout published literature
may elucidate these concepts. Here we review 101 years of biofluorescent studies encompassing 108 published papers
and 977 unique species records. Our results provide insights into areas of improvement that should be made moving
forward in biofluorescent studies and hypotheses to be tested. Collated records of biofluorescent indicate that
fluorescence is strongly associated with nocturnal and arboreal lifestyles. Our reconstruction of ancestral lineages
based on biofluorescent species records indicate a potential origins and trends in evolution of biofluorescence around
the Middle Miocene Climate Optimum (MMCO) where fluorescent color diversity proliferates with declining global
temperatures and could possibly be indicative of a widespread climate relict among modern taxa; we therefore term
this new concept the Biofluorescent Climate Relict Hypothesis (BCRH).
... However, pocket gophers make aboveground movements associated with natal dispersal (Warren et al., 2017) and searching for mates (Hickman and Brown, 1973). Observations of other taxa (Pine et al., 1985;Kohler et al., 2019;Anich et al., 2021;Olson et al., 2021), along with our observations, suggest biofluorescence is not a sexually dimorphic trait in mammals as might be expected if it played a role in mate selection (Hausmann et al., 2003). Nonetheless, biofluorescence may function in species recognition or territorial establishment. ...
Spectacular photoluminescence (PL) phenomena have been increasingly reported in various organisms from diverse ecosystems. However, the chemical basis of this PL remains poorly defined, and its potential ecological function is still blurry, especially in mammals. Here we used state-of-the-art spectroscopy and multispectral imaging techniques to document new cases of mammalian ultraviolet-induced PL (UV-PL) and to identify free-base porphyrins and natural derivatives as the organic compounds responsible for the reddish luminescence observed in the hairs and spines of distantly related species. We argue that pink to red UV-PL is predominantly observed in crepuscular and nocturnal mammals because porphyrins are photodegradable, and that this phenomenon might not have a specific function in intra- or interspecific communication but consists of a byproduct of a widespread physiological condition, overlooked in mammals.
Co-first authors: Séverine Toussaint and Jasper Ponstein
Spectacular photoluminescence (PL) phenomena have been increasingly reported in various organisms from diverse ecosystems. However, the chemical basis of this PL remains poorly defined, and its potential ecological function is still blurry, especially in mammals. Here we used state-of-the-art spectroscopy and multispectral imaging techniques to document new cases of mammalian ultraviolet-induced PL (UV-PL) and to identify free-base porphyrins and natural derivatives as the organic compounds responsible for the reddish luminescence observed in the hairs and spines of distantly related species. We argue that pink to red UV-PL is predominantly observed in crepuscular and nocturnal mammals because porphyrins are photodegradable, and that this phenomenon might not have a specific function in intra- or interspecific communication but consists of a byproduct of a widespread physiological condition, overlooked in mammals.
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.