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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
... The fluorescent reflective properties of certain opossum species (Didelphidae) has long been known (Anderson et al., 1978;Meisner, 1983;Pine, 1978Pine, , 1979Pine, , 1981Pine & Handley Jr, 1984;Pine et al., 1985), and recently the coverage of other taxonomic groups showing these properties has increased (Hunt et al., 2009;Gruber & Sparks, 2015;Kohler et al., 2019;Olson et al., 2020, Sobral & Souza-Gudinho, 2022Weidensaul et al., 2011). The ecological significance of fluorescence remains unclear, but theories have been posited that it acts to influence mate choice (Arnold et al., 2002), to dissuade predators (Olofsson et al., 2010), that it is related to crepuscular activity (Kohler et al., 2019), or is evolutionary by-product that is ecologically functionless (Snyder et al., 2012). ...
... The ecological significance of fluorescence remains unclear, but theories have been posited that it acts to influence mate choice (Arnold et al., 2002), to dissuade predators (Olofsson et al., 2010), that it is related to crepuscular activity (Kohler et al., 2019), or is evolutionary by-product that is ecologically functionless (Snyder et al., 2012). Pine et al. (1985) documented fluorescence in 23 species of didelphid but was unable to identify any patterns of age, sex or season within his sample of over 600 specimens (in several mammal collections at the following institutions: National Museum of Natural History, Field Museum of Natural History, Carnegie Museum of Natural History, American Museum of Natural History, Museum of Natural History of the University of Kansas, Los Angeles County Museum of Natural History). Only five of the species examined by Pine that returned a positive result (Caluromys lanatus, Chironectes minimus, Lutreolina crassicaudata, Metachirus nudicaudatus, Monodelphis domestica) form part of the Paraguayan didelphid fauna, as well as one other that returned a negative result (Monodelphis dimidiata listed as Monodelphis sorex). ...
... Given that the current extent of geographic overlap between these two species is limited, this may seem like an unlikely explanation, but we do not know enough about the evolutionary histories of these two species to quantify its historic potential as an isolating mechanism. Pine et al. (1985) found luminescence to be widespread in the genus Marmosa (as currently taxonomically defined) with Marmosa andersoni Pine, 1972 The species sampled by Pine et al. (1985) were classified into distinct subgenera by Voss et al. (2014), with the fluorescing species Ma. andersoni in Stegomarmosa Pine, 1972 andMa. mexicana, Ma. robinsoni andMa. ...
Many species of opossum (Didelphimorphia) are known to fluoresce, but the significance of this characteristic is unclear. In the interests of contributing to the faunal inventory of fluorescence in Didelphids, we examined 62 specimens of 10 species of Paraguayan opossums under a UV light and describe the patterns observed. Of particular interest is a clear apparent difference in fluorescence between two cryptic and occasionally sympatric species, Marmosa rapposa and Marmosa paraguayana which may be a potential isolating mechanism. Furthermore, we suggest the possibility that fluorescence declines with time since collection in Didelphis albiventris, and the fluorescence in that species is not related to age or sex. While the significance of fluorescence in Didelphids remains obscure, patterns observed show some degree of species specificity within the geographic boundaries of this study.
... Numerous organisms have been reported to fluoresce including plants [3], corals [4], insects [5], spiders [6], scorpions [7], crustaceans [8], molluscs [9], fish [10], amphibians [11], reptiles [12] and birds [13]. Fluorescent compounds have been identified in a variety of animal materials including bone, teeth, claws, fur, feathers, carapace and skin, and the visible fluorescent colours observed include red, yellow, green, blue and pink [2,[12][13][14][15][16][17][18]. The reported evolutionary functions for this fluorescence are varied and include the enhanced camouflage [19], signalling to conspecifics including mate signalling [9,13], threat displays to predators and conspecifics [8], enhanced photosynthesis [4] and environmental marking [20]. ...
... To date, reports of fluorescence among mammals have been limited to a relatively small number of species [2,15,16,18,[22][23][24][25]27]. Here, we were able to reproduce the results of these previous studies and observe apparent fluorescence in additional species; we report fluorescence for 125 mammal species, from half of all mammalian families and representing almost all clades in the mammalian phylogeny ( figure 3). ...
... Indeed, the fluorescent property of borax is one reason it is widely used as a cleaning agent to brighten white clothing and other materials. Interestingly, Pine et al. [16], Olson et al. [23] and Nummert et al. [25] reported a decrease in fluorescence intensity for preserved compared with live dormice while Kohler et al. [22] reported a similar degree of fluorescence for live and preserved flying squirrels, but they were tested in different conditions. Storage conditions over the life of preserved specimens may impact the intensity of fluorescence observed; newer specimens protected from light may retain fluorescent characteristics if fluorescent molecules are photodegradable [16,18]. ...
Mammalian fluorescence has been reported from numerous species of monotreme, marsupial and placental mammal. However, it is unknown how widespread this phenomenon is among mammals, it is unclear for many species if these observations of ‘glowing’ are true fluorescence and the biological function of fluorescence remains undetermined. We examined a wide range of mammal species held in a museum collection for the presence of apparent fluorescence using UV light, and then analysed a subset of preserved and non-preserved specimens by fluorescent spectroscopy at three different excitation wavelengths to assess whether the observations were fluorescence or optical scatter, and the impact of specimen preservation. We also evaluated if fluorescence was related to biological traits. We found that fluorescence is widespread in mammalian taxa; we identified examples of the phenomena among 125 species representing all 27 living mammalian orders and 79 families. For a number of model species, there was no evidence of a corresponding shift in the emission spectra when the wavelength of excitation was shifted, suggesting that observations of ‘glowing’ mammals were indeed fluorescence. Preservation method impacted the intensity of fluorescence. Fluorescence was most common and most intense among nocturnal species and those with terrestrial, arboreal and fossorial habits, with more of their body being more fluorescent. It remains unclear if fluorescence has any specific biological role for mammals. It appears to be a ubiquitous property of unpigmented fur and skin but may function to make these areas appear brighter and therefore enhance visual signalling, especially for nocturnal species.
... 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.
... Photoluminescence in living beings (sensu Reinhold et al. 2023) has been reported in an increasing number of species of plants, microorganisms, fungi, and animals. This includes several crepuscular and nocturnal mammals with ultraviolet-induced photoluminescence (sensu Toussaint et al. 2023), such as didelphids (Pine et al. 1985), New World flying squirrels (Glaucomys spp., Kohler et al. 2019), the duck-billed platypus (Ornithorhynchus anatinus, , springhares (Pedetidae, Olson et al. 2021), several al. 2021) to navigate through space, interact with other individuals, and locate their food sources. The Mexican freetailed bat (Tadarida brasiliensis: Molossidae) is a highly gregarious aerial insectivorous bat that is widely distributed and abundant across tropical and subtropical ecosystems of the American continent, except in the Amazon (Wilkins 1989). ...
... The dry museum specimens, however, had greenish photoluminescent skin that did not contrast with the photoluminescent feet bristles like that of live individuals. Observed photoluminescence in the feet of T. brasiliensis could be a by-product of the secretion of tryptophan derivatives on fur, which can produce blue colours (Pine et al. 1985), or of the bristles being composed of a similar keratin compound to that found in the bats' claws, which can contain photoluminescent tryptophan and tyrosine (Melhuish and Smith 1993). Keratinisation has been associated with green photoluminescent structures in some rodents (Sobral and Souza-Gudinho 2022), and some keratin structures such as sheep's wool are known to photoluminesce in the bluegreen region under UV light, probably due to tryptophan residues (Melhuish and Smith 1993). ...
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We describe ultraviolet-induced photoluminescent structures in a nocturnal mammal: the Mexican free-tailed bat (Tadarida brasiliensis: Molossidae). Twenty-four individuals from two roosts near Mexico City were captured and photographed under white and ultraviolet light to corroborate the findings. All 24 presented the same ultraviolet-induced cyan photoluminescent combs of bristles on digits one and five of the feet, as well as some longer photoluminescent hairs on the toes and the edge of the uropatagium. Four individuals of another species sharing one of these roosts, the cave myotis (Myotis velifer: Vespertilionidae), were also captured and photographed, but none exhibited this striking pattern. A further individual of T. brasiliensis was captured opportunistically and photographed in Coahuila, around 700 km away, also showing these photoluminescent bristles. Photoluminescence in museum specimens was ambiguous. This is the first molossid bat for which a photoluminescent structure has been described. It remains to be seen whether any function exists, such as intraspecific communication.
Gliding is only present in six extant groups of mammals—interestingly, despite divergent evolutionary histories, all mammalian gliders are strictly nocturnal. Gliding mammals also seem to have relatively high rates of ultrasound use and ultraviolet-induced photoluminescence (UVP) in contrast with their close relatives. Therefore, we hypothesized that, despite diverging lineages, gliding mammals use similar modes of cryptic communication compared to their non-gliding counterparts. We developed two datasets containing the vocal range (minimum-maximum of the dominant harmonic; kHz) and UVP of 73 and 82 species, respectively; we report four novel vocal repertoires and 57 novel observations of the presence or absence of UVP. We complemented these datasets with information about body size, diel activity patterns, habitat openness, and sociality to explore possible covariates related to vocal production and UVP. We found that the maximum of the dominant harmonic was significant higher in gliding mammals when vocalizing than their non-gliding relatives. Additionally, we found that nocturnality was the only significant predictor of UVP, consistent with the previous hypothesis that luminophores primarily drive UVP in mammal fur. In contrast, however, we did not find UVP ubiquitous in nocturnal mammals, suggesting that some unknown process may contribute to variation in this trait.
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.