Glowing green: A quantitative analysis of photoluminescence in North American bats

Glowing green: A quantitative analysis of photoluminescence in North American bats | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL Ecology and Evolution This is a preprint and has not been peer reviewed. Data may be preliminary. 15 March 2025 V1 Latest version Share on Glowing green: A quantitative analysis of photoluminescence in North American bats Authors : Briana Roberson , Santiago Perea , Daniel Derose-Broeckert , and Steven Castleberry 0000-0002-3320-7900 [email protected] Authors Info & Affiliations https://doi.org/10.22541/au.174203284.42456385/v1 370 views 231 downloads Contents Abstract Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract Photoluminescence produced by excitation with ultraviolet light has been documented in an increasing number of nocturnal-crepuscular mammal species. Here, we provide a quantitative analysis to confirm visual observations of UV-induced photoluminescence in six North American bat species. We used museum specimens to examine wavelength and irradiance at peak photoluminescent emission, within and among species and sexes. We observed green photoluminescence on the wings, uropatagium, and hind limbs of all 60 museum specimens examined. Spectral scans revealed a consistent emission peak between 538 and 560 nm corresponding to the observed green color. We found that Brazilian free-tailed bats (Tadarida brasiliensis) and big brown bats (Eptesicus fuscus) exhibited higher irradiance levels than other species. We found no differences in irradiance or wavelength between sexes and irradiance was not related to specimen age. Our results suggest that photoluminescence is homologous in origin for the species we examined and may serve an important role in social behavior. We emphasize the need for further exploration into the evolutionary and functional roles of photoluminescence across mammalian taxa. 1. Introduction Photoluminescence describes the phenomenon by which molecules absorb photons at a shorter wavelength and produce emission of light at a longer wavelength. The term ‘photoluminescence’ encompasses several mechanisms, including fluorescence, phosphorescence, and light scattering (Shinde et al. 2012, Reinhold 2023). The phenomenon of photoluminescence in biological systems is historically well documented in plants, invertebrates, and marine organisms (Lagorio et al. 2015, Poding et al. 2024). However, the trait is also present within the animal kingdom with mammals recently garnering attention for displaying fluorescence across many taxa (Tumlinson & Tumlinson 2021, Reinhold et al. 2023, Travouillon et al. 2023), suggesting that photoluminescence may be a common synapomorphy among mammals as opposed to an individually derived trait. There is discourse as to whether ultraviolet induced mammal photoluminescence has an adaptive significance that would explain its widespread existence. The trait is currently thought to be attributed to adaptation in low-light conditions, as nearly all species currently confirmed to luminesce are nocturnal, crepuscular, or fossorial (Kohler et al. 2019, Anich et al. 2021, Pynne et al. 2021). Most theories can be grouped into potential advantages for predator evasion, communication, or improving vision in low-light conditions (Kohler et al. 2019, Anich et al. 2021, Olson et al. 2021, Pynne et al. 2021). In addition, most light available during nocturnal and crepuscular hours is within the ultraviolet and blue range (Endler 1993, Cohen et al. 2014). The presence of visible light through ultraviolet induced photoluminescence may provide adaptive advantages such as enhancing visual signaling in nocturnal or crepuscular species (Johnsen 2006). Bats (order Chiroptera) are an interesting model to study potential functions of photoluminescence due to their distinct morphology, adaptations for sensory perception, and social systems. Photoluminescence has been documented in several bat species, including presence on the foot bristles of Mexican free-tailed bats ( Tadarida brasiliensis mexicana) (Suarez et al. 2024) and the wings of Eastern tube-nosed fruit bats ( Nyctimene robinsoni ) (Reinhold, 2022). In addition, Greater Antillean long-tongued bats ( Monophyllus redmani ) exhibit piebald spots that are enhanced visibly in the presence of ultraviolet light (Kurta et al. 2023). Ultraviolet light and its byproducts within the visual spectrum may play a significant role in bat behavior and communication. Patterns between natural history or phylogeny and characteristics of fluorescence in mammals are not easily isolated (Reinhold, 2023), especially because many studies have described fluorescence qualitatively by perceived color or intensity (Pine et al. 1985, Kohler et al. 2019, Pynne et al. 2021, Tumlinson & Tumlinson 2021, Reinhold et al. 2023). Several studies have quantified spectra and noted differences in intensity of emission (Anich et al. 2021) or performed in-depth analyses relating characteristics of emission to life history (Travouillon et al. 2023). However, there are few studies involving within-species replicates and comparisons of closely related species with differing ecological niches, or that quantified specific characteristics of emission such as light intensity. Examining differences in the characteristics of photoluminescent emission among closely related species can provide support for potential phylogenetic patterns. If species exhibit synonymous characteristics of emission, it can be inferred that there is a shared physiological mechanism producing luminescence. Here, we provide a quantitative analysis to confirm visual observations of UV-induced photoluminescence in six species of bats native to North America. To do so, we examined spectral characteristics of emission for differences within and among species and sex and interpreted the results to offer hypotheses for the evolution and function of photoluminescence in bats. We hypothesized that characteristics of emission and therefore proximate origin would be synonymous among the species examined. 2. Materials and Methods 2.1 Specimens We examined five female and five male adult museum specimens of big brown bats ( Eptesicus fuscus ), eastern red bats ( Lasiurus borealis ), Seminole bats ( Lasiurus seminolus ), Southeastern myotis ( Myotis austroriparius ), gray bats ( Myotis grisescens ), and Brazilian free-tailed bats ( Tadarida brasiliensis ) from the Georgia Museum of Natural History (GMNH; Athens, Georgia, USA) mammal collections. Most specimens were collected in Georgia, USA, but collection localities ranged geographically across the United States including South Carolina, Tennessee, Illinois, and California. Specimens ranged from 22 to 103 years since collection (Supplementary Table 1). We first visibly observed specimens for presence of photoluminescence under 410 nm ultraviolet light with an emission spectrum ranging from 395 nm to 425 nm (±15 nm full width half maximum) using yellow UV-filtering lens (Circus, New York, USA, and LPSAFP, Amazon, China) to reduce visual noise from UV and blue light. We photographed specimens in a dark box using a Nikon D5600 camera with an AF-P NIKKOR 18-55 mm lens (Nikon, Melville, New York, USA). For comparison, photographs were taken under only UV light and through the UV-filtering lens. In addition, we used a MIDOPT LP470 yellow longpass filter (Midwest Optical Systems Inc., Palatine, Illinois, USA) to completely filter out incident light under 470 nm and photograph photoluminescent emission color objectively without influence from ultraviolet and blue wavelengths. Specimen photos were digitized with a black background for visualization. 2.2 Measurements We quantified specimen photoluminescent emission spectra with an ILT950 spectroradiometer (International Light Technologies, Peabody, Massachusetts, USA) using an integration time of 4000 ms. The probe was positioned 10 mm over the area of brightest perceived photoluminescence within the uropatagium, which was the body region with the greatest area of photoluminescence available to scan. Intensity of light was recorded as irradiance (µW/cm 2 ). To account for confounding light in the dark room and to isolate photoluminescent emission from the UV light, we recorded initial dark scans with no light present and reference scans of the UV light before specimen scans, using an A253 diffuse reflectance standard reference panel (International Light Technologies, Peabody, Massachusetts, USA). We subtracted dark scans and reference scans from specimen scans using the following formula to ensure analyses only included light produced by specimens. Photoluminescence = | specimen irradiance values - (dark scan irradiance values + reference irradiance values) | We then processed scans to identify characteristics of emission for each species, which included identifying the emission peak as the greatest irradiance value within each scan and recording wavelength value at the emission peak for each specimen. 2.3 Statistical analysis All analyses, scans, and data processing were conducted in R version 4.4.1 (R Core Team, 2024). We first examined specimen emission spectra for inter and intraspecific as well as intersex differences in wavelength (nm) at the emission peak (hereafter ‘peak wavelength’) and irradiance values at the emission peak (hereafter ‘peak irradiance’). We performed a Shapiro-Wilk test for normality and found that response variables were not normally distributed (P < 0.001). Therefore, we used Kruskal-Wallis non-parametric tests to determine differences in peak wavelength and peak irradiance across species and between males and females. When differences were detected, we performed post-hoc pairwise Dunn’s tests using the ‘dunn.test’ package (version 1.3.5; Dinno, 2017), with Bonferroni’s adjustments. To quantify variation in photoluminescence characteristics within species and potential divergence in the amount of variation among species, we evaluated differences in inter and intraspecific dispersion of peak wavelength and irradiance values with permutational analysis of dispersions (PERMDISP) using the ‘betadisper’ function in the ‘vegan’ package (version 2.6-8; Oksanen 2010) with 999 permutations. Intraspecific variability was quantified as average dispersion from median wavelength values (nm) and irradiance values (µW/cm²). We then conducted pairwise post-hoc comparisons using the ‘pairwiseAdonis’ package (version 0.4.1, Martinez Arbizu 2020) with Bonferroni’s adjustment to identify which species differed. To determine if specimen age influenced peak irradiance, we compared a model with specimen age since collection as a predictor variable to a null model with only an intercept term (no trend term) with Generalized Linear Models (GLMs) using the stats package in R. We combined all specimens examined because we did not expect to see species-specific influences of specimen age on irradiance. We used a gamma distribution because the response variable was continuous and not normally distributed. Models were compared using Akaike’s Information Criterion (AIC) with a threshold of ≥ 2 units to determine if the age-predictor model differed in fit from the null model (Burnham & Anderson 2003). We did not expect specimens age to influence wavelength of emission, therefore the relationship between specimen age and peak wavelength was not investigated. Specimens of E. fuscus were excluded from specimen age analysis because all were collected in the same year (Supplementary material 1). 3. Results 3.1 Visual observations Bright green photoluminescence was observed on the uropatagium, wings, and hind limbs of all 60 specimens examined (Figure 1). While differences in photoluminescence intensity were observed, color was consistent among specimens. The use of UV-filtering lens for visual observations was critical in observing true emission color by mitigating the strength of UV and blue light. 3.2 Spectral characteristics We identified a peak in emission wavelength ranging from 520 – 552 nm, consistent with the observed green color (Figure 2). We found no interspecific differences in peak wavelength (Kruskal Wallis: χ² = 10.595, df = 5, p > 0.05), but peak irradiance varied among species (Kruskal Wallis: χ² = 17.833, df = 5, p < 0.001). Post-hoc pairwise comparisons revealed differences in peak irradiance between L. seminolus and T. brasiliensis (χ² = 21.118, p adj. = 0.001) and E. fuscus and L. seminolus (χ² = 21.118, p adj. = 0.001). No differences in peak irradiance were observed between species of the same genus or between males and females of the same species (p > 0.05). Specimen age did not influence irradiance values (AIC GLM = -408.7633, AIC null model = -409.6144). Permutational dispersion tests revealed no differences in interspecific variation in peak wavelength (F 5,52 = 1.8633, p=0.105). However, variation in peak irradiance was different among species (F 5,54 = 2.7743, p=0.024). Post-hoc pairwise comparisons revealed no differences in variation between species of the same genus but identified differences in dispersion of peak irradiance between L. seminolus and T. brasiliensis (F = 13.893 p adj. = 0.015) and E. fuscus and L. seminolus (F = 17.660, p adj. = 0.015). 4. Discussion We provide observations of UV-induced photoluminescence in nocturnal mammal species with specialized life histories. These observations contribute to current findings of photoluminescence being widespread across mammal taxa (Tumlinson & Tumlinson 2021, Reinhold et al. 2023, Travouillon et al. 2023). Our observations are consistent with similar yellow-green photoluminescence on the ventral wing surfaces of Nyctimene robinsoni in Australia (Reinhold, 2022) but are the first confirmation of similar photoluminescence in North American bat species. Our observations differ from the red UV-fluorescence found across distantly related mammal taxa that can be attributed endogenously to porphyrins (Toussaint 2023, Olson 2020) and other colors of pelage fluorescence in mammals currently thought to originate from tryptophan metabolites (Nicholls & Reinits 1971, Reinhold 2023). Based on our results, we can draw several conclusions regarding potential evolutionary drivers of photoluminescence in bats. Because we found no link between either wavelength or irradiance and sex, we conclude that sexual selection is not a likely evolutionary force driving the presence or characteristics of photoluminescence. The species examined differ in their roosting ecology, both by environmental preference and social behavior. Species in the genus Lasiurus are foliage roosters, therefore emission spectra of photoluminescence would be expected to be similar to chlorophyll-a fluorescence with a peak at 680 nm (Lagorio et al. 2015) if functioning to provide camouflage among foliage. Species in the genus Myotis , T. brasilensis , and E. fuscus primarily roost in structures, including cavities, caves, and hollow trees or under bark (Davis et al. 1962, Agosta 2002, Lacki et al. 2009). Given we found no differences in wavelength (and therefore color of light emitted) correlating to these roosting preferences, we do not believe that natural selection via camouflage is a significant factor controlling the characteristics of photoluminescence for any of the roosting strategies represented. Our results do suggest a link between characteristics of photoluminescence and sociality. While the color of emission did not differ among species, differing intensity of light emitted suggests a potential phylogenetic divergence. Both Lasiurus species we examined exhibited the lowest irradiance, and L. seminolus differed in intraspecific variation in irradiance from E. fuscus and T. brasiliensis , the two species exhibiting the greatest irradiance values. Lasiurus species are solitary roosters (Shump & Shump 1982, Klug et al. 2012) whereas Myotis , E. fuscus , and T. brasiliensis all exhibit social roosting behaviors (Rice 1957, Davis et al. 1962, Phillips 1966). There are current hypotheses that fluorescence in marine systems functions in photoenhancement, by providing contrast in environments in which light is highly attenuated (Anthes et al. 2016, Marshall & Johnsen 2017, Poding et al. 2024). The same hypotheses may be applied in nocturnal settings. Bats exhibit preferential roosting site selection based on microclimate conditions (Willis & Brigham 2005, Willis & Brigham 2007, Webber & Willis 2018, Ingersoll et al. 2010). For social species that form roosting aggregations, photoluminescence may act as a signal identifying ideal microclimates in dark environments. Therefore, selection for greater intensity could explain the differences in spectral characteristics of emission observed between solitary and social species. While echolocation is regarded as the primary sensory modality in bats, vision also plays an important role. Members of the family Pteropodidae rely primarily on vision as opposed to laryngeal echolocation (Graydon et al. 1987). Medium to longwave sensitive (M/LWS) vision is highly conserved in bats, with M/LWS opsins able to absorb light in the mid-500 nm range (Wang et al. 2003, Zhao et al. 2009, Simoes et al. 2019). Simões et al. (2019) found the M/LWS opsin is maximally sensitive to a range of 536-560 nm, coinciding with the peak ranges observed in all species we examined. Therefore, it is likely bats can detect the wavelengths of photoluminescent emission we documented in this study. Because there were no interspecific differences in peak wavelength, we can infer similarity of the proximal source of photoluminescence through a shared luminophore and therefore suggest the trait is a synapomorphy among the species examined. Consequently, we can infer that if color is the primary determinant of the ecological function of photoluminescence, the function is synonymous among the species examined. However, our finding of no apparent divergence in intraspecific variation of peak wavelength supports the idea that it is not likely for the color of photoluminescent emission to be adapted for niche-specific function. We recognized the potential for older specimens to exhibit lower emission intensity as a result of degradation. However, our results did not support this supposition. While we found no evidence of specimen age influencing irradiance values, comparison of photoluminescence in live individuals with museum specimens could be important to confirm characteristics and further investigate potential ecological function. Additionally, all specimens examined were adults at the time of collection. Comparative research on characteristics of photoluminescence between juveniles and adults could offer additional insights into the ontogeny of the trait. The term photoluminescence encompasses several mechanisms by which light is emitted following initial excitation, including true fluorescence and light scattering (Clarke & Oprysa, 2006). Whereas studies encompassing multiple mammal taxa by Toussant et al. (2022) & Trouvillon et al. (2023) confirmed emission was a result of fluorescence as opposed to light scattering, further tests involving excitation at multiple wavelengths would be required to conclude the same for the species studied here. Whether light emission is due to true fluorescence or light scattering is not likely a significant factor influencing ecological function. However, additional distinction of mechanisms responsible for photoluminescence may provide greater insight into the molecular origins of emission. Quantifying characteristics of emission allowed us to test specific hypotheses regarding phylogenetic patterns and adaptive significance of photoluminescence in North American bats. Our results suggest that photoluminescence is homologous in origin for the species we examined and is not likely to function in sexual selection or camouflage but may be significant for social behavior. Due to the quality of data produced by the specimens of a range of ages, specimen collections are an important source of data for future photoluminescence studies, and an emphasis is placed on the value of maintaining comprehensive specimen collections to inform future studies. We suggest that future research quantifying differences in photoluminescent characteristics between specimens and live individuals and that further examination of the potential ecological functions of photoluminescence in social species would be beneficial. Data Accessibility Statement R code and museum specimen information are uploaded as supplementary material. We will provide raw data from spectral scans on GitHub. Competing Interest Statement The authors declare no conflict of interest. Author Contributions Briana Roberson: Conceptualization (Lead), Data curation (Lead), Formal analysis (Equal), Investigation (Lead), Methodology (Lead), Writing - original draft (Lead). Santiago Perea: Conceptualization (Supporting), Formal analysis (Equal), Supervision (Lead), Writing - review & editing (Equal). Daniel Derose-Broeckert: Conceptualization (Supporting), Investigation (Supporting), Methodology (Supporting), Writing - review & editing (Supporting). Steven Castleberry: Conceptualization (Supporting), Project administration (Lead), Resources (Lead), Supervision (Supporting), Writing - review & editing (Supporting). Acknowledgements We thank Nicole Pontzer at the Georgia Museum of Natural History for providing specimens and Dr. Billy Hammond at the University of Georgia Vision Sciences laboratory for providing access to the lab and equipment. Literature Cited Agosta, S. J. 2002. Habitat use, diet, and roost selection by the Big Brown Bat ( Eptesicus fuscus ) in North America: a case for conserving an abundant species. Mammal Review 32:179–198. Anich, P. S., S. Anthony, M. Carlson, A. Gunnelson, A. M. Kohler, J. G. Martin, and E. R. Olson. 2021. Biofluorescence in the platypus ( Ornithorhynchus anatinus ). Mammalia 85:179–181. Anthes, N., J. Theobald, T. Gerlach, M. G. Meadows, and N. K. Michiels. 2016. Diversity and ecological correlates of red fluorescence in marine fishes. Frontiers in Ecology and Evolution 4. Brooks, M. E., K. 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Physiological and ecological aspects of roost selection by reproductive female hoary bats ( Lasiurus cinereus ). Journal of Mammalogy 86:85–94. Willis, C. K. R., and R. M. Brigham. 2007. Social thermoregulation exerts more influence than microclimate on forest roost preferences by a cavity-dwelling bat. Behavioral Ecology and Sociobiology 62:97–108. Wood, S. N. 2011. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society (B) 73:3–36. Zhao, H., S. J. Rossiter, E. C. Teeling, C. Li, J. A. Cotton, and S. Zhang. 2009. The evolution of color vision in nocturnal mammals. Proceedings of the National Academy of Sciences 106:8980–8985. Figure legends Figure 1. Specimens of Myotis austroriparius (a-c), Lasiurus seminolus (d-f), Lasiurus borealis (g-i), and Eptesicus fuscus (j-l). Specimens were illuminated under 410 nm light and photographed under UV light alone (column 1), under filtration using yellow tinted UV-filtering lens (column 2), and under filtration using a 470 nm longpass filter (column 3). Figure 2. Photoluminescence emission spectra for museum specimens of six North American bat species (n = 10 for each species). Shaded regions represent 95% confidence intervals. Information & Authors Information Version history V1 Version 1 15 March 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Collection Ecology and Evolution Keywords comparative description evolutionary ecology natural history terrestrial vertebrate Authors Affiliations Briana Roberson University of Georgia View all articles by this author Santiago Perea University of Georgia View all articles by this author Daniel Derose-Broeckert University of Georgia View all articles by this author Steven Castleberry 0000-0002-3320-7900 [email protected] University of Georgia View all articles by this author Metrics & Citations Metrics Article Usage 370 views 231 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Briana Roberson, Santiago Perea, Daniel Derose-Broeckert, et al. Glowing green: A quantitative analysis of photoluminescence in North American bats. Authorea . 15 March 2025. DOI: https://doi.org/10.22541/au.174203284.42456385/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. 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