CC BY
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ISSN 0869-4362
Русский орнитологический журнал 2019, Том 28, Экспресс-выпуск 1768: 2134-2142
Fluorescence among Fraterculinae subfamily
G.Yu.Evtukh
Grigory Evtukh. Faculty of Biology, Lomonosov Moscow State University. Leninskie Gory, 1-12, Moscow, 119991, Russia. E-mail: grisha59599@yandex.ru
Григорий Юрьевич Евтух. Биологический факультет, Московский государственный университет им. М.В.Ломоносова. Ленинские горы, д. 1, стр. 12, Москва, 119991, Россия
Received 15 April 2019
In recent years fluorescence was found in many vertebrate species. In reptiles there are bony tubercles protruding from the skull in the genus Calumma (Prötzel et al. 2018). The same mechanism is possible for recently discovered fluorescence in geckos (Sloggett 2018). The number of fluorescent tubercles in chameleons is sexually dimorphic in most species, suggesting a signaling role, and also strongly reflects species groups, indicating systematic value of these features (Prötzel et al. 2018).
Fluorescence was also found in many bird species feathering (Lagorio et al. 2015). Among marine birds UV coloration caused by structural reflection was found in two large Aptenodytes species, King Aptenodytes pata-gonicus and Emperor A. forsteri penguins (Jouventin et al. 2005). There is a multilayer reflector photonic microstructure in the bill of King Penguin that produces the UV reflections in the king penguin beak (Dresp et al. 2005).
Previously photoluminescence in bird bills was described in Crested Auklet Aethia cristatella (Wails et al. 2017), Atlantic Puffin Fratercula arctica (Dunning et al. 2018) and Rhinoceros Auklet Cerorhinca monocer-ata (Wilkinson et al. 2019).
The shape of the Puffins high and bilaterally compressed bill is highly adaptive for digging borrows. Narrower jaws exert the higher pressure during grasping and extrude a more limited water volume during the mouth closure that helps birds in catching small shrimps. Also there is an abutment of the mandible against the cranial base, which prevents the former from retreating when bird presses the bill into soil (turf) during digging (Бадикова, Дзержинский 2014) This kind of shape becomes a great opportunity to provide information among individuals about bird condition and readiness for the mating season and could serve as a 'billboard'. Also the conspicuous billing ceremony in the Atlantic Puffin, almost always initiated by the male, functions in pair maintenance but not as a greeting display (Nettleship, Bonan 2019).
In every species that have fluorescent bill patterns bill itself undergoes seasonal shedding. Colorful ornamented rhamphotheca appears only little bit before the mating season, remains during the mating season and
vanishes after chick rising. It relates also to the prominent feathering of Alcidae.
Cerorhinca monocerata has only a deciduous elevated horn at the base of the culmen. Similarly, F. corniculata and F. cirrhata have a deciduous shield covering the base of the bill. This deciduous phenomenon is known in a few other alcids: A. cristatella, A. psittacula (only expected, but not known - Konyukhov 2001) and Alca (Watada et al. 1987).
The seasonal bill-plate shedding is necessary only for those species in which its gradual shedding is impossible because of the complex bill outlines. Among the Auklets, bill-plate shedding was reported, in addition to the whiskered auklet, in the crested auklet (Konyukhov 1993 - cit. by: Konyukhov 2001).
Those that are almost exclusively fish-eaters, such as the Razorbill, the Common Murre Uria aalge and Brachyramphus murrelets, have relatively narrow bills and high tongue cornification to press prey against evenly-spaced but less dense palatal denticles. Intermediate between these extremes are the more generalist feeders on fish and plankton, such as the puffins, the Thick-billed Murre Uria lomvia and the Rhinoceros Auklet Cerorhinca monocerata (Nettleship, Bonan 2019). Badikova and Dzerzhin-sky (Бадикова, Дзержинский 2014) proposed Fratercula morphology as a basal to the group Fraterculini and secondary despecialization of Rhinoc-erous Auklet. Complete adaptation to fish eating in this species is prevented by concurrence with Murres Uria and could be compensated by crepuscular lifestyle.
Methods
The work was provided with collection of Zoological Museum of Moscow State University. I examined all 54 carcasses of Horned puffin, 44 carcasses of Tufted puffin, 4 Aethia species Cassin's auklet and Rhinoceros auklet 1 carcass each to determine presence or absence of light eradiation.
Of each bird I took one photo in RAW. I used DSLR camera (Nikon D610), focal length 300 mm (Nikon 70-300mm f/4.5-5.6G ED-IF AF-S VR Zoom-Nikkor) and the following parameters: ISO 200, f 5.6 at 1/2 s (for Horned puffin) and 1 s (for Tufted puffin because of its dimmer glow). Minimum focus distance was used (1.5 m). Birds were placed all in the same position: bill was turned perpendicular to the axis of lens direction; bill was pointing to the right. UV torch (AloneFire UV, 9-LED) with 395 nm wavelength was placed 50 cm away from bill and it was 45° angle between torch and camera. Torch was placed to the right of the camera. Photos was taken in dark room. Camera, bird and torch were at the same height.
For the fluorescence of bills of Atlantic Puffins estimated mean lambda (max±SE = 492.0±0.58 nm) (Dunning et al. 2018) corresponds with 'cyan' colors in Adobe Photoshop, so these colors were chosen to represent fluorescence in other Puffins. Saturation of colors with shorter wavelengths (blues', 'purples' and 'magentas') was set up to -100 in Adobe Photoshop Camera Raw; cyans were set up to +100. Than photos were saved as JPG images. I tested this method on white paper sheet. After that no 'cyans' or other colors were spotted on the image. I used Adobe Photoshop CC 'Analysis' menu to
conduct further measurements. Ruler placed in the same position was used to set up correspondence between physical bill length and number of pixels on photo (1 cm equivalent = 464 p). To measure fluorescent area and relative brightness of that area I rose saturation of 'cyans' to +100 again to make 'Select > Color range' tool find more pixels colored 'cyans'. It represents the amount of observable light emission in specific part of spectrum. These measurements were recorded as a text (.txt) file and converted to Excel file (.xlsx). Further statistical treatment was provided in 'Statistica 8'. To measure sex differences properly I excluded newest and oldest exemplars from the analysis because of insufficient sampling in new ones and bleaching of old ones. The oldest Horned puffin in collection was killed 117 years ago. Based on this date quartiles were excluded: less than 29 years old and more than 88 years old.
Results and discussion
The photoluminescent glow in bills of Fraterculinae in previous researches supposed to be fluorescence (Wails et al. 2017; Dunning et al. 2018; Wilkinson et al. 2019) or phosphorescence (Dunning et al. 2018). But unlike fluorescence, a phosphorescent material does not immediately re-emit the radiation it absorbs, and I observed no delayed light emission in bills. I suppose it to be the same process among the Fraterculinae subfamily.
I prove the occurrence of fluorescence in Fraterculinae, theorized by previous researchers (Wails et al. 2017; Dunning et al. 2018; Wilkinson et al. 2019) and connect it with close phylogenetic relationship within the fluorescent billed Alcidae. Also fluorescent glow revealed in tuffs of Tufted puffin (fig. 1).
Fig. 1. Area of fluorescent glow in: 1 — Horned puffin bill; 2 — Tufted puffin bill; 3 — Tufted puffin tuffs. ' Temperature' parameter in Adobe Photoshop Camera Raw set up to maximum (50000) to make glow more visible on the picture. Рис. 1. Зона флуоресцентного свечения: 1 — клюва ипатки; 2 — клюва топорка; 3 — заглазничных пучков топорка. Параметр 'температура' установлен на максимум (50000), чтобы сделать свечение
более видимым на изображении.
Kuroda (1954, 1955 - cit. by: Watada et al. 1987) suggested ostelogi-cally close relatedness among the three puffins. Strauch (1985) found Ce-rorhinca to be a puffin. He suggested that the puffins are a monophyletic group that includes Cerorhinca.
Monophyly of this group is also supported by several molecular studies (Watada et al. 1987; Friesen et al. 1996; Thomas et al. 2004; Baker et al. 2007; Pereira, Baker 2008; Mayr 2011). Watada et al. (1987) also proposed inclusion Cerorhinca in Fratercula.
Aethia and Ptychoramphus are closest relatives to puffins both in morphological and in molecular studies. All of them except Ptychoramphus aleuticus have certain degree of bill fluorescence (fig. 2).
Fig. 2 Proposed phylogenetic relationships for the Fraterculinae with geological timescale indicated in the bottom (by Pereira, Baker 2008, fig. 5). Black lines to the right of species names indicate presence of fluorescence; color of the circle near the line indicates the color of glow; red dots indicates fluorescence described in this article; red question mark indicates presence of glow with yet unknown nature. Рис. 2. Схема филогенетических отношений в подсемействе Fraterculinae с геологической временной шкалой (внизу), предложенная Pereira, Baker (2008, рис. 5). Чёрные линии справа от видовых названий говорят о присутствии флуоресценции в группе; цвет кружка возле чёрной линии соответствует цвету свечения; красные точки возле видового названия обозначают факт флуоресценции, впервые описанный в этой статье; красные знаки вопроса возле видового названия говорят о наличии свечения
с пока ещё неизвестной природой.
Bill fluorescence might be unique feature to the common ancestor of this group. Loss of that feature in Ptychoramphus and reduction in 3 species of Aethia and Cerorhinca could be secondary phenomenon.
There is significant difference in fluorescent bill area between two sexes in Horned puffin (t-test: t = 2,83; P = 0,01; valid n: m = 13, f = 9, fig. 3). And bill size between sexes differs only by 5.34% (males in summer: n = 14, mean = 50.6; females in summer: n = 12, mean = 47.9. Exemplars from the same collection) (Скокова 1990; Харитонов 1990). It indicates high possibility for this feature to play role in the process of sexual selection.
There is significant correlation between the time passed after bird death and fluorescent bill area (r = -0.5110; P = 0.00009) (fig. 4). But when
only males were left for this analysis correlation became insignificant but still tends to be the same (r = -0.2399; P = 0.3083). That could be because of properties of male's bills (it tend to fade slower with time than of females) or because of lack of birds collected recently.
Fig. 3. Differences in fluorescent area (cm2 pixel analog) between sexes in Horned puffin. Рис. 3. Различия в измеряемой площади флуоресценции (аналог пикселей в см2) между полами у ипатки (m — самцы; f— самки).
Fig. 4. Correlation between the time passed after bird death (years) and fluorescent bill area
(cm2 pixel analog) in Horned puffin. Рис. 4. Корреляция между количеством времени прошедшим с момента смерти птицы (число лет) и измеряемой площади флуоресценции (аналог пикселей в см2) у ипатки.
The same trait was found in Tufted puffin (fig. 5). Exemplars that were collected in recent 12 years were excluded from analysis because of insufficient data sampling and big gap between more earlier collected birds. Juvenile and subadult birds were also excluded from analysis.
3,0 2,5 2,0
TO
2 1,5
<
1,0 0,5 0,0
40 50 60 70 80 90 100 110 120
Death:Area: r = -0,6207; p = 0,0012; r* = 0,3853 Death
Fig. 5. Correlation between the time passed after bird death (years) and fluorescent bill area
(cm2 pixel analog) in Tufted puffin.
Рис. 5. Корреляция между временем, прошедшим с момента смерти птицы (число лет) и измеряемой площади флуоресценции (аналог пикселей в см2) у топорка.
The more time carcass spends in collection, the less intense fluorescent bill coloration becomes. It could be proof for the presence of specific fluorescent pigment, accumulated in certain parts of bill. However, it needs further investigation and more specific testing.
There are significant differences in fluorescent bill area between age groups in Tufted puffin (fig. 6). It was possible to determine age of the bird by the bill structure among Tufted puffins: bird considered adult if 2 or 3 vertical bill strikes were visible; subadult if 1 or no strikes were visible; juvenile if bill was slender and had very thin ramphotheca.
Age differences of bill size and in fluorescent area could be indicator of adultness and readiness to reproduction.
I couldn't assess sex differences in bills of Tufted puffin because there were not enough exemplars with determined sex to provide statistically reliable analysis. Nevertheless, I could gently presume same differences as in Horned puffin based on diurnal lifestyle, similarities in behavior, morphology and borrow nesting of these species.
Fig. 6. Differences in fluorescent area (cm2 pixel analog) between different ages in Tufted puffin. Рис. 6. Различия в измеряемой площади флуоресценции (аналог пикселей в см2) между разными возрастными группами топорков (n: ad = 29; sad = 6; juv = 7).
Bright orange-red fluorescence of bill on some exemplars of Crested auklet is still visible. I observed very low light emission (fluorescence?) in bills of all other Aethia. Weak orange-red glow was visible by naked eye and it became visible on photo only if 'Temperature' parameter in Adobe Photoshop Camera Raw was set up to max (50000). But the nature of that phenomenon is unclear.
Rhinoceros auklets exemplars demonstrated almost no visible light emission and I found none of that in carcasses of Atlantic puffins and Cassin's auklet. It could be due to very low content of fluorescent agent and it rapid fading with time in bills of these species.
Wilkinson et al. (2019) found no evidence for a sex-specific difference in the amount of bill fluorescence. Absence of differences in the amount of fluorescence displayed between the sexes in Rhinoceros Auklet could be due to the nocturnal lifestyle of that species. And it could also be secondary degradation of fluorescent parts of bill along with secondary despecial-ization of Rhinoceros Auklet as it proposed by Badikova and Dzerzhinsky (Бадикова, Дзержинский 2014).
To better understanding sex differences in bill fluorescence, experiments with live birds is needed. Still the precise function of bill luminescence in Puffins is still currently unknown and needs further exploration.
I thank Y.A.Red'kin at the Zoological Museum of Moscow University for providing access to museum collection. Anna Gorshkova for presenting me a scull of Tufted puffin in which I first observed fluorescence in that species.
Флуоресценция в подсемействе Fraterculinae
Г.Ю.Евтух
Ранее фотолюминесценция в клювах птиц была описана на примере большой конюги Aethia cristatella (Wails et al. 2017), атлантического тупика Fratercula arctica (Dunning et al. 2018) и тупика-носорога Cerorhinca monocerata (Wilkinson et al. 2019). В настоящей работе сообщается об обнаружении фотолюминесценции у двух других представителей группы Fraterculini: ипатки Fratercula corniculata и топорка Fratercula cirrhata. Флуоресцентные паттерны окраски рамфотеки очень похожи среди Fraterculini. В этой группе свечение клюва наблюдается как в ринотеке, так и в гнатотеке ближе к основанию клюва. Также флуоресценция обнаружена в пучках перьев над глазами у топорка. Возрастные различия во флуоресцентной области клюва выявлены у топорка и половые различия выявлены у ипатки. Выцветание флуоресцентной окраски со временем может свидетельствовать о наличии специфического флуоресцентного пигмента. Красно-оранжевое излучение в клювах Aethia нуждается в более подробном изучении.
References
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ISSN 0869-4362
Русский орнитологический журнал 2019, Том 28, Экспресс-выпуск 1768: 2142-2150
О редких видах птиц на Вишерском Урале
В.А.Колбин
Василий Анфимович Колбин. ФГБУ «Государственный заповедник «Вишерский».
Ул. Гагарина, д. 36Б, г. Красновишерск, Пермский край, 618590, Россия. E-mail: kgularis@mail.ru
Поступила в редакцию 16 апреля 2019
Заповедник «Вишерский» находится на северо-востоке Пермского края, имеет площадь 241.2 тыс. га, что составляет около 16% площади Красновишерского района, данную территорию в последнее время ещё принято называть Вишерским Уралом.
Особенностью Вишерского заповедника является его близкое соседство с другими заповедниками Урала — Печоро-Илычским и «Денеж-кин Камень». Так, от северной границы Вишерского заповедника до Печоро-Илычского заповедника — около 50 км, а от юго-восточной границы до заповедника «Денежкин Камень» — около 30 км. Поэтому я не ограничивался рамками Красновишерского района, а по мере возмож-
