Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine
The second lower molars of the red squirrel Sciurus vulgaris from different regions of Ukraine were examined in order to search for additional features to study the variability and clarify the subspecies status of its individual populations. Generally accepted methods were used to study the enamel u...
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irk-123456789-1651872020-02-13T01:27:27Z Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine Rekovets, L. Kovalchuk, O. Demeshkant, V. Shevchenko, L. Морфологія та мінливість The second lower molars of the red squirrel Sciurus vulgaris from different regions of Ukraine were examined in order to search for additional features to study the variability and clarify the subspecies status of its individual populations. Generally accepted methods were used to study the enamel ultrastructure. It is established that the tooth enamel of the red squirrel has a layered structure and is represented by different types (radial, HSB and PLEX), which are also characteristic for other rodent species. The arrangement of crystalline prisms of the radial layer in the IPM matrix is the main distinguishing feature of the morphological variability of enamel on main tooth conids. In various regional populations of the species, they act as an indicator of the adaptability of the teeth and their functionality as a single structure. This was reflected in differences in the thickness ratio of the radial layer and HSB, especially between the metaconid and the entoconid. The development of HSB is usually associated with greater functional load. Squirrel populations in the northern part of Ukraine have a relatively thick HSB layer, while those from central and southern parts of the country have a more strongly developed radial layer. According to these features, the Crimean populations are close to those from southern Ukraine and slightly differ from the Altai subspecies Sciurus vulgaris exalbidus, which was introduced into the Crimea in the first half of XX century. It is assumed that the enamel ultrastructure as a morphological character has changed in the process of adaptation of squirrels to a new environment. The distinguishing character of the enamel structure of Altai populations of the Teleut squirrel is that prisms do not fill cells of the radial layer on the hypoconid and protoconid. The tooth enamel ultrastructure of the Eurasian red squirrel cannot be an independent morphological character for their intraspecific differentiation. However, it can be successfully used in combination with other characters (e.g., fur coloration, craniometrical data), as well as the results of special molecular studies.. Досліджували корінні зуби (нижні м2) вивірки звичайної Sciurus vulgaris різних регіонів України з метою пошуку додаткових ознак для вивчення мінливості і уточнення підвидового статусу окремих популяцій. Використано загальноприйняті методики вивчення ультраструктури емалі зубів. Встановлено, що емаль зубів цього виду має шарувату структуру і представлена різними типами (радіальна, HSB i PLEX), які властиві також іншим видам гризунів. Особливості розміщення кристалічних призм радіального шару в матриці IPМ є основними ознаками мінливості морфології емалі, особливо на основних конідах зубів. У локальних популяціях виду з різних регіонів структура емалі є подібною і виступає показником адаптивності зубів як єдиної функціональної структури. Певною мірою така мінливість відбилася на відмінностях у співвідношенні товщини радіального шару і HSB, особливо між метаконідом та ентоконідом. Розвиток HSB, як правило, пов’язаний із виконанням більшого функціонального навантаження. Популяції північної частини України мають порівняно товстий шар HSB, а центральної та південної частини – більш розвинений радіальний шар. Кримські популяції за цими показниками близькі до південноукраїнських і відрізняються від алтайського підвиду S. vulgaris exalbidus, який був інтродукований до Криму в першій половині ХХ століття. Висловлено припущення, що ультраструктура емалі як морфологічна ознака зазнала змін у процесі адаптації вивірок до нових умов. Відмінною рисою структури емалі вивірки з алтайської популяції є те, що чарунки радіального шару на гіпо- та протоконіді не заповнені призмами. Ультраструктура емалі зубів вивірки не може розглядатися у якості незалежної морфологічної ознаки для внутрішньовидової диференціації. Водночас, вона може бути застосована у поєднанні з забарвленням хутра, краніометричними даними, а також результатами молекулярних досліджень. 2019 Article Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine / L. Rekovets, O. Kovalchuk, V. Demeshkant, L. Shevchenko // Theriologia Ukrainica. — 2019. — Т. 17. — С. 55–63. — Бібліогр.: 25 назв. — англ. 2616-7379 DOI: http://doi.org/10.15407/pts2019.17.055 http://dspace.nbuv.gov.ua/handle/123456789/165187 en Theriologia Ukrainica Національний науково-природничий музей НАН України |
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Морфологія та мінливість Морфологія та мінливість |
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Морфологія та мінливість Морфологія та мінливість Rekovets, L. Kovalchuk, O. Demeshkant, V. Shevchenko, L. Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine Theriologia Ukrainica |
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The second lower molars of the red squirrel Sciurus vulgaris from different regions of Ukraine were examined in order to search for additional features to study the variability and clarify the subspecies status of its individual populations. Generally accepted methods were used to study the enamel ultrastructure. It is established that the tooth enamel of the red squirrel has a layered structure and is represented by different types (radial, HSB and PLEX), which are also characteristic for other rodent species. The arrangement of crystalline prisms of the radial layer in the IPM matrix is the main distinguishing feature of the morphological variability of enamel on main tooth conids. In various regional populations of the species, they act as an indicator of the adaptability of the teeth and their functionality as a single structure. This was reflected in differences in the thickness ratio of the radial layer and HSB, especially between the metaconid and the entoconid. The development of HSB is usually associated with greater functional load. Squirrel populations in the northern part of Ukraine have a relatively thick HSB layer, while those from central and southern parts of the country have a more strongly developed radial layer. According to these features, the Crimean populations are close to those from southern Ukraine and slightly differ from the Altai subspecies Sciurus vulgaris exalbidus, which was introduced into the Crimea in the first half of XX century. It is assumed that the enamel ultrastructure as a morphological character has changed in the process of adaptation of squirrels to a new environment. The distinguishing character of the enamel structure of Altai populations of the Teleut squirrel is that prisms do not fill cells of the radial layer on the hypoconid and protoconid. The tooth enamel ultrastructure of the Eurasian red squirrel cannot be an independent morphological character for their intraspecific differentiation. However, it can be successfully used in combination with other characters (e.g., fur coloration, craniometrical data), as well as the results of special molecular studies.. |
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Rekovets, L. Kovalchuk, O. Demeshkant, V. Shevchenko, L. |
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Rekovets, L. Kovalchuk, O. Demeshkant, V. Shevchenko, L. |
| author_sort |
Rekovets, L. |
| title |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine |
| title_short |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine |
| title_full |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine |
| title_fullStr |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine |
| title_full_unstemmed |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine |
| title_sort |
enamel ultrastructure of lower molars of the red squirrel sciurus vulgaris (mammalia, rodentia) from different populations in ukraine |
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Національний науково-природничий музей НАН України |
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2019 |
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Морфологія та мінливість |
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http://dspace.nbuv.gov.ua/handle/123456789/165187 |
| citation_txt |
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from different populations in Ukraine / L. Rekovets, O. Kovalchuk, V. Demeshkant, L. Shevchenko // Theriologia Ukrainica. — 2019. — Т. 17. — С. 55–63. — Бібліогр.: 25 назв. — англ. |
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Theriologia Ukrainica |
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| fulltext |
Theriologia Ukrainica, 17: 55–63 (2019)
http://doi.org/10.15407/pts2019.17.055
ENAMEL ULTRASTRUCTURE OF LOWER MOLARS OF THE RED SQUIRREL
SCIURUS VULGARIS (MAMMALIA, RODENTIA) FROM DIFFERENT
POPULATIONS IN UKRAINE
Leonid Rekovets1, Oleksandr Kovalchuk2, Vitalii Demeshkant1, Liudmila Shevchenko2
1 Wroclaw University of Environmental and Life Sciences (Wroclaw, Poland)
2 National Museum of Natural History, National Academy of Sciences of Ukraine (Kyiv, Ukraine)
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia) from
different populations in Ukraine. — L. Rekovets, O. Kovalchuk, V. Demeshkant, L. Shevchenko. — The
second lower molars of the red squirrel Sciurus vulgaris from different regions of Ukraine were examined in or-
der to search for additional features to study the variability and clarify the subspecies status of its individual
populations. Generally accepted methods were used to study the enamel ultrastructure. It is established that the
tooth enamel of the red squirrel has a layered structure and is represented by different types (radial, HSB and
PLEX), which are also characteristic for other rodent species. The arrangement of crystalline prisms of the ra-
dial layer in the IPM matrix is the main distinguishing feature of the morphological variability of enamel on
main tooth conids. In various regional populations of the species, they act as an indicator of the adaptability of
the teeth and their functionality as a single structure. This was reflected in differences in the thickness ratio of
the radial layer and HSB, especially between the metaconid and the entoconid. The development of HSB is usu-
ally associated with greater functional load. Squirrel populations in the northern part of Ukraine have a rela-
tively thick HSB layer, while those from central and southern parts of the country have a more strongly devel-
oped radial layer. According to these features, the Crimean populations are close to those from southern Ukraine
and slightly differ from the Altai subspecies Sciurus vulgaris exalbidus, which was introduced into the Crimea
in the first half of XX century. It is assumed that the enamel ultrastructure as a morphological character has
changed in the process of adaptation of squirrels to a new environment. The distinguishing character of the
enamel structure of Altai populations of the Teleut squirrel is that prisms do not fill cells of the radial layer on
the hypoconid and protoconid. The tooth enamel ultrastructure of the Eurasian red squirrel cannot be an inde-
pendent morphological character for their intraspecific differentiation. However, it can be successfully used in
combination with other characters (e.g., fur coloration, craniometrical data), as well as the results of special mo-
lecular studies.
Key words: Sciurus vulgaris, taxonomy, teeth, enamel, prisms, Ukraine.
Cor respondence to : L. Rekovets; Wroclaw University of Environmental and Life Sciences, Chelmonskiego
St., 38c, Wroclaw, 51-630 Poland; e-mail: leonid.rekovets@upwr.edu.pl: orcid: 0000-0001-9934-7095
Introduction
The Eurasian red squirrel Sciurus vulgaris Linnaeus, 1758 is a common species in the fauna of
Ukraine (Zagorodniuk, 2006, 2009). However, it is still inadequately studied in environmental and
taxonomical aspects (Mygulin, 1938; Tsjupka, 2012). Studies concerning the taxonomic structure of
the red squirrel were mainly focused on their intraspecific variation (Zizda, 2008).
The opinions about the taxonomic status of geographic forms remain controversial (Sidorowicz,
1971; Lurtz et al., 2005; Amori et al., 2014). From two to six squirrel subspecies are considered for
the territory of Ukraine. Among them, three are the most reliable — S. vulgaris vulgaris L. (inhabit-
ing the lowland forests), the Carpathian subspecies S. vulgaris carpathicus Pietruski, 1853 (Ukrain-
ian Carpathians) and the Teleut squirrel S. vulgaris exalbidus Pallas, 1778 brought to the Crimea
from the Altai in the 1940s (Puzanov, 1959; Dulitskaya et al., 1990; Zagorodniuk, 2006). The last
clearly separated subspecies is of interest in terms of morphological changes during their adaptation
to a new environment — mountain forests of the southern Crimea (Dulitsky, Dulitska, 2006).
According to the most recent data (Zizda, 2008, 2018), at least four color morphs (or subspe-
cies) of Sciurus vulgaris were identified for the territory of Ukraine: Sciurus vulgaris carpathicus
Leonid Rekovets, Oleksandr Kovalchuk, Vitalii Demeshkant, Liudmila Shevchenko 56
Pietruski, 1853 (the darkest morph from the Carpathian highlands), S. v. fuscoater Altman, 1855
(brown morph from the Carpathian region; Barkaszi, Zagorodniuk, 2016), S. v. kessleri Migulin,
1928 (red morph of the northern part of Right-Bank Ukraine), S. v. ukrainicus Migulin, 1928 (light-
red squirrel of Right-Bank Ukraine). The animals from the Crimean population of the Teleut squirrel
(S. v. exalbidus) are similar in fur coloration to S. v. ukrainicus (Zizda, 2018).
Craniometric and genetic studies (Zizda, 2008; Bilokon et al., 2014; Zizda, 2018) did not reveal
any significant differences between the studied populations of this species in Ukraine, and molecular
data aiming to solve this issue are currently absent. Our study results on the enamel ultrastructure of
Sciurus vulgaris from different regions, corresponding to different colored morphs or subspecies,
were aimed to identify possible local variations in the structure of their teeth enamel.
It is known that the structure of the tooth enamel is strongly correlated with their function and,
therefore, with environmental conditions. The enamel structure has evolved in parallel with the teeth
function and morphology (Koenigswald, 1997; Rekovets, Kovalchuk, 2017). An approach for the
study of enamel ultrastructure was successfully used to establish family relationships between the
relatively close groups of animals and for the creation of phylogenetic schemes (Koenigswald, 1996;
Martin, 1997). It is believed that the tooth enamel has a complicated structure and consists of indi-
vidual layers. Its basis is a relatively primitive (radial) enamel type; other layers are represented by
the tangential and lamellar types (Koenigswald, 1980). Besides, additional enamel types (e.g.,
Hunter-Schreger bands in various modifications, lemming enamel, PLEX, etc.) were also identified
(Koenigswald, 1990; Koenigswald, Sander, 1997). Each enamel layer is composed of prisms, laying
in various directions on the interprismatic matrix (IPM).
Relative position and inclination of prisms, and the IPM (linear, reticular, weave, tilted) indi-
cates the level of evolutionary advancement of each enamel layer (progressive and primitive enamel
types), as well as the nature of adaptation and the role of enamel as a functional structure (Rekovets,
Kovalchuk, 2017). It allowed us to characterize the enamel structure in teeth of different taxa in con-
nection with their teeth function (Rekovets, Nowakowski, 2013; Popova, 2016; Rabiniak et al.,
2017) as well as to justify its taxonomic significance as a diagnostic character (Koenigswald, 1990).
Material and methods
Thirteen second lower molars (m2) of adult, wild-caught squirrels from different regions of
Ukraine were used for this study: Volyn (n = 1), Zhytomyr (1), Poltava (1), Sumy (1), Cherkasy (1),
Chernihiv regions (2), as well as the Ukrainian Carpathians (2), Crimea (2), and Altai (n = 2). Our
previous studies (L. Rekovets, unpublished data) showed the absence of any reliable differences in
the enamel structure of other molars and incisors of the Eurasian red squirrel from different popula-
tions; therefore, we focused on a detailed investigation of m2 ultrastructure.
The preparation of the teeth for the analysis follows von Koenigswald (1980). The method was
slightly modified by omitting the cut with a diamond saw (IsoMet® Low Speed Saw), which can
damage the tooth. The specimens were ground immediately after embedding them in epoxy resin
(Epoxy Embedding Medium kit — 45359 Sigma-Aldrich GmbH). The quality of grinding was con-
trolled under stereomicroscope. The samples were rinsed for 10 seconds in a 5% HCl solution fol-
lowed by ethanol, and placed for 30 seconds in ultrasonic bath to remove the dust. The samples were
analyzed using a scanning electron microscope (Zeiss LEO 435) in the Laboratory of Electron Mi-
croscopy, Wrocław University of Environmental and Life Sciences (Poland).
The number of examined tooth areas depends on the regions of interest and the quality of grind-
ing. The images were taken at different magnifications. Preparation and photography of examined
samples were performed in Wrocław University of Environmental and Life Sciences. The paper
presents the figures that are compared. In some cases, depending on the level of the teeth wear, the
enamel at the talonid was also investigated (Fig. 1). The enamel ultrastructure was studied on stan-
dardized cross sections, i.e. in parallel to the occlusal surface, which is usually taken in such studies
for other groups of animals. It should be noted that Koenigswald (2004) used the vertical (longitudi-
nal) sections of the teeth. The scheme and the names of all elements for the squirrel teeth were es-
sentially taken from the specified work (Fig. 1).
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia)...
57
Abbreviations in the text and f igs : HSB, Hunter-
Schreger Bands; EDJ, enamel-dentine junction; IPM, inter-
prismatic matrix; OES, outer enamel surface; PLEX, prism-
less external enamel; R, radial enamel type.
Fig. 1. Scheme of placement of lower molar elements in Sciuridae.
Studied places around the tooth perimeter are marked by rectangles.
Рис. 1. Схема розміщення, позначення і назви елементів нижніх
корінних зубів у Sciuridae. Прямокутниками виділені місця дослі-
дження емалі по периметру зубa.
Results of the study
There are no significant differences in the enamel ultrastructure of molars in the Eurasian red
squirrel on their horizontal and vertical sections. The tooth enamel of this species has a layered
structure and consists of IPM, crystalline prisms, radial layer R (= portio externa according to
Koenigswald, 1990, 2004) and relatively coarse multiserial HSB layer (= portio interna after
Koenigswald, 1990, 2004). This enamel type was called as S-type (Koenigswald, Sander, 1997). It
was formed from the more primitive enamel, which is typical for Paleogene rodents. The S-type
enamel of Sciurus vulgaris is represented mainly by the radial type. The HSB layer is coarse and can
be placed in different places with a total thickness of the enamel layer. The enamel ultrastructure of
lower molars (m2) of Sciurus vulgaris from different parts of Ukraine is described in detail below.
Ukrainian Carpathians
The HSB layer of m2 consists of coarse structures (except those at the mesostylid), in contrast
to other comparable populations. It takes 30 % (up to 90 % at the entoconid-mesostylid) of the total
enamel thickness (Fig. 2 c, e, f) along the tooth perimeter. Cells of the radial layer are not densely
filled by small prisms (Fig. 2 d). The talonid enamel consists only of the reticular IPM with prisms.
The boundary between enamel layers is somewhat blurred. Moreover, the transitional layer is com-
posed by the IPM with ellipsoid cells filled by prisms. This character is common for all studied
populations. The enamel structure at the entoconid of m2 in squirrels from the Carpathian population
resembles the pauciserial type, i.e. alternation of prisms in the radial and HSB layers (Fig. 2 a, b, e).
It is similar to those in individuals from Zhytomyr and Sumy regions, as well as those from Altai.
Volyn region
Near 90 % of the enamel thickness around the tooth perimeter is composed of coarse HSB
structures. The presence of rare prisms in small IPM cells of the radial layer and uncertain structures
such as PLEX is noted at the posterior tooth wall, near the EDJ (Fig. 3 a). These characters distin-
guish this population from the others and may be associated with greater tooth erasure. The radial
layer at the mesostylid consists of structures, sloping to the EDJ and resembling the HSB (Fig. 3 b).
Zhytomyr region
The radial layer with prisms in the IPM cells is well-developed. The cells are more ellipsoid in
shape toward the middle part of the enamel layer. The HSB is located near the OES and forms a
ridge structure together with the radial enamel. This feature relates the population from Zhytomyr
region to those from Sumy region and the Carpathians, and distinguishes it from the others
(Fig. 4 a). The enamel of the lingual tooth wall is composed only of coarse HSB, especially at the
mesostylid (Fig. 4 b). Unusual ribbed HSB structure at the hypoconid and protoconid is associated
with irregular vertical deflection of the radial structures to the OES. It is visible in cross-sections as
rings (near the EDJ) or ellipses (closer to the middle layer). This ribbed structure is not characteristic
for other populations, except those from the Carpathians and Sumy region.
Leonid Rekovets, Oleksandr Kovalchuk, Vitalii Demeshkant, Liudmila Shevchenko 58
a b c
d e f
Fig. 2. Ultrastructure of the m2 enamel of Sciurus vulgaris from the Ukrainian Carpathians: a — protoconid, b —
entoconid, c — mesostylid, d — posterolophid, e — hypoconid, f — anterolophid.
Рис. 2. Ультраструктура емалі м2 Sciurus vulgaris з регіону Українських Карпат: a — протоконід, b —
ентоконід, c — мезостилід, d — постеролофід, e — гіпоконід, f — антеролофід.
a b
Fig. 3. Ultrastructure of the m2 enamel of Sciurus vulgaris from Volyn region: a — protoconid, b — mesostylid.
Рис. 3. Ультраструктура емалі м2 Sciurus vulgaris з Волинської області: a — протоконід, b — мезостилід.
a b
Fig. 4. Ultrastructure of the m2 enamel of Sciurus vulgaris from Zhytomyr region: a — protoconid, b — mesostylid.
Рис. 4. Ультраструктура емалі м2 Sciurus vulgaris з Житомирської області: a — протоконід, b — мезостилід.
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia)...
59
a b
Fig. 5. Ultrastructure of the m2 enamel of Sciurus vulgaris from Sumy region: a — hypoconid, b — anterolophid.
Рис. 5. Ультраструктура емалі м2 Sciurus vulgaris із Сумської області: a — гіпоконід, b — антеролофід.
Sumy region
The structure of the tooth enamel is identical to those from the above-mentioned regions. Some
differences (except the ribbing) are in the radial layer that is filled by prisms at the anterior and pos-
terior surfaces (anterolophid, posterolophid), as well as on the lingual side (entoconid — metaconid).
The HSB structure is wavy. It occupies near 50 % of the total thickness of the tooth enamel
(Fig. 5 a). For comparison, the HSB layer of m2 in the specimens from Zhytomyr comprises from 80
to 100 % of the enamel thickness. The structure of the radial layer consists of densely packed fine
prisms in the elongated IPM cells. The boundaries between cells are not clearly visible (Fig. 5 b).
Chernihiv region
The enamel has a structure similar to the previous one, but ribbing (i.e. interlace of the R and
HSB) is absent. The radial enamel is well-developed at the hypoconid (Fig. 6 a). Cells of this layer
form the prisms disposed at an acute angle to the EDJ. The HSB is undulating in structure (Fig. 6 b).
The inner enamel ring consists predominantly of the radial layer with prisms in the IPM cells. The
HSB layer is very poorly represented.
Cherkasy region
The enamel is similar to the previous one. It is represented by the radial layer with prisms at the
hypoconid. The HSB has an undulating structure and occupies about 50 % of the total enamel thick-
ness. On other parts of the tooth, including the lingual one, the HSB comprises up to 80 %. Fine
prisms of the radial layer resemble those in squirrels from Sumy region. They densely fill distinct
ellipsoid cells of the IPM (Fig. 7).
a b
Fig. 6. Ultrastructure of the m2 enamel of Sciurus vulgaris from Chernihiv region: a — protoconid, b — entoconid.
Рис. 6. Ультраструктура емалі м2 Sciurus vulgaris із Чернігівської області: a — протоконід, b — ентоконід.
Leonid Rekovets, Oleksandr Kovalchuk, Vitalii Demeshkant, Liudmila Shevchenko 60
Poltava region
The tooth enamel in representatives of this population somewhat differs from those in other
studied populations. The HSB at the hypoconid occupies only 20 % (radial layer — 80 %). At the
same time, this layer is up to 80 % of the total enamel thickness at the protoconid (Fig. 8 a), an-
terolophid and posterolophid. The HSB is up to 100 % at the mesostylid, where the presence of
PLEX enamel is possible (Fig. 8 b). It should be noted that squirrels from this region (and the adja-
cent part of the Sumy region) differ considerably in color, and some morphological characters from
other lowland populations within Ukraine. This was the basis for Mygulin (1938) to identify this
population as a separate subspecies S. v. ukrainicus.
OES HSB
R
EDJ
a b
Fig. 7. Ultrastructure of the m2 enamel of Sciurus vulgaris from Cherkasy region: a — hypoconid, b — metaconid.
Рис. 7. Ультраструктура емалі м2 Sciurus vulgaris із Черкаської області: a — гіпоконід, b — метаконід.
a b
Fig. 8. Ultrastructure of the m2 enamel of Sciurus vulgaris from Poltava region: a — posterolophid, b — mesostylid.
Рис. 8. Ультраструктура емалі м2 Sciurus vulgaris із Полтавської області: a — постеролофід, b — мезостилід.
a b
Fig. 9. Ultrastructure of the m2 enamel of Sciurus vulgaris from the Crimean Peninsula: a — hypoconid, b — talonid.
Рис. 9. Ультраструктура емалі м2 Sciurus vulgaris із Кримського півострова: a — гіпоконід, b — талонід.
Enamel ultrastructure of lower molars of the red squirrel Sciurus vulgaris (Mammalia, Rodentia)...
61
a b
c d
Fig. 10. Ultrastructure of the m2 enamel of Sciurus vulgaris from the Altai: a — protoconid, b — protoconid,
c — protoconid, d — entoconid.
Рис. 10. Ультраструктура емалі м2 Sciurus vulgaris з території Алтаю: a — протоконід, b — протоконід,
c — протоконід, d — ентоконід.
The Crimean Peninsula
The radial enamel at the hypoconid has very small IPM cells filled by prisms ellipsoid in the
middle part. It depends on the degree of vertical deviation of the IPM structures (Fig. 9 a). The HSB
has an undulating structure and comprises up to 70 % of the total enamel thickness. On the other
tooth surfaces this layer can take up to 50 % (Fig. 9 b). The HSB of the second, more erased, m2 has
a wavy structure and occupies 80 % of the enamel thickness, and up to 100 % at the lingual side.
Altai
Aboriginal population of S. v. exalbidus is of interest for comparison. On the labial side of the
tooth (hypoconid — protoconid) the radial enamel comprises up to 30 % of the total enamel thick-
ness (HSB layer — 70 %) and small cells in the IPM are filled by prisms only near the EDJ.
Other cells of the radial layer, particularly at the hypoconid and protoconid, lack prisms (Fig. 10
a, b). The anterior and posterior tooth walls (antero- and posterolophids) have about 50 % thickness
of the HSB and the radial layer. The talonid enamel has not yielded the HSB. Small cells of the ra-
dial enamel at the tooth perimeter (except the hypo- and protoconids) are filled by prisms. The
enamel at the lingual side (metaconid–entoconid section) is composed only of HSB (Fig. 10 c, d).
Discussion and conclusions
Obtained data on the tooth enamel ultrastructure for Sciurus vulgaris from different populations
of Ukraine and the Altai territory of Russia, as well as the results of their comparison with previ-
ously published data (Koenigswald, 1990, 2004) indicate that there is no significant difference
among these populations. The enamel ultrastructure is almost identical to each other.
Leonid Rekovets, Oleksandr Kovalchuk, Vitalii Demeshkant, Liudmila Shevchenko 62
It is established that the entire perimeter of the tooth enamel is mainly composed of two enamel
types — radial (R) and HSB. They are formed mostly on the IPM whose cells are almost always
filled by crystalline prisms. According to Koenigswald (2004), this structure has the S-type enamel.
It is characteristic for the representatives of Sciuromorpha and Sciuravidae with low tooth crowns. It
is characterized by a relatively strong development of the HSB. The latter may be located near the
EDJ or the OES, or inside the radial layer. In the samples studied here, the HSB layer is always lo-
cated near the OES. Other distinguishing characters include the different thickness of the HSB
around the tooth perimeter (from 30 to 100 %) and its location near the OES.
This character probably depends on the individual age, i.e. from the level of the teeth wear. In
addition, the enamel of talonid structures consists only of the radial layer and its IPM is always filled
with prisms, except for the samples from the Ukrainian Carpathians. More undulating structure of
the HSB is characteristic for the populations from Cherkasy region, the Crimea and the Carpathians.
The specificity of alternating layers of the radial enamel and HSB (grooved structure) in populations
from Zhytomyr, Sumy, as well as the Carpathians should be emphasized.
The squirrels of all studied populations could be divided into three groups based on their enamel
ultrastructure: (1) Carpathians, Zhytomyr and Sumy — characterized by a distinct ridge structures
(alternation of the R and HSB); (2) Volyn, Chernihiv, Cherkasy, Poltava and the Crimea — the ra-
dial layer is located near the EDJ, and HSB near the OES; (3) Altai — the absence of prisms in the
radial layer, especially on the protoconid and hypoconid.
The proportion of HSB can be increased up to 100 % of the enamel layer during the teeth wear
in this species (Figs 6 b, 8 b). The same applies to the undulation and proportion of the radial
enamel. Zhytomyr, Sumy and Carpathian populations are the most different among the compared
groups. These populations have a ribbed HSB structure (alternating of the radial layer and HSB).
The Teleut squirrels (S. v. exalbidus) of the Crimean population seem to be closer in their
enamel structure to the populations of the Ukrainian plain than to those from the Altai. Such conclu-
sion is further supported by the complex of craniometric characters (L. Shevchenko, unpubl. data). A
significant increase in skull height at the level of M1 in the Teleut squirrels of the Crimean popula-
tion was reported by Dulitsky and Dulitska (2006). Such an increase of this feature is beyond the
variability range of S. v. exalbidus, and even was a basis for the recognition of a new subspecies —
S. v. puzanovi (Dulitskaya et al., 1990). As it was noted by Dulitsky and Dulitska (2006: 73), “the
ecological status of the squirrel in the Crimea has changed, but the systematic status requires further
clarification”. The enamel ultrastructure as a morphological character has also changed in the proc-
ess of adaptation of these squirrels to new conditions in the Crimea. The distinguishing character of
the enamel structure of Altai populations of the Teleut squirrel (from the Crimean Peninsula) is that
the cells of the radial layer on the hypoconid and protoconid are not filled with prisms.
It should be noted that the tooth enamel ultrastructure of the Eurasian red squirrel cannot be a
reliable morphological character for their intraspecific differentiation. However, it can be success-
fully used in combination with other data — fur coloration, craniometrical data as well as special
molecular studies.
Acknowledgements
The authors are thankful to M. Sinitsa and an anonymous reviewer for their constructive com-
ments. We express our thanks to I. Zagorodniuk for his effective management of our submission.
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