Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae)
We studied 8 skull and 42 dental characters in nine Myotis species (M. myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. daubentonii, M. brandtii, M. mystacinus) to analyze correlations between hardness of food and skull and dental traits. Contrary to the common bat...
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Інститут зоології ім. І.І. Шмальгаузена НАН України
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| Zitieren: | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) / M. Ghazali, I. Dzeverin // Вестник зоологии. — 2013. — Т. 47, № 1. — С. 73–82. — Бібліогр.: 46 назв. — англ. |
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| author | Ghazali, M. Dzeverin, I. |
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| citation_txt | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) / M. Ghazali, I. Dzeverin // Вестник зоологии. — 2013. — Т. 47, № 1. — С. 73–82. — Бібліогр.: 46 назв. — англ. |
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| description | We studied 8 skull and 42 dental characters in nine Myotis species (M. myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. daubentonii, M. brandtii, M. mystacinus) to analyze correlations between hardness of food and skull and dental traits. Contrary to the common bat pattern, Myotis that are specialized on hard-shelled dietary items tend to have relatively narrow skull and long tooth rows. The dentition of durophagous Myotis is composed by relatively enlarged second and reduced third molars.
Для анализа связи между твердостью пищи и значениями черепных и зубных признаков исследовано 8 черепных и 42 зубных промера у девяти видов ночниц (Myotis myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. daubentonii, M. brandtii, M. mystacinus). Вопреки общим для летучих мышей закономерностям у ночниц, специализированных к поеданию объектов питания с твердыми покровами, выявлена тенденция к сужению черепа и удлинению зубных рядов. В зубном аппарате такие ночницы имеют относительно увеличенные вторые и редуцированные третьи моляры.
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UDC 599.426:[591.431.4+591.471.4+591.53]
CORRELARTIONS BETWEEN HARDNESS
OF FOOD AND CRANIODENTAL TRAITS IN NINE
MYOTIS SPECIES (CHIROPTERA, VESPERTILIONIDAE)
M. Ghazali, I. Dzeverin
Schmalhausen Institute of Zoology, NAS of Ukraine,
vul. B. Khmelnytskogo, 15, Kyiv, 01601 Ukraine
E-mail: ghazali.maria@gmail.com, igordzeverin@gmail.com
Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera,
Vespertilionidae). Ghazali M., Dzeverin I. – We studied 8 skull and 42 dental characters in nine Myotis
species (M. myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. dauben-
tonii, M. brandtii, M. mystacinus) to analyze correlations between hardness of food and skull and dental
traits. Contrary to the common bat pattern, Myotis that are specialized on hard-shelled dietary items tend
to have relatively narrow skull and long tooth rows. The dentition of durophagous Myotis is composed
by relatively enlarged second and reduced third molars.
Ke y wo r d s: Myotis, hardness of food, skull, teeth.
Ñâÿçü ìåæäó òâåðäîñòüþ ïèùè è êðàíèîäåíòàëüíûìè ïðèçíàêàìè äåâÿòè âèäîâ íî÷íèö, Myotis
(Chiroptera, Vespertilionidae). Ãõàçàëè Ì., Äçåâåðèí È. – Äëÿ àíàëèçà ñâÿçè ìåæäó òâåðäîñòüþ ïèùè
è çíà÷åíèÿìè ÷åðåïíûõ è çóáíûõ ïðèçíàêîâ èññëåäîâàíî 8 ÷åðåïíûõ è 42 çóáíûõ ïðîìåðà ó äåâÿ-
òè âèäîâ íî÷íèö (Myotis myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri,
M. daubentonii, M. brandtii, M. mystacinus). Âîïðåêè îáùèì äëÿ ëåòó÷èõ ìûøåé çàêîíîìåðíîñòÿì
ó íî÷íèö, ñïåöèàëèçèðîâàííûõ ê ïîåäàíèþ îáúåêòîâ ïèòàíèÿ ñ òâåðäûìè ïîêðîâàìè, âûÿâëå-
íà òåíäåíöèÿ ê ñóæåíèþ ÷åðåïà è óäëèíåíèþ çóáíûõ ðÿäîâ.  çóáíîì àïïàðàòå òàêèå íî÷íèöû
èìåþò îòíîñèòåëüíî óâåëè÷åííûå âòîðûå è ðåäóöèðîâàííûå òðåòüè ìîëÿðû.
Êëþ÷åâûå ñ ëîâ à: Myotis, òâåðäîñòü ïèùè, ÷åðåï, çóáû.
Introduction
Skull and dental morphologies are in close association with the trophic specializations of most animals.
Dietary adaptations are among the clearest changes that can be traced in fossils. Diversification rates of mam-
mals are connected with diet: herbivores have relatively the highest rates and diversity, carnivores are in between,
and omnivores have the slowest rates and lowest diversity (Price et al., 2012).
Bats are the second largest group in number of species after rodents (Simmons, 2005). They have a vari-
ety of feeding strategies that presumably evolved from an insectivorous bat ancestor (Slaughter, 1970).
Diversification can occur during dietary niche shift, when animals change morphologically and fill new adap-
tive zones, as exemplified by transition from insectivory to frugivory in phyllostomids (Dumont et al., 2011).
Within frugi- and insectivore feeding strategies, minor specializations of the skull, muscles and dentition to soft
and hard objects have been distinguished. Freeman has thoroughly studied the bats from this point of view
(Freeman, 1979; 1981a; 1981b; 1998; 2000). She found that cranial morphology closely correlates with the hard-
ness of food and type of echolocation in bats. Bats that prey mostly on hard-shelled items have strong mus-
cles that allow them to develop a force sufficient to crush those items. Such oral-emitting durophagous bats
usually have reduced number of teeth, high coronoid processes, short faces and wide skulls (Freeman, 1981b;
2000).
Myotis (Chiroptera, Vespertilionidae) species retain the ancestral dental formula (38 teeth with upper third
premolars (P3) being present) and are rather diverse in body size and trophic preferences. They feed on arthro-
pods with variable body size and integumental characteristics (Dietz et al., 2009; see also references in
table 1), and rarely on fish (e. g., M. vivesi: Blood, Clark, 1998). Myotis myotis is the most durophagous among
the European Myotis species. It feeds mostly on Coleoptera (Bauerová, 1978) and has more reduced premo-
lars (P3), which could enhance mechanical efficiency of the jaws (Ghazali, Dzeverin, 2004). A few other ves-
Vestnik zoologii, 47(1): e-67—e-76, 2013
DOI 10.2478/vzoo-2013-0006
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pertilionids have lost one or both small premolars on the maxilla and mandible during their evolution
(Slaughter, 1970). P3 is lost in the dentition of Plecotus, upper and lower third premolars are lost in Pipistrellus,
and Eptesicus has lost one more tooth – the upper second premolar. Some vespertilionid genera have addi-
tionally lost one of their upper incisors. These trends indicate that there could be a relationship between size
of the animal and efficiency of the jaws’ construction, e. g., Eptesicus serotinus is almost as large as Myotis blythii,
but its diet is similar to the evidently larger M. myotis, mostly composed by hard-shelled Coleoptera (Gajdošík,
Gaisler, 2004).
Given the lack of prior research on this area, the main purpose of our research is to explore how the
shape and size of the Myotis skull and teeth are connected with the hardness of their diet.
Material and methods
We studied nine species of Myotis: 45 specimens of Myotis myotis (Borkhausen, 1797), 115 M. blythii (Tomes,
1857), 2 M. nattereri (Kuhl, 1817), 30 M. daubentonii (Kuhl, 1817), 2 M. bechsteinii (Kuhl, 1817), 14 M. mystac-
inus (Kuhl, 1817), 13 M. dasycneme (Boie, 1825), 15 M. emarginatus (Geoffroy, 1806) and 2 M. brandtii
(Eversmann, 1845).
We measured 5 paired skull traits (CBL – condylobasal length, MXT and MDL – length of upper and
lower toothrows, GMDL – length of mandibula, HCP – height of coronoid process), 3 skull breadth traits
(ZYGB – zygomatic breadth, ORB – anterior between orbital breadth, MASTB – mastoid breadth), and 42
tooth traits from both sides of jaw. Measurements were taken according to Wołoszyn (1987) and Gromov et
al. (1963). Left and right sides were denoted with prefix S and D, respectively. Upper teeth are denoted with
capital letters (I for incisors, C for canine, P for premolars, M for molars), and lower teeth are labelled with
lower-case letters. Height of upper canines (C1he) and length and width (for lower molars, width of trigonid
and talonid) of each tooth were measured (fig. 1). A proxy for area (abbreviated as A) of each tooth was esti-
mated as a product of length and width. For each of the lower molars, A was estimated as the product of length
and mean width of trigonid and talonid. Sum of all upper and lower teeth areas is denoted as ‘sumup’ and ‘sumlw’,
respectively.
Dietary items of bats are usually identified to the order level. Index of hardness (HARD) was calculat-
ed from the published data on diet of bats according to Freeman (1981b) from soft (1) to hard (5): 1 for
Ephemeroptera, Isoptera, Trichoptera, Plecoptera, Neuroptera, Diptera; 2 for Araneae, Odonata, Homoptera,
and Lepidoptera; 3 for Orthoptera; 4 for Hemiptera, Hymenoptera, Chilopoda, Diplopoda; and 5 for
Coleoptera. Psocoptera, Dermaptera and Blattaria were not ranked by Freeman (1981b). We estimated hard-
ness of their shells on the basis of their description. Psocoptera are small insects and we assigned HARD = 1
for them. Dermaptera have sclerotized forewings (Haas et al. , 2000) and we assigned HARD = 4. Hardness
of Blattidae shells is close to the hardness of Orthoptera (Aguirre et al. , 2003) and we assigned HARD = 3.
Trophic data are usually expressed as percent volume or percent frequency of diet items in feces. Percent
frequency is a percent of droppings that include specific dietary item. Percent volume is measured as the per-
centage of the area of Petri dish covered with the specific item (see Bauerová, 1986). When possible, we choose
percent volume for calculating index of hardness. Otherwise, we use formula of Safi & Kerth (2004) to trans-
form percent frequency (F) to percent volume (V): V = —2.59F3 + 3.20F2 + 0.43F. The estimated percent vol-
e-68 M. Ghazali, I. Dzeverin
Fig. 1. Measurements of upper and lower molars.
Ðèñ. 1. Ïðîìåðû âåðõíèõ è íèæíèõ ìîëÿðîâ.
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umes in sum for each dietary item were higher than 100 %, thus we rescaled these percent volumes so that
they cumulatively made 100 %.
According to Freeman (1981b), HARD index for the whole diet of each species is a multiplication of
HARD of the dietary item and its percent volume. For those species with multiple dietary descriptions, we aver-
aged index of hardness (table 1). Thus, we calculated index of hardness for the average animal with no regard
to regional and seasonal differences. We visualized interspecies differences in diets with correspondence anal-
ysis (in PAST software) of the prepared dataset of percent volumes.
Before doing the main statistic analyses we tested whether similarity between species was due to their phy-
logenetic relationships. The phylogenetic signal was estimated using Blomberg’s K statistics (Blomberg et al.,
2003) that is implemented in phylosig function in R package phytools (Revell, 2012). Randomization test with
1000 permutations was conducted to test significance of K. The calculations were performed using R software
(version 2.15.1, R Core Development Team 2012)
For the sake of brevity, we do not explain our phylogenetic hypothesis here (fig. 2), for details see Dzeverin,
Ghazali (2010) and the references there. However we did not mention M. mystacinus in that paper. In the pre-
sent paper, this species is treated in the wide sense (Mayer, Helversen, 2001) and is placed in the phylogeny
according to the reconstruction of Stadelmann et al. (2004).
As the generalized descriptor of size and shape, we calculated principal components using variance-covari-
ance matrix for skull measurements, upper teeth areas, and lower teeth areas. Missing values were replaced with
iterative imputation algorithm that is implemented in PAST software (PAST 2.03, Hammer et al., 2001). We
used a Spearman coefficient to study the correlation of traits with hardness of food. These statistical calcula-
tions were made using PAST software (PAST 2.03, Hammer et al., 2001). Corrections for multiple compar-
isons were made using R software (version 2.15.1, R Core Development Team 2012) with p. adjust function.
We employed false discovery rate (fdr) procedure, which is powerful for large number of comparisons and does
not require strong control of family-wise error rate (Benjamini, Hochberg, 1995).
e-69Correlations Between Hardness of Food and Craniodental Traits...
Tab l e 1. Characteristics of diet of the studied Myotis: Dominant item – up to 3 arthropod orders with the biggest
volume percentages; Prey size – in mm, NA – data were not available; HARD – index of hardness
Ò à á ëèö à 1. Îñîáåííîñòè ïèòàíèÿ èññëåäîâàííûõ Myotis
Species Dominant item Prey size HARD Source
M. myotis [myo] Coleoptera 13—25 4.59 Bauerová, 1978; Beck, 1995; Arlettaz,
1996; Zahn et al., 2006; Whitaker,
Karataş, 2009
M. blythii [bly] Orthoptera NA 3.48 Arlettaz, 1996; Whitaker, Karataş, 2009
M. nattereri [nat] Diptera 2—20 2.20 Taake, 1992
M. daubentonii [dau] Diptera 2—18 1.53 Taake, 1992; Beck, 1995
M. bechsteinii [bec] Diptera, Arachnida,
Coleoptera
3—26 2.37 Taake, 1992; Wolz, 1993
M. mystacinus [mys] Arachnida, Diptera 2—20 1.67 Taake, 1992; Beck, 1995
M. dasycneme [das] Diptera NA 1.58 Britton et al., 1997
M. emarginatus [ema] Arachnida NA 1.80 Bauerová, 1986; Beck, 1995
M. brandtii [bra] Diptera 3—20 1.50 Taake, 1992
Fig. 2. Phylogenetic tree of the studied Myotis species.
Ðèñ. 2. Ôèëîãåíåòè÷åñêîå äåðåâî èññëåäîâàííûõ âèäîâ Myotis.
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Results
Correspondence between dietary items and Myotis is well seen on fig. 3. Both cor-
respondence axes explain 60.8 % of total variation (Axis 1 = 39.6 %, eigenvalue = 0.808;
Axis 2 = 21.2 %, eigenvalue = 0. 433). Since bats usually hunt abundant insects, their
diet is rather diverse; it depends greatly on region and season. Nevertheless, distinction
of the diets is preserved: species for which we have several points group together. Large-
sized gleaners M. myotis and M. blythii have evident correspondence with Coleoptera and
Orthoptera, the insects that are to lesser extent available for other Myotis. Small and medi-
um-sized Myotis with different foraging strategies (aerial hawking, gleaning, trawling) most-
ly choose other arthropods (fig. 3).
Testing for the correlation of hardness index with each morphological trait was redun-
dant. So, we decided to analyze principal components of different sets of traits (skull,
upper teeth areas, lower teeth areas). The first principal component explained more than
99 % of total variance, since it is mostly connected with animals’ body size and associ-
ated shape differences. The second principal components explained less than 1 % of the
variance. Position of bats on principal components biplots agrees with the peculiarities
of Myotis skull and teeth (fig. 4). Two extremes between which other bats are placed are
clear. M. bechsteinii has relatively long skull with well-developed small premolars and rel-
atively small molars. M. dasycneme has wider skull with well-developed molars and
more reduced small premolars.
Usually, morphological differences in Myotis species agree with the species ecolo-
gy, and the genus taxonomy was formerly based on both morphological and ecological
data (Findley, 1972; Tate, 1941). However, molecular genetic studies (Ruedi, Mayer, 2001)
showed a considerably high degree of morphological convergence in evolution of Myotis
lineages. Thus, phylogeny and morphology are supposed to be uncoupled in Myotis. We
assume Brownian motion to be a plausible pattern for evolution of the traits under study
e-70 M. Ghazali, I. Dzeverin
Fig. 3. Correspondence analysis of dietary preferences of the studied Myotis species. Species acronyms as in
table 1.
Ðèñ. 3. Àíàëèç ñîîòâåòñòâèé ïèùåâûõ ïðåäïî÷òåíèé èññëåäîâàííûõ âèäîâ Myotis. Àêðîíèìû âèäîâ êàê
â òàáë. 1.
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in Myotis (Dzeverin, 2008; Dzeverin, Ghazali, 2010), i. e. changes in sister lineages were
independent.
Phylogenetic signal of HARD and other traits and morphological indices was not
significant. K for principal components ranged from 0.542 to 1.003. For morphological
indices K ranged from 0.311 to 1.114 (table 2). Since we found no significant phyloge-
netic signal, we could use standard statistical methods without phylogenetic corrections.
The main trend is evident – the bigger is an animal, the harder food it can process.
However, HARD does not significantly correlate with the first principal components, if
adjusted probability is calculated (table 3). Shape differences expressed with second prin-
cipal components in skull and teeth did not correlate with HARD, that is proved with
both significance tests.
For detailed correlation analysis we chose several morphological indices of skull and
teeth (table 2). We expected durophagous species have more mechanically effective skull:
with relatively shorter tooth rows and more reduced small premolars that put canines clos-
er to the craniomandibular joint. Instead, we observed that relative length of tooth row
(MXT/CBL) increased with the increase of hardness of diet, while relative facial breadths
e-71Correlations Between Hardness of Food and Craniodental Traits...
Fig. 4. Principal components analysis of skull traits and teeth areas. Only right measurements are named.
Ðèñ. 4. Àíàëèç ãëàâíûõ êîìïîíåíò ïðîìåðîâ ÷åðåïà è ïëîùàäåé çóáîâ. Íà ðèñóíêàõ îáîçíà÷åíû òîëü-
êî ïðîìåðû ïðàâîé ñòîðîíû.
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almost did not change (ORB/CBL, ZYG/CBL), and relative mastoid breadth
(MASTB/CBL) decreased. As was expected, Myotis that eat hard-shelled prey had rel-
atively higher coronoid processes (HCP/GMDL). Relative height of upper canines (to
the length of upper tooth row as in Freeman, 1981b) has been supposed to correlate with
the hardness of diet, but not in case of Myotis (C1he/MXT).
The relative contribution of small premolars to the sum of areas of all upper or lower
teeth did not correlate with HARD (P23/sumup, p23/sumlw). Other vestigial teeth, third
molars, were inversely related to HARD (M3/sumup, m3/sumup). Part of lower incisors
also decreases (i123/sumlw). Relative area of large teeth, first and second molars, in total
teeth area do not correlate with diet. In particular, the contribution of the first molar area
to the total area of molars (M1/M123, m1/m123) do not correlate with HARD, where-
as second molar area (M2/M123, m2/m123) increase with the index of hardness.
Discussion
Cranial and dental anatomy are thought to reflect the feeding adaptations of ani-
mals. The mastoid process and lambdoidal crest are the sites of attachment for head-mov-
ing muscles. However, mastoid breadth and height of the skull at bullae still correlate with
diet adaptations; they are relatively bigger in carnivorous and sanguivorous bats in com-
e-72 M. Ghazali, I. Dzeverin
Ta b l e 2. Blomberg’s K statistic for index of hardness, morphological indices and principal components
Ò à á ëèö à 2. Ê-ñòàòèñòèêà Áëîìáåðãà äëÿ èíäåêñà òâåðäîñòè ïèùè, ìîðôîëîãè÷åñêèõ èíäåêñîâ è ãëàâíûõ
êîìïîíåíò
Trait N K p
HARD 9 0.790 0.333
PC1 Skull 9 1.003 0.138
PC2 Skull 9 0.832 0.342
PC1 Upper teeth 9 0.848 0.301
PC2 Upper teeth 9 0.542 0.503
PC1 Lower teeth 9 0.878 0.256
PC2 Lower teeth 9 0.633 0.476
ORB/CBL 9 0.840 0.199
ZYG/CBL 9 0.980 0.103
MASTB/CBL 9 1.063 0.072
MXT/CBL 9 1.076 0.072
HCP/GMDL 9 0.602 0.445
C1he/MXT 9 0.869 0.275
I12/sumup 9 0.593 0.504
i123/sumlw 8 0.848 0.181
C1/sumup 9 0.790 0.242
c1/sumlw 8 0.643 0.523
P23/sumup 9 0.780 0.283
p23/sumlw 8 0.840 0.295
P4/sumup 9 0.864 0.224
p4/sumlw 8 0.311 0.823
M12/sumup 9 1.086 0.063
m12/sumlw 8 0.758 0.271
M3/sumup 9 0.958 0.153
m3/sumlw 8 0.860 0.223
M1/M123 9 0.836 0.250
m1/m123 8 0.832 0.298
M2/M123 9 1.114 0.063
M2/m123 8 1.035 0.070
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parison with insectivorous and frugivorous bats (Van Cakenberghe et al., 2002). This could
be related with the distribution of bite stresses during mastication.
Relative mastoid breadth and relative tooth row length are negatively correlated in
Myotis (fig. 5, RS = – 0.903, p = 0.001). Relatively wide skulls and short tooth rows in
soft-eating bats may be the result of their higher masticatory demands as could be pre-
dicted from their body size. Larger bats also need to improve their prey detection sys-
tem to hunt larger prey, meanwhile smaller bats usually hunt in air and are “opportunists
to small-prey items” (Barclay, Brigham, 1991). In comparison with other vespertilion-
ids Myotis have variable, but interspecifically similar echolocation signals (Obrist et al.,
2004). So, prey of large and small Myotis are similar in size, but due to different func-
tional abilities of their masticatory apparatus, these differ in exoskeleton properties. We
assume that relatively wide braincase and short rostrum in small Myotis is an adaptation
to relatively big and hard prey items. This makes sense, because a relatively big prey item
would be “hard” in relation to the bite force a small bat can produce, thus a wide and
short skull would have a better mechanical advantage (Santana, personal communica-
tion).
Tooth size also correlates with functional demands of mastication. In the dentition
of insectivorous bats, molars usually occupy half of the toothrow (Freeman, 1998). Certain
diminution of incisors and third molars is the most vivid trend in the dentition of the Myotis
e-73Correlations Between Hardness of Food and Craniodental Traits...
Ta b l e 3. Spearman correlation coefficients (RS) of index of hardness with principal components and morpho-
logical indices: p and p (fdr) – traditional and fdr-adjusted significance test. The significant results are shown
in bold
Òàáëèöà 3. Êîýôôèöèåíòû êîððåëÿöèè Ñïèðìåíà (RS) èíäåêñà òâåðäîñòè ïèùè ñ ãëàâíûìè êîìïîíåíòàìè
è ìîðôîëîãè÷åñêèìè èíäåêñàìè: p è p (fdr) – òðàäèöèîííûé è fdr-ñêîððåêòèðîâàííûé ìåòîä îöåíêè
äîñòîâåðíîñòè. Çíà÷èìûå ðåçóëüòàòû âûäåëåíû ïîëóæèðíûì øðèôòîì
Trait RS p p (fdr)
PC1 Skull 0.717 0.031 0.069
PC2 Skull -0.217 0.552 0.615
PC1 Upper teeth 0.767 0.021 0.056
PC2 Upper teeth 0.333 0.359 0.495
PC1 Lower teeth 0.733 0.031 0.069
PC2 Lower teeth 0.467 0.194 0.281
ORB/CBL 0.233 0.521 0.615
ZYG/CBL 0.267 0.463 0.584
MASTB/CBL -0.933 <0.001 0.003
MXT/CBL 0.833 0.006 0.029
MDL/GMDL 0.800 0.011 0.035
HCP/GMDL 0.817 0.008 0.030
C1he/MXT 0.238 0.536 0.615
I12/sumup -0.611 0.087 0.169
i123/sumlw -0.905 0.002 0.013
C1/sumup 0.783 0.014 0.040
c1/sumlw 0.619 0.115 0.184
P23/sumup 0.583 0.097 0.175
p23/sumlw 0.643 0.083 0.169
P4/sumup -0.567 0.121 0.184
p4/sumlw 0.619 0.115 0.184
M12/sumup 0.283 0.463 0.584
m12/sumlw 0.095 0.840 0.840
M3/sumup -0.933 <0.001 0.003
m3/sumlw -0.857 0.007 0.030
M1/M123 0.183 0.644 0.691
m1/m123 -0.095 0.840 0.840
M2/M123 0.983 <0.001 <0.001
m2/m123 0.905 0.002 0.013
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species studied. Although a portion of areas of the first two molars with respect to the
total area of teeth does not change, the contribution of the 2nd molar to the total area
of molars increases significantly with the increase of hardness of diet. Maximal bite forces
are applied at post-canine teeth (Dumont et al., 2005). In functional terms, as the point
of bites approaches to the fulcrum, the out-lever is shortening and bite force increases.
Large second molars may indicate displacement of the maximal bite force from first to
second molar.
Bite force in bats is rather associated with absolute size than with specific traits of
skull; along with increasing of skull length, fiber length of mastication muscles (especial-
ly m. masseter and m. temporalis, Herrel et al., 2008). The moment at the temporo-
mandibular joint is generated mainly by three muscles (m. temporalis, m. masseter, m.
pterygoideus medius). The relative importance of these muscles is associated with the pecu-
liarities of diet. The contribution of the temporalis to the jaw moment is dominant in bats
with hard diets, masseter muscles input is important in bats with soft diets, and medial
pterygoid increases in importance in bats with liquid diet (Santana et al., 2010).
Wide and short skulls may lead to a relative increase of cross-sectional area of mus-
cles and thus higher bite force (Swartz et al., 2003). We suppose that functional demands
on eating tough prey are satisfied with the increased body-sized and associated expan-
sion of muscles’ cross-sectional area. However these changes may not be seen in rela-
tive scale of the traits, they may be masked under increase of body-size.
In spite of having a small sample of Myotis species, we consider our results to be rep-
resentative since rather different trophic strategies and different body sizes were present-
ed in the sample. However, we expect that more species would make a stronger analysis.
We thank Sharlene E. Santana for valuable comments, advice, and criticisms. We also thank the cura-
tors and staffs of the zoological museums, who gave an opportunity to work with collections: Zoological Museum
of Moscow University (Moscow, Russia), Zoological Museum of Kyiv University (Kyiv, Ukraine); National
e-74 M. Ghazali, I. Dzeverin
Fig. 5. Relative breadth of skull at mastoids (MASTB/CBL) decreases with relative elongation of the rostral
part of skull (MXT/CBL). Size of bubbles is proportional to HARD.
Ðèñ. 5. Îòíîñèòåëüíàÿ øèðèíà ÷åðåïà ìåæäó ñîñöåâèäíûìè îòðîñòêàìè (MASTB/CBL) óìåíüøàåòñÿ
ñ îòíîñèòåëüíûì óäëèíåíèåì ðîñòðàëüíîé ÷àñòè ÷åðåïà (MXT/CBL). Ðàçìåð ïóçûðüêîâ ïðîïîðöèî-
íàëåí HARD.
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Download Date | 12/5/16 8:30 PM
Museum of Natural History of the National Academy of Sciences of Ukraine (Kyiv, Ukraine). We are grate-
ful to the organizers of the XII European Bat Research Symposium (Vilnius, Lithuania, 2011), where we had
presented the results.
References
Aguirre L. F., Herrel A., Van Damme R., Matthysen E. The implications of food hardness for diet in bats //
Functional Ecology. – 2003. – 17, 2. – P. 201—212.
Arlettaz R. Feeding behaviour and foraging strategy of free-living mouse-eared bats, Myotis myotis and Myotis
blythii // Anim. Behav. – 1996. – 51. – P. 1—11.
Barclay R. M. R., Brigham R. M. Prey detection, dietary niche breadth, and body size in bats: why are aerial
insectivorous bats so small? // The American Naturalist. – 1991. – 137, N 5. – P. 693—703.
Bauerová Z. Contribution to the trophic bionomics of Myotis emarginatus // Folia zoologica. – 1986. – 35,
4. – P. 305—310.
Bauerová Z. Contribution to the trophic ecology of Myotis myotis // Folia zoologica. – 1978. – 27, 4. –
P. 305—316.
Beck A. Fecal analyses of European bat species // Myotis. – 1995. – 32—33. – P. 109—119.
Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple
testing // J. R. Statist. Soc. B. – 1995. – 57, N 1. – P. 289—300.
Blomberg S. P., Garland T., Jr., Ives A. R. Testing for phylogenetic signal in comparative data: Behavioral traits
are more labile // Evolution. – 2003. – 57, N 4. – P. 717—745.
Blood B. R., Clark M. K. Myotis vivesi // Mammalian Species. – 1998. – 588. – P. 1—5.
Britton A. R. C., Jones G., Rayner J. M. V. et al. Flight performance, echolocation and foraging behaviour in
pond bats, Myotis dasycneme (Chiroptera: Vespertilionidae) // J. Zool. – 1997. – 241, 3. – P. 503—522.
Dietz C., von Helversen O., Nill D. Bats of Britain, Europe and Northwest Africa. – London : A&C Black
Publishers Ltd., 2009. – 400 p.
Dumont E. R., Dávalos L. M., Goldberg A. et al. Morphological innovation, diversification and invasion of a
new adaqptive zone // Proc. R. Soc. B. – 2012. – 279, 1734. – P. 1797—1805.
Dumont E. R., Piccirillo J., Grosse J. R. Finite-element analysis of biting behavior and bone stress in the facial
skeletons of bats // The Anatomical Record Part A. – 2005. – 283 A. – P. 319—330.
Dzeverin I. The stasis and possible patterns of selection in evolution of a group of related species from the bat
genus Myotis (Chiroptera, Vespertilionidae) // J. Mammal. Evol. – 2008. – 15. – P. 123—142.
Dzeverin I., Ghazali M. Evolutionary mechanisms affecting the multivariate divergence in some Myotis species
(Chiroptera, Vespertilionidae) // Evol. Biol. – 2010. – 37. – P. 100—112.
Findley J. S. Phenetic relationships among bats of the genus Myotis // Systematic Zoology. – 1972. – 21,
1. – P. 31—52.
Freeman P. W. A multivariate study of the family Molossidae (Mammalia, Chiroptera): morphology, ecolo-
gy, evolution // Fieldiana (Zoology). – 1981 a. – 7. – P. 1—173.
Freeman P. W. Correspondence of food habits and morphology in insectivorous bats // J. Mamm. – 1981 b. –
62, 1. – P. 164—166.
Freeman P. W. Form, function, and evolution in skulls and teeth of bats // Bat Biology and Conservation /
Ed. T. H. Kunz, P. A. Racey. – Washington, DC : Smithsonian Institution Press, 1998. – P. 140—156.
Freeman P. W. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny // Evol.
Ecol. Res. – 2000. – 2. – P. 317—335.
Freeman P. W. Specialized insectivory: Beetle-eating and moth-eating molossid bats // J. Mamm. – 1979. –
60, 3. – P. 467—479.
Gajdošík M., Gaisler J. Diet of two Eptesicus bat species in Moravia (Czech Republic) // Folia Zool. – 2004. –
53, N 1. – P. 7—16.
Ghazali M. A., Dzeverin I. I. Biometrics of reduced elements of the dental system in some mouse-eared bats,
Myotis (Vespertilionidae) // Plecotus et al. – 2004. – 7. – P. 7—17. – Russian : Ãõàçàëè Ì. À. , Äçåâåðèí
È. È. Áèîìåòðè÷åñêàÿ õàðàêòåðèñòèêà ðåäóêöèè ýëåìåíòîâ çóáíîé ñèñòåìû íåêîòîðûõ âèäîâ íî÷-
íèö, Myotis (Vespertilionidae).
Gromov I. M., Gureev A. A., Novikov G. A. et al. Mammals of the fauna of the USSR. Part 1. Moskva-Leningrad:
Izdatelstvo Akademii Nauk SSSR, 1963. – 639 p. – Russian : Ãðîìîâ È. Ì., Ãóðååâ À. À., Íîâèêîâ Ã. À.
è äð. Ìëåêîïèòàþùèå ôàóíû ÑÑÑÐ. ×àñòü 1.
Haas F., Gorb S., Wootton R. J. Elastic joints in dermapteran hind wings: materials and wing folding // Arthropod
Structure & Development. – 2000. – 29. – P. 137—146.
Hammer O., Harper D. A. T., Ryan P. D. PAST: Paleontological Statistics software package for education and
data analysis // Palaeontologia Electronica. – 2001. – 4, 1. – P. 1—9. – http:// palaeo–electronica.
org/2001_1/past/issue1_01. htm.
Herrel A., De Smet A., Aguirre L. F., Aerts P. Morphological and mechanical determinants of bite force in bats:
do muscles matter? // J. Exp. Biol. – 2008. – 211. – P. 86—91.
Mayer F., von Helversen O. Cryptic diversity in European bats // Proc. R. Soc. Lond. B. – 2001. – 268. –
P. 1825—1832.
e-75Correlations Between Hardness of Food and Craniodental Traits...
Unauthenticated
Download Date | 12/5/16 8:30 PM
Obrist M. K., Boesch R., Flückiger P. F. Variability in echolocation call design of 26 Swiss bat species: conse-
quences, limits and options for automated field identification with a synergetic pattern recognition
approach // Mammalia. – 2004. – 68, N 4. – P. 307—322.
Price S. A., Hopkins S. S. B., Smith K. K., Roth V. L. Tempo of trophic evolution and its inpact on mammalian
diversification // Proc. Natl Acad. Sci USA. – 2012. – 109, 18. – P. 7008—7012.
R Development Core Team. R: A language and environment for statistical computing. – Vienna : R Foundation
for Statistical Computing, 2012. – http: // www.R-project.org/.
Revell L. J. phytools: An R package for phylogenetic comparative biology (and other things) // Methods Ecol.
Evol. – 2012. – 3. – P. 217—223.
Ruedi M., Mayer F. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests determinis-
tic ecomorphological convergences // Molecular Phylogenetics and Evolution. – 2001. – 21, N 3. –
P. 436—448.
Safi K., Kerth G. A comparative analysis of specializations and extinction risk in temperate zone bats //
Conservation Biology. – 2004. – 18, 5. – P. 1293—1303.
Santana S. E., Dumont E. R., Davis J. L. Mechanics of bite force production and its relationship to diet in bats
// Functional Ecology. – 2010. – 24, N 4. – P. 776—784.
Slaughter B. H. Evolutionary trends of chiropteran dentitions // About bats: A chiropteran biology symposium
/ Eds B. H. Slaughter, D. W. Walton. – Dallas, Texas : Southern Methodist University Press, 1970. –
P. 51—84.
Stadelmann B., Jacobs D. S., Schoeman C., Ruedi M. Phylogeny of African Myotis bats (Chiroptera,
Vespertilionidae) inferred from cytochrome b sequences // Acta Chiropterologica. – 2004. – 6, N 2. –
P. 177—192.
Swartz S. M., Freeman P. W., Stockwell E. F. Ecomorphology of bats: comparative and experimental approach-
es relating structural design to ecology // Bat Ecology / Eds T. H. Kunz, M. B. Fenton. – Chicago :
The University of Chicago Press, 2003. – P. 257—300.
Taake K. H. Strategien der Ressourcennutzung an Waldgewässern jagender Fledermäuse (Chiroptera:
Vespertilionidae) // Myotis. – 1992. – 30. – P. 7—74.
Tate G. H. H. A review of the genus Myotis (Chiroptera) of Eurasia, with special reference to species occur-
ring in the East Indies (Results of the Archbold expeditions, N 39) // Bull. Amer. Mus. Natur. Hist. –
1941. – 78, 8. – P. 537—565.
Van Cakenberghe V., Herrel A., Aguirre L. F. Evolutionary relationships between cranial shape and diet in bats
(Mammalia: Chiroptera) // Topics in Functional and Ecological Vertebrate Morphology / Eds P. Aerts
et al. – Maastricht : Shaker Publishing, 2002. – P. 205—236.
Whitaker J. O., Karataş A. Food and feeding habits of some bats from Turkey // Acta Chiropterologica. – 2009. –
11, 2. – P. 393—403.
Simmons N. B. Order Chiroptera // Mammal Species of the World. A Taxonomic and Geographic Reference /
Ed. D. E., Wilson, D. M. Reeder. – 3rd ed. – Baltimore : Johns Hopkins University Press, 2005. –
P. 312—529. – http: // bucknell.edu/msw3/
Wołoszyn B. Pliocene and Pleistocene bats of Poland // Acta Palaeontologica Polonica. – 1987. – 32, N 3-4. –
P. 207-325.
Wolz I. Das Beutespektrum der Bechsteinfledermaus Myotis bechsteini (Kuhl, 1818) ermittelt aus Kotana lysen
// Myotis. – 1993. – 31. – P. 27—68.
Zahn A., Rottenwallner A., Güttinger R. Population density of the greater mouse-eared bat (Myotis myotis), local
diet composition and availability of foraging habitats // J. Zoology. – 2006. – 269. – P. 486—493.
Received 3 July 2012
Accepted 21 November 2012
e-76 M. Ghazali, I. Dzeverin
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|
| id | nasplib_isofts_kiev_ua-123456789-109672 |
| institution | Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| issn | 0084-5604 |
| language | English |
| last_indexed | 2025-12-07T15:43:40Z |
| publishDate | 2013 |
| publisher | Інститут зоології ім. І.І. Шмальгаузена НАН України |
| record_format | dspace |
| spelling | Ghazali, M. Dzeverin, I. 2016-12-06T16:35:43Z 2016-12-06T16:35:43Z 2013 Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) / M. Ghazali, I. Dzeverin // Вестник зоологии. — 2013. — Т. 47, № 1. — С. 73–82. — Бібліогр.: 46 назв. — англ. 0084-5604 DOI 10.2478/vzoo-2013-0006 https://nasplib.isofts.kiev.ua/handle/123456789/109672 599.426:[591.431.4+591.471.4+591.53] We studied 8 skull and 42 dental characters in nine Myotis species (M. myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. daubentonii, M. brandtii, M. mystacinus) to analyze correlations between hardness of food and skull and dental traits. Contrary to the common bat pattern, Myotis that are specialized on hard-shelled dietary items tend to have relatively narrow skull and long tooth rows. The dentition of durophagous Myotis is composed by relatively enlarged second and reduced third molars. Для анализа связи между твердостью пищи и значениями черепных и зубных признаков исследовано 8 черепных и 42 зубных промера у девяти видов ночниц (Myotis myotis, M. blythii, M. bechsteinii, M. dasycneme, M. emarginatus, M. nattereri, M. daubentonii, M. brandtii, M. mystacinus). Вопреки общим для летучих мышей закономерностям у ночниц, специализированных к поеданию объектов питания с твердыми покровами, выявлена тенденция к сужению черепа и удлинению зубных рядов. В зубном аппарате такие ночницы имеют относительно увеличенные вторые и редуцированные третьи моляры. We thank Sharlene E. Santana for valuable comments, advice, and criticisms. We also thank the curators and staffs of the zoological museums, who gave an opportunity to work with collections: Zoological Museum of Moscow University (Moscow, Russia), Zoological Museum of Kyiv University (Kyiv, Ukraine); National Museum of Natural History of the National Academy of Sciences of Ukraine (Kyiv, Ukraine). We are grateful to the organizers of the XII European Bat Research Symposium (Vilnius, Lithuania, 2011), where we had presented the results. en Інститут зоології ім. І.І. Шмальгаузена НАН України Вестник зоологии Морфология Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) Связь между твердостью пищи и краниодентальными признаками девяти видов ночниц, Myotis (Chiroptera, Vespertilionidae) Article published earlier |
| spellingShingle | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) Ghazali, M. Dzeverin, I. Морфология |
| title | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) |
| title_alt | Связь между твердостью пищи и краниодентальными признаками девяти видов ночниц, Myotis (Chiroptera, Vespertilionidae) |
| title_full | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) |
| title_fullStr | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) |
| title_full_unstemmed | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) |
| title_short | Correlations Between Hardness of Food and Craniodental Traits in Nine Myotis Species (Chiroptera, Vespertilionidae) |
| title_sort | correlations between hardness of food and craniodental traits in nine myotis species (chiroptera, vespertilionidae) |
| topic | Морфология |
| topic_facet | Морфология |
| url | https://nasplib.isofts.kiev.ua/handle/123456789/109672 |
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