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Structure and evolutionary implications of the musculi arrectores pilorum in chiroptera.

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Structure and Evolutionary Implications of the
Musculi Arrectores Pilorum in Chiroptera
W. B. QUAY
Department of Zoology, University of California, Berkeley, California
ABSTRACT
Skin samples from 16 genera and 19 species of bats we:re studied histologically. These and review of the literature revealed musculi arrectores pilorum composed of smooth muscle present only in Megachiroptera and complex cutaneous striated muscle systems best developed in Microchiroptera. Smooth muscle arrectores of
the mid-dorsal neck skin of Hypsignathus monstrosus are described in detail and resemble those of generalized structure in other mammalian Orders. Shoulder pouches
of the epaulet bats (Epomophorus and Epomops) contain compound smooth and striated muscle systems for eversion of hair tufts and pouch respectively. An evolutionary
trend within the Chiroptera of reduction in smooth muscle arrectores and replacement
by integumentary striated muscle fibers is suggested.
Absence of evidence of smooth muscles tained from museum collections had been
of the musculi arrectores pilorum in bats fixed presumably in 10% formalin and
(Chiroptera) impressed the author during later transferred to ethanol solutions for
recent review of integumentary structure storage. Serial paraffin sections were cut
in this group of mammals. On the other at thicknesses ranging from 5 to 10 v and
hand, it has been appreciated for many affixed in order on slides. Different slides
years that bats have special striated muscle were stained according to the following
bands in, or inserting on, the integument, procedures : ( 1) Ehrlichs acid alum hemaparticularly that of the flight membranes, toxylin and eosin Y (Bensley and Bensley,
ear pinna and facial structures. However, '38 ) ; (2 ) periodic acid-Schiff (PAS ) with
these features are developed notably pri- hematoxylin nuclear stain (Lillie, '54);
marily in the Microchiroptera, which are ( 3 ) chrome alum hematoxylin and phloxcommonly considered to be more advanced ine (Gomori, '41); ( 4 ) modified Bodian
in an evolutionary sense according to their protargal; and ( 5 ) 1 % azure A with differmorphology than are the Megachiroptera. entiation in colophonium alcohol (Lillie,
They are also more frequently studied and '54).
better known anatomically. The present
OBSERVATIONS
study sought to demonstrate the occurrence
Megachiroptera.
At least many of the
of arrector pili muscles in bats by histological study of skin samples from body hair follicles of the mid-dorsal neck skin
regions known to have the ability in life of the hammer-headed bat (Hypsignathus
of raising or everting the hair in particular monstrosus) are equipped with arrector
genera of Megachiroptera. Furthermore, pili smooth muscles. The few follicles seen
the histological study of skin samples from belonging to guard hairs appear to lack
both groups of bats served to provide evi- arrector smooth muscles. The arrector musdence of a trend in the evolution of smooth cles of the neck hairs in this species are
and striated muscles of the integument in representative of the most typical mammalian pattern in major features of structhis Order (Chiroptera) of mammals.
ture and arrangement (fig. 1). Inserting
MATERIALS AND METHODS
near the base of the resting hair bulb of
Skin samples from 16 genera and 19 a particular follicle by means of a threadspecies (table 1 ) were processed according like strand of compact connective tissue
to standard procedures for histological fibers, each arrector niuscle extends posstudy. Specimens collected by the author teriorly and superficially within the dermis
were fixed in either 10% neutral buffered and fades into a usually more diffuse conformalin or Bouin's fluid. Specimens obReceived Oct. 10, '68. Accepted Nov. 18, '68.
ANAT. REC., 163: 587-594.
58 7
W. B. QUAY
588
TABLE 1
Specimens studied
Suborder
Genus species
Megachirop tera
Pteropus mariannus
Hypsignathus monstrosus
Epomorphorus angolensis
Epomorphorus anurus
Epomops biittikoferi
Epomops franqueti
Eonycteris spelaea
Microchiroptera
Rhinopoma cystops
Lavia f r o m
Number
and sex
Regions sampled
19
19
lips, muzzle, urogenital-anal area
mid-dorsal area of neck
shoulder pouch
shoulder pouch
shoulder pouch
shoulder pouch
shoulder pouch and axillary nipple
Id
1d
Id
In"
43,29
13
19
Rhinolophus sp.
Glossophaga soricina
Mornoops blainvillii
Phyllostomus discolor
Sturnira lilium
Myotis Zucifugus
1-
Myotis sodalis
Pizonyx vivesi
Eptesicus fuscus
Plecotus townsendi
3d, 1 9
1d,19
29
1-
1P
Id
19
19
Id,1 9
nective tissue attachment either near the
epidermis or near the neck of the next hair
follicle posteriorly. In the latter instance
a slight epithelial spur sometimes extends
anteriorly from the neck or uppermost portion of the adjacent follicle toward the
fibers of the arrector muscle. The means
and ranges of the lengths, maximum crosssectional diameters, and smooth muscle
cell contents of eight longitudinally sectioned arrector muscles are: 318 p (180420), 13 p (8-17), and 50 cells (20-80).
The length measurements include the
thread-like tendon of insertion which usually appears to consist only of connective
tissue. This tendon is closely applied to the
ventral surface of the associated sebaceous
gland alveolus and h a s its site of major
attachment to smooth muscle fibers close
to the distal and posterior boundary of the
sebaceous alveolus. No striated muscle fibers are seen within the dermis of the middorsal neck skin of this species.
A strikingly different and specialized
pattern of muscles is seen in the skin
lining the shoulder pouches of the species
of epaulet bats studied (genera: Epomophorus and E p o m o p s ) . Within each shoulder
pouch are clusters of long white hairs.
__ -
rostrum and nose-leaf
nose-leaf, muzzle, circumorbital and
Fectoral skin
rostrum and nose-leaf
face and lower jaw
face and lower jaw
face and lower jaw
face and lower jaw and axillary nipple
face, ear, urogenital-anal area, wing, wrist,
feet
Wings
wing and uropatagial membranes
wing membranes
muzzle, ear pinna and tragus
Mean and modal numbers of hairs per
cluster or group depend upon species and
position within the pouch. A probably near
maximal group size of 21 (9-26) is seen
in Epomophorus angolensis. The follicles
within a group are specialized by being:
( 1 ) positioned perpendicular to the skin's
surface, (2) tightly bound to each other
by connective tissue around their necks
(= upper pilo-sebaceous ducts), ( 3 ) dilated at mid-length to form thin-walled
sinuses, and ( 4 ) expanded basally by an
epithelial-connective tissue interdigitation
(fig. 2 ) . Inserting over this last and basal
area on each follicle are sheets and strands
of smooth muscle fibers of the arrector pili
system. These pass to the neck and adjacent epidermis of the same follicle and
are attached a t one or both sites by means
of connective tissue fibers. These arrector
muscles thus form slings of probable major
significance in the eversion of the hairs,
accompanied most likely by folding of the
follicle walls in the sinus region. Such follicular sinuses are found only in these
erectile follicles of the shoulder pouches.
While they are continuous with sebaceous
gland ducts, the associated sebaceous alveoli are modest in size and do not appear
ARRECTORES PILORUM IN BATS
to be sites of unusual activity or specialization. Outside the smooth muscle sling are
isolated fibers of striated muscle inserting
individually in the superficial connective
tissue of the dermis between the groups of
follicles and within the skin folds separating such groups. These striated fibers
can be seen to originate at least primarily
from cutaneous but subdermal sheets passing over the shoulder. They probably serve
to evaginate the pouch as a whole, since
each pouch fundus is not pointed directly
inward, but is at a ventro-medial angle.
Microchirqptera. In none of the species
or areas examined from this group were
arrector pili muscles found. It remains possible, however, that very slight or attenuated fibers or bands may have been overlooked. The primary observation to be
made concerning Microchiroptera is the
abundance and complexity of striated muscle fiber systems especially within the
facial structures, ear pinna and tragus,
and the flight membranes. Although some
striated fibers are seen in some of these
regions in Pteropus, representing the Megachiroptera, they are relatively much less
numerous and less specialized in arrangement. The elaborate and gross fleshy features of the facial region in Microchiroptera are found to contain, as a rule,
abundant striated muscle fibers and elastic
cartilage spicules or plates. Hair follicles
within these features appear to have little
if anything in the category of smooth muscle arrectors.
589
those seen in ovine skin and implicated in
crimp formation (Chapman, '65) are not
seen in this species (Hypsignathus manstrosus). Some similarity is seen, nevertheless, between the ovine arrector structure
and arrangement and that of the arrectors
of the shoulder pouches in E p m o r p h o r u s
and E p m o p s . Although a slight waviness
occurs in the hair of this region, the primary function of arrector contraction here
is eversion of the hair, as suggested by observations of living specimens (Rosevear,
'65) as well as by the histology. The vibratory activity of the hair tufts in life and
their retraction post mortem (Rosevear,
'65) are probably more dependent on
the striated muscle constituents than the
smooth muscle, but no experimental studies have been made.
The insertions of the arrector muscles in
Hypsignathus are notable for the thinness
and length of their tendinous cords. Broad
muscular insertions on follicle bases near
the resting hair bulbs, such as seen in some
Insectivora (Sokolov, '68),are true for the
arrectores in the shoulder pouches of Epomophorus and Epomops. In all of the bats,
arrector insertion is at or near the base of
the follicles in the region of the hair bulb,
certainly in part due to the resting (telogen) stage represented by the follicles in
the specimens studied. Distinct bulges or
epithelial enlargements of follicle walls at
arrector insertions are seen distinctly only
in the case of the shoulder pouches.
Motility of integumentary extensions in
Microchiroptera is effected by complex striDISCUSSION
ated muscle fiber systems according to
Detailed morphological and quantitative published studies, both histological and
information concerning arrector pili mus- physiological (Leydig, 1859; Schobl, 1871 ;
cles of relatively few species has been Redtel, 1873; Morra, 1899; Schumacher,
published (Kanaizuka, '26; Okajima and '31, '32, '32a; Jazuta, '37; Werner et al.,
Kanaizuka, '29, '29a). Comparisons of the '50; Dalquest et al., '52; Mohres, '53; Dalarrector muscles of the hammer-headed bat quest and Werner, '54; Quay and Reeder,
with those of better known mammalian '54; Schneider and Mohres, '60; Madkour,
genera (Homo, Macaca, Canis, Ovus, Felis, '61; Griffin et al., '62; Gupta, '67; and
Lepus) reveal the bat muscles to be rela- others).
Megachiroptera have striated muscle
tively simple in structure and comparable
in cross-sectional diameter, but somewhat bands within the alar membranes but have
longer and forming a more acute angle relatively little development of the facial
with the skin surface. Variation in length systems of such diverse forms seen in Miand extent of the hammer-headed bat's crochiroptera. It can be suggested that
arrectores occurs through lesser develop- within bats, an evolutionary and funcment of the epidermally or superficially di- tional replacement of smooth muscle arrecrected end of the bundle. Complex arrector tores by cutaneous striated muscle systems
systems and directional variations such as has occurred. Comparative histology and
590
W. B. QUAY
degrees of morphological specialization presented in the published literature suggest
that this process occurred earliest in the
flight membranes, later in the facial features and most recently in the dorsal and
shoulder regions of the body proper.
ACKNOWLEDGMENTS
I am indebted to Drs. Richard Van
Gelder and Karl Koopman of the American
Museum of Natural History and Drs. Henry
Setzer and Charles Handley of the U. S.
National Museum for the opportunity of obtaining tiissue samples from certain exotic
species. I wish to thank also Sue Evans,
Helen Sherry and Victor Gin for laboratory
assistance, Alfred Blaker for photomicrography and Emily Reid for final presentation of figures.
LITERATURE CITED
Bensley, R. R., and S. H. Bensley 19338 Handbook of Histological and Cytological Technique.
Univ. of Chicago Press, Chicago, 162 pp.
Chapman, R. E. 1965 The ovine arrector pili
musculature and crimp formation in wool. In:
Biology of the Skin and Hair Growth. A. G.
Lyne and B. F. Short, eds. Angus and Robertson, Sydney, pp. 201-232.
Dalquest, W. W., and H. G. Werner 1954 Histological aspects of the faces of North American
bats. J. Mammal., 35: 147-160.
Dalquest, W. W., H. J. Werner and J. H. Roberts
1952 The facial glands of a fruit-eating bat,
Artibeus jamaicensis Leach. J. Mammal., 33:
102-103.
Gomori, G. 1941 Observations with differential
stains o n human islets of Langerhans. Am. J.
Path., 17: 395-406.
Griffin, D. R., D. C. Dunning, D. A. Cahlander,
F. A. Webster, J. D. Pye, M. Flinn and A. Pye
1962 Correlated orientation sounds and ear
movements of horseshoe bats. Nature, 196:
1185-1 188.
Gupta, B. B. 1967 The histology and musculature of plagiopatagium in bats. Mammalia, 31;
313-321.
Jazuta, K. 1937 Zur vergeichenden Anatomie
der Hautmuskulatur bei Saugetieren. 4 mitteilung: Halshautmuskulatur bei den Chiropteren.
Anat. Anz. Jena., 84: 26-31.
Kanaizuka, 2. 1926 Beitrage zur Morphologie
des Musculus arrector pili. Folia Anat. .Tauon..
- _
4: 141-169.
~
Leydig, F. 1859 Uber die ausseren Bedeckungen der Saugetiere. Arch. f. Anat., Physiol.
und wiss. Medizin. Leipzig: 677-747.
Lillie, R. D. 1954 Histopathologic Technic and
Practical Histochemistry. Blakiston Co., New
York, x 501 pp.
Madkour, G. A. 1961 The structure of the facial
area in the mouse-tailed bat, Rhinopoma hardwickei cystops, Thomas. Bull. 2001.SOC.Egypt,
16: 50-54.
Mohres, F. P. 1953 Uber die Ultraschallorientierung der Hufeisennasen (Chiroptera-Rhinolophinae). Z. Vergl. Physiol., 34: 547-588.
Morra, T. 1899 I muscoli cutanei della membrana alare dei Chirotteri. Boll. dei Musei di
Zool. e di Anat. Comparata della R. Univ. di
Torino (Turin), 14: 1-6.
Okajima, K.,and Z. Kanaizuka 1929 Quantitative Untersuchung des Haarbalgmuskels bei
den Saugetieren. Folia Anat. Japon., 7; 185202.
1929a Die Morphologie des Haarbalgmuskels bei den Saugetieren. Folia Anat.
Japon., 7: 445-456.
Quay, W. B., and W. G. Reeder 1954 The hemorrhagic and hemopoietic nodules in the alar
and interfemoral membranes of Pizonyx vivesi
(Chiroptera). J. Morph., 94: 43-72.
Redtel, A. 1873 Der Nasenaufsatz des Rhinolophus Hippocrepis. Zeitschr. f. wiss. Zool., 23:
254-288.
Rosevear, D. R. 1965 The bats of West Africa.
British Mus. (Nat. Hist.) London: xvii-418.
Schneider, H., and R. P. Mohres 1960 Die Ohrbewegungen der Hufeisenfledermause (Chiroptera, Rhinolophidae) und der Mechanismus des
Bildhorens. Zeit. Vergl. Physiol., 44: 1-90.
Schobl, J. 1871 Die Flughaut der Fledermause,
namentlich die Endigung ihrer Nerven. Arch.
Mikro. Anat., 7: 1-31.
Schumacher, S. 1931 Der “M. propatagialis
proprius” und die “Tendo propatagialis” in
ihren Beziehungen zur V. cephalica bei den
Fledermausen. Nebst Bemerkungen uber den
Bau der Flughaut im allgemeinen. Zeit. Ges.
Anat., Abt. 1, Zeit. Anat. Entwickl., 94: 642679.
1932 Muskeln und Nerven der Fledermausflughaut. Nach Untersuchung an Pteropus.
Zeit. Anat. Entw. Besch., Berlin 97: 610-621.
1932a Die Entwicklung der Fledermausflughaut. Zeit. Anat. Entw. Gesch., Berlin 98:
703-721.
Sokolov, V. E. 1968 The structure and adaptive
peculiarities of the skin of insectivorous mammals. Vestnik, Biol. Pochovo (Moscow Univ.)
Ser. 6, 1968: 20-31.
Werner, H. J., W. W. Dalquest and J. H. Roberts
1950 Histological aspects of the glands of the
bat, Tadarida cynwephala (LeConte). J. Mammal., 31: 395-399.
+
PLATES
PLATE 1
EXPLANATION OF FIGURES
Both sections stained with hematoxylin and eosin.
1
Parasagittal section of dorsal skin of neck of Hypsignathus monstTos u s (adult 0 , Rembo Kotou, French Congo).
2
Vertical section of group of erectile hairs in fundus of shoulder pouch
of Epomops biittikoferf (adult 8,Mt. Coffee, Liberia).
Abbreviations: AP, musculi arrectores pilorum; API, insertions on hair
follicles of arrectores pilorum; AT, adipose tissue; E, epidermis; H, hair;
SE, sebaceous gland; SKL, striated muscle fiber in longitudinal section;
SKO, striated muscle fibers in oblique section.
592
ARRECTORES PILORUM IN BATS
W. B. Quay
PLATE 1
593
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