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Phylogenetic significance of the skin of New World monkeys (Order primates infraorder platyrrhini).

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Phylogenetic Significance of the Skin of New World
Monkeys (Order Primates, Infraorder Platyrrhini)
EDWIN M. PERKINS2
Department of Biotogical Sciences, University of Southern California,
Los Angeles, California 90007
KEY WORDS
n8ic ance.
New World monkeys . Skin . Phylogenetic sig
ABSTRACT
The combined properties of a given cutaneous system, like other
characters classically employed by systematic zoologists, are useful criteria in
the assessment of primate taxonomy and phylogeny. From the synthesis of all
available data, it is also concluded that (1) the results define a baseline regarding the normal histology and histochemistry of the skin of most genera and
many species of New World monkeys; ( 2 ) intrageneric and intraspecsc subtleties in cutaneous variation exist in primate integument; ( 3 ) single and multiple cutaneous traits contribute to the characterization and accurate identification of most levels of taxa within the primate hierarchy; (4) some traits,
however, negate recent taxonomic practices, e.g., the familial position of CaZlimico; (5) basic cutaneous patterns confirm currently accepted concepts of
taxonomy and phylogeny; and (6) the various cutaneous signatures of extant
platyrrhines record a history of adaptive radiation in isolation, and suggest that
the designation of at least two distinct families is warranted.
Primate skin is not a new subject. Many
fragmentary publications in the older literature are concerned with pigmentation,
hair texture, coat coloration, dermatoglyphics, hair patterns or glandular concentrations. Most authors of these early
studies managed to make significant contributions to our understanding of the skin
of primates.
In the first comprehensive study to employ modern methods of histology and histochemistry, Montagna and Ellis ('59) suggested that systematic comparative studies
of skin in members of a family or order
may reveal modifications which provide
information on phylogenetic relationships.
It was hoped that emphasis on basic underlying patterns in the many adaptations
should be a valuable point of reference
to students of evolution and systematics.
As the cutaneous systems of an increasing number of prosimians and Old World
monkeys (catarrhines) were subsequently
examined and cataloged, this aim was partially realized; general phylogenetic trends
began to develop. However, the New World
monkeys (platyrrhines) were a conspicuous
vacuum.
AM. J. PHYS. ANTHROP.,42: 39-24.
Constituting a large and highly divergent complex, New World monkeys represent one of the most varied of all primate
infraorders. To date, for example, as many
as five to seven subfamilies, 20 genera and
subgenera, 75 species, and 175 subspecies
have been described (Napier and Napier,
'67). The New World monkeys also represent approximately 30% of all primate
genera and 34% of all primate species
(Buettner-Janusch, '63); however, the integument of only one species of platyrrhine
nad been examined in detail (Hanson and
Montagna, '62) prior to the initiation of
the present survey in 1966.
In the ensuing seven years, 47 additional
New World monkeys, representing 13 genera and 21 species, have been obtained.
Certain data have been periodically reported (Perkins, '66; Machida et al., '67;
1 This work was supported in part by grant FR 00163
of the National Institutes of Health and by funds from
Public Health Service grants AM 05512 and AM 08445,
Biology of Skin of Man and Other Primates. Also s u p
ported in part by funds from the Revlon Research Center, Inc., New York, and the A l l a n Hancock Foundation.
University of Southern California.
2 Permanent address: Dr. Edwin M. Perkins. Jr., Department of Biological Sciences, University of Southern
California, Los Angeles, California 90007.
395
396
EDWIN M. PERKINS
Perkins and Machida, ’67; Machida and
Giacometti, ’68; Perkins, ’68; Perkins et
al., ’68; Perkins and Ford, ’69; Perkins,
’69a,b,c); other findings have been published in the form of system surveys
(Machida and Perkins, ’67; Arao and
Perkins, ’68; Perkins et al., ’69); still other
findings remain unpublished. The most
recent study on the skin of the silvered
sakiwinki (Perkins and Ford, ’75) contributes still more information to a rapidly
accumulating mass of fragmentary knowledge.
A synthesis of the numerous and dissociated data is imperative. Organization
and appraisal of information among the
various New World monkey taxa, together
with a comparison of the infraorder Platyrrhini to other monophyletic taxa in the
Order Primates, may facilitate the more
comprehensive understanding of primate
phylogeny and stature of these colorful
New World inhabitants.
This, then, is the aim of the present
work.
MATERIALS A N D METHODS
Acquisition of material and its processing has been described in previous articles
(cf., Perkins, ’69c).
In all, 51 animals were examined in the
course of the “Skin of the Primates” studies on New World monkeys: white-browed
capuchins (Cebus albirons), 9 8 8 2 0 9 ;
common squirrel monkeys (Saimiri sciureus), 230” ; owl monkeys (Aotus triuirgatus), 3 d d 3 9 9 ; devil titi (Callicebus moloch), l d ; woolly monkeys (Lagothrix
lagothricha), 2 d d ; golden spider monkey
(Ateles geoffroyi), 1d ; necklaced titi (Callicebus torquatus), 13 ; silvered sakiwinkis
(Pithecia monachus), Id 1 9 ; red uacaris
(Cacajao rubicundus), 2 8 d 1 9 , ; Goeldi’s
monkeys (Callimico goeldii), 2 8 8 1 9 ;
white-shouldered marmoset ( C d i t h r i x humeralifer), 18 ; silver marmosets (Callithrix argentata), 2 d d ; pigmy marmosets
(Callithrix pygmaea), 9 d d ; red-mantled
tamarins (Saguinus fuscicollis illigeri),
4 d d 19 ; and cottontop pinches (Saguinus
oedipus), l a 1 9 .
In each study, certain criteria had to
be established and/or defined prior to the
recording and subsequent interpretation
of pertinent histological and histochemical observations.
The length of the sebaceous duct, sizes
of the sebaceous gland and arrector pili
muscle, and extent of the thin or thick
epidermis, papillary body and reticularis
dermis are expressed in dimensions proportionate to comparable adnexa of other
body regions. Sweat gland dimensions, however, are reported in relation to other
structures; e.g., the overall length of the
gland and its duct are stated as a function
of the level at which the glomeruli rest in
relation to the mid-dermis, lower reticular
layer or tela subcutanea. The narrow or
wide diameters of secretory coils and excretory ducts are expressed as their proportion to one another; i.e., the respective
ratio of secretory and excretory ducts may
be 1 : l in eccrine glands of hairy skin, but
4 : 1 in glands of friction surfaces.
The term “friction surface” denotes a
weight-bearing body region subject to excessive abrasion. It is characterized by an
absence of hair and sebaceous glands and
the presence of a greatly thickened epidermis. Examples include the palm and
fingerballs of the ventral manus, sole and
toe pads of the ventral pes, distal and ventral surface of prehensile tails, knuckle
pads, and ischial callosities.
The term “general body surface” refers
to that major portion of body skin that is
both hirsute and unspecialized, in contrast
to those regions that are either glabrous
or exhibit a high degree of specialization.
Examples of “general body surface” include the neck, back, chest, belly, forelimbs and hindlimbs. Examples of “specialized regions” include friction surfaces
of the pes, manus and prehensile tail,
ischial callosities, eyelids, lips, nose, ears,
axilla, ventral wrist, circumanal area, external genitalia, and such fields of glandular aggregation as the gular region, sternum, posterior abdomen, brachium and/or
antebrachium.
The criteria for the gradation of melanotic pigmentation and classification of hair
follicle groupings are those devised in two
earlier studies, respectively (Machida and
Perkins, ’67; Perkins et al., ’69).
The interpretation of histochemical procedures employed in the various studies
is solely dependent upon the localization
and intensity of color formation. Therefore, the quantitative assessment of enzyme reactivity is necessarily expressed by
such oversimplified terms as absent (0),
weak ( +), moderate ( + +>, and strong
THE SKIN OF NEW WORLD MONKEYS
+
+ +). Unlike the alkaline phosphatase
and cholinesterase techniques, which may
be used to demonstrate blood vessels and
nerves, respectively, the other histochemical methods are used primarily to appraise
tissue viability and characteristic levels
of enzyme activity.
The terms “primitive” and “specialized”
must also be qualified. The possession of
highly specialized cutaneous structures
does not imply that all other parts or systems of an animal are correspondingly
specialized. “Primitive” and “specialized”
here refer to the morphological grade of
an organ or system. They should not be
interpreted in a strict phylogenetic sense,
wherein the terms would refer to the evolutionary grade of a taxon within a given
lineage, and nothing more; as Hershkovitz
(pers. comm.) points out: “ . . . the most
primitive cat among cats, family Felidae,
is a highly specialized mammal.”
(
DISCUSSION
A detailed account of the integument of
every species formerly examined is precluded by the scope of this survey. Hence,
an abridged recapitulation of cutaneous
findings, the citation of new findings, and
respective investigators’ impressions will
be presented in the sequential order of
their historical availability and exploration.
Reuiew
Owl monkey or Douroucouli
(Aotus trivirgatus)
In this first detailed study of a New
World monkey, Hanson and Montagna
(‘62) noted that the skin resembles that
of the prosimian families Lemuridae and
Lorisidae (Montagna and Ellis, ’59, ’60;
Montagna et al., ’61a,b). For example,
whereas apocrine glands occur over the
general body surface, poorly-differentiated
eccrine glands are confined exclusively to
the volar friction surfaces of the pes and
manus. However, because all sudoriferous
glands (except those in the friction surfaces) evince some phosphorylase activity
and because their ducts open at the pilary
orifices rather than independently onto
the skin surface (as do those of the Lorisidae), they may represent an intermediate
type between apocrine and eccrine glands.
Hanson and Montagna also noted large
aggregations of sebaceous and apocrine
glands particularly well developed in the
397
sternal and subcaudal fields (fig. l), reminiscent of observations made in the skin
of various prosimians. Also similar to the
Prosimii are the long, slender and poorly
vascularized hair follicles, which are arranged in elongated clusters of 4-20.
The thin, relatively unpigmented epidermis is weakly reactive for monoamine
oxidase. Beneath, the scantily vascularized
dermis contains occasional elastic fibers
and variable numbers of melanocytes located around the adnexa. Although the
sebaceous glands generally resemble those
of other Primates, those associated with
sinus hairs contain cholinesterases; in this
respect, they are comparable to the sebaceous glands of the rat (Gerebtzoff and
Hoessels, ’58; Montagna and Beckett, ’58).
The investigators concluded that the
skin is so similar to that of prosimians
studied earlier that some platyrrhines
could possibly be considered “New World
Prosimii.”
Woolly monkey (Lagothrix lagothricha)
Machida and Perkins (’66) observed a
heavily-pigmented epidermis and the near
absence of dermal melanocytes (fig. 2),
resembling in this respect the lutong
(Machida and Montagna, ’64). The rich
vascularization of the skin is similar to
that of the green and Sykes’ monkeys
(Machida et al., ’64) and mangabey (Machida et al., ’65).
Hair follicles occur in clustered groups
of 4 to 15, as in the owl monkey and prosimians. In some body regions, follicles
have alkaline phosphatase-positive endorgans like those of various prosimians
(Yasuda et al., ’61; Montagna and Yun,
’62a). Large arrectores pilorum muscles
are present, as in the Cercopithecoidea
(Old World monkeys). The sebaceous glands
are histologically and histochemically similar to those of the green and Sykes’ monkeys and mangabey.
Whereas the Cercopithecoidea have both
apocrine and eccrine sweat glands over
the general body surface, the woolly monkey has both types only in the tail and external genitalia. Whereas the owl and
spider monkeys possess sternal and subcaudal glandular fields, the woolly monkey does not.
The nerve fibers around eccrine sweat
glands contain only acetylcholinesterase,
and thus resemble those of the green mon-
398
EDWIN M. PERKINS
key. With minor differences, the skin of
the glabrous area of the prehensile tail is
similar to that of the palm and sole.
The authors concluded that the skin of
the woolly monkey is histologically and
histochemically intermediate between that
of platyrrhines and cercopithecoids.
the ring-tailed lemur (Montagna and Yun,
'62b).
The outstanding feature of the red-mantled tamarin's apocrine glands is the presence of melanotic, dendritic melanocytes
situated around secretory coils in the external genitalia and ulnar gland. Melanocytes that invest apocrine glands have
been found heretofore only in the domestic
pig (Montagna and Yun, '64).
Aggregations of apocrine glands in the
suprasternal region are comparable to similar gatherings in the owl monkey (Hill
et al., '59), spider monkey (Schwarz, '37)
and orangutan (Wislocki and Schultz, '25).
Other than the brow and pubic region,
true eccrine sweat glands are found only
in the volar friction surfaces. This limited
distribution resembles that in the owl monkey and all prosimians except the tree
shrew (Montagna et al., '62). Whereas the
eccrine glands of most other animals are
rich in glycogen and phosphorylase, those
of the red-mantled tamarin are weak, resembling both Nycticebus and Loris; perhaps this is indicative of a more primitive
type of eccrine gland.
The skin of this callithricid, the first to
be extensively examined, shares characteristics with both the Prosimii and Catarrhini (Perkins, '66).
Red-mantled tamarin (Saguinus
fuscicollis illigeri)
Possessing a moderately pigmented epidermis, similar to that of the black lemur
and Spix's pinche, the red-mantled tamarin
also exhibits a relative abundauce of dermal elastin. Although cholinesterase-reactive Meissner corpuscles and mucocutaneous end-organs are present, mammalian
end-organs (Winkelmann, '59, 'SO), such
as those noted in some lorisoids, are not.
Single melanocytes reside in the dermal
papillary layer, whereas scattered aggregations occur in the upper reticularis
dermis.
The grouping of hair follicles into three
and four is unlike the Prosimii, and similar to that of higher primate groups such
as the macaques, baboons, gibbons, chimpanzees, and gorilla. In spite of this similarity, there is one apocrine gland with
each hair group, as in the Prosimii. Unlike
either the Prosimii or higher primates,
however, hair follicles are arranged in
Squirrel m o n k e y (Saimiri sciureus)
"linear perfect sets" (fig. 3). The occurThe thin, moderately MAO-reactive epirence of hairs in groups of three on the
muzzle is peculiar; hair follicles grow sin- dermis of all body surfaces lacks melanotic
gly on the muzzle of other primates studied melanocytes. However, Machida et al. ('67)
thus far. The presence of melanotic mela- recorded a relatively thin dermis which
nocytes on the pilary canal and hair bulge abounds in them. This type of melanocyte
is shared with howler monkeys, spider distribution resembles that of some cermonkeys, woolly monkeys, Celebes ma- copithecoids.
Hair follicles occur in linearly disposed
caques, gibbons (Parakkal et al., '62), and
the great apes (Ellis and Montagna, '62; groupings of 3-15. In this respect, they
Montagna and Yun, '63a; Ford and Per- are similar to the owl monkey and dissimkins, '70). The occurrence of sinus hairs ilar to Old World monkeys, whose hairs ocon the ventral ulnar surface of the wrist cur in randomly arranged groups of 3-6.
is shared with some lemurs.
The peripheral acini of the squirrel
Unlike those of most prosimians, larger monkey's sebaceous glands are alkaline
sebaceous glands are surrounded by cho- phosphatase-reactive, resembling those of
linesterase-reactive nerve fibers. Assem- the tree shrew, lemurs and owl monkey.
Eccrine sweat glands are confined to
blages of large sebaceous glands, collectively referred to as periinguinal or volar friction surfaces, like the Prosimii
perigenital glands (Pocock, '20; Wislocki, and owl monkey. Although smaller and
'30), are composed of numerous lobules not so well organized, an aggregation of
whose ducts empty into ampulliform pilary apocrine glands in the chest is somewhat
canals. Their general structure is some- similar to the sternal glands of the redwhat analogous to the brachial gland of mantled tamarin and owl monkey.
THE SKIN OF NEW WORLD MONKEYS
The skin of the squirrel monkey possesses two outstanding features. Papillary
nerve end-organs in the friction surfaces
are rich in butyrylcholinesterase (fig. 4);
similar, but not so clear-cut end-organs
have been encountered in only four other
species of subhuman primates: the whitecrowned mangabey, stump-tail macaque,
Philippine tarsier and silvered sakiwinki
(Machida et al., '67). Hair follicle nerve
end-organs in the muzzle are surrounded
by dendritic, melanotic melanocytes; in
the skin of 49 species of subhuman primates examined (Machida and Perkins,
'67), the latter characteristic has been
observed only in this species.
The authors concluded that the skin of
the squirrel monkey generally resembles
both that of callithricids and cebids.
399
alkaline phosphatase, eccrine glands of
the howler monkey resemble those of the
white-browed gibbon, Anubis baboon, owl
monkey, tarsier (Montagna and Machida,
'66; Arao and Perkins, '69) and angwantibo (Montagna et al., '66b).
In summary, the skin of the howler
monkey most closely resembles that of the
woolly monkey.
Golden spider monkey (Ateles geoffroyi)
Like the skin and appendages of the
woolly and howler monkeys, those of the
golden spider monkey abound in melanotic
melanocytes. In the spider monkey, however, the apocrine excretory ducts are also
pigmented. The moderately well-developed
dermis contains elastic fibers in both the
papillary and reticular layers. Hair groupings of 3-5 follicles, and acid phosphatase
Howler m o n k e y (Alouatta caraya)
and phosphorylase activities are also cuWhereas its epidermis is heavily pig- taneou s characteristics similar to those
mented (fig. 5) but no dermal melanocytes of the howler monkey.
occur, Machida and Giacometti ('68) stated
Sebaceous glands, somewhat larger than
the skin of the howler monkey resembles those of the howler and woolly monkeys,
that of the spider monkey, woolly monkey, are rich in alkaline phosphatase. The presCelebes macaque, lutong and gorilla. How- ence of acetylcholinesterase-positive nerve
ever, the further distribution of melanotic fibers around eccrine sweat glands, and
melanocytes about hair follicles, sebaceous the opening of apocrine gland excretory
glands and eccrine sweat glands resembles ducts at the pilary orifice are both feaonly the woolly and spider monkeys. Addi- tures the spider monkey shares with the
tionally, all three species possess a histo- woolly monkey. The abundance of alkaline
logically characteristic prehensile tail. The phosphatase in eccrine glands, however,
presence of epidermal glycogen in the is peculiar to the spider monkey.
friction surfaces (including the howler
The species-specific distribution of ecmonkey's prehensile tail) has also been crine glands in the hairy skin of all three
observed in the slender loris, slow loris, prehensile-tailed genera merits attention
ring-tailed lemur, mangabey, rhesus ma- (Montagna, '72): in the woolly monkey,
caque (Montagna et al., '64) and Anubis the glands are found only in the tail and
baboon (Montagna and Yun, '62c). A well- external genitalia; in the spider monkey,
defined dermis contains numerous elastic they are restricted to the chest, axilla,
fibers, as in the chimpanzee and stump- back, tail (fig. 6) and external genitalia;
in the howler monkey, they are present
tail macaque (Montagna et al., '66a).
Hair follicles grow in groups of three to throughout the hairy skin.
With minor differences, the skin of the
five; however, neither associated sebaceous glands nor hair follicle nerve end- glabrous surface of the prehensile tail of
organs are reactive for alkaline phospha- the golden spider monkey is similar to that
tase, as they are in the woolly monkey. of its palms and soles. Perkins and MaApocrine glands, which open at the pilary chida ('67) concluded that the skin of the
orifice, are histologically similar to those spider monkey is more similar to that of
of the woolly monkey. Eccrine sweat glands the howler than woolly monkey.
occur both in friction surfaces and throughPigmy marmoset (Callithrix pygmaea)
out the general body surface, unlike those
of the woolly monkey which are confined
Mild to moderate amounts of epidermal
to the external genitalia, prehensile tail pigment in the dorsum are similar to that
and volar friction surfaces. Unreactive for observed in the black lemur and red-man-
400
EDWIN M. PERKINS
tled tamarin; however, pigmentation is
suppressed in the ventral tail, chest, gular
region and friction surfaces. Scattered
melanocytes in the papillary body of friction surfaces and piebald aggregations
in the upper reticularis dermis (although
less pronounced in ventral body regions)
are comparable to those observed in the
white-shouldered marmoset, tamarins and
pinches.
Like the red-mantled tamarin, hair follicles grow in “linear perfect sets” of
three or four. The occurrence of one apocrine gland per hair follicle group is similar to many Prosimii; the presence of sinus
hairs on the ventral ulnar wrist, like the
white-shouldered marmoset (fig. 7), is
comparable to that noted in the red-mantled tamarin. However, unlike those of the
red-mantled tamarin, neither pilary canals
nor hair bulges are heavily pigmented,
and radial papillae are not discernible.
Alkaline phosphatase-positive hair follicle
nerve end-organs (fig. 8) are more prevalent than those formerly observed in the
potto, lesser bushbaby or woolly monkey.
As in other Anthropoidea, the larger
sebaceous glands are surrounded by cholinesterase-reactive nerves. A suprapubic
aggregation of large, multiacinar sebaceous glands resembles the suprapubic gland
of the red-mantled tamarin.
Like the white-shouldered marmoset,
the scalp and back of the pigmy marmoset
contain few or no apocrine glands; elsewhere, apocrine glands occur throughout
the hairy skin. A concentration of large
apocrine glands in the sternal region corresponds to those groupings that comprise
the brachial glands of the slow and slender
lorises, the inguinal glands of the potto,
and the sternal localizations of the redmantled tamarin, owl monkey, spider monkey and orangutan.
The limited distribution of eccrine glands
to the volar surfaces of the pes and manus
is similar to that of all Prosimii (except
the tree shrew), the red-mantled tamarin,
white-shouldered marmoset and many
Cebidae. Unlike those of the red-mantled
tamarin but like those of the angwantibo,
owl monkey and white-shouldered marmoset, the dark cells contain glycogen;
unlike those of the red-mantled tamarin
and owl monkey but like those of the angwantibo and white-shouldered marmoset,
the clear cells contain none. In addition,
both argyrophilic granules and an acid
mucopolysaccharide substance, previously
observed in the squirrel monkey, occur in
the karyoplasm of the dark cell nuclei.
Eccrine secretory coils are surrounded by
specific cholinesterase-containing nerves;
this phenomenon was previously observed
in the tree shrew, slow loris, squirrel,
golden spider and woolly monkeys. These
findings suggest that pigmy and whiteshouldered marmosets, like the red-mantled tamarin, possess somewhat primitive
sweat glands.
Perkins (’68) concluded that the skin
of the pigmy marmoset is primitive in
many respects, and vacillates between that
of the Prosimii and Anthropoidea.
Red uacari (Cacajao rubicundus)
Moderate amounts of epidermal pigment
are found in those body regions that
also contain large melanotic melanocytes
throughout upper dermal levels - a finding similar to that encountered in adult
tamarins, marmosets and pinches.
An extensive field of subepidermal vascular sinuses, reflected in the red faces of
uacaris (fig. 9), is comparable to superficial vascular beds in the sex skin, scalp
and face of rhesus and stump-tail macaques.
The skin of the red uacari is richly innervated by nerve endings that contain
both acetyl- and butyrylcholinesterase.
Noteworthy among these neural elements
are the specialized, hederiform endings
and papillary nerve end-organs. Hederiform endings, relatively common in the
face and scalp of the uacari, were formerly
observed over the neural spines of the
potto, between islands of hair follicles in
the great bushbaby, beneath the sex skin
of the rhesus macaque and Anubis baboon,
and in the face and scalp of the stumptail and pig-tail macaques (Perkins et al.,
’68).
Arranged in a “linear perfect independent” fashion, hair groupings consist of
two to five follicles. This cutaneous character is somewhat phylogenetically advanced in that it is shared with such
species as the howler monkey, squirrel
monkey, macaque, baboon and lutong
(Perkins et al.,’69).
Only apocrine glands occur throughout
the hairy skin; in this respect, the uacari tail macaque and whitecrowned mangaresembles all prosimians and other nonpre- bey, the white-browed capuchin possesses
hensile-tailed New World monkeys. Num- cholinesterase-reac tive, papillary nerve
bers of apocrine glands are greatly reduced end-organs at the bases of its volar epiderover the dorsum, a trait shared with the mal ridges.
Hair follicles are arranged in “linear
Callithricidae. An accumulation of apocrine glands on the chest, in a 1:l ratio perfect independent” fashion. Apocrine
with hair follicles, resembles comparable glands, distributed over the general body
localizations noted in the white-browed surface in a 1: 1 ratio with hair groupings,
capuchin, pig-tail macaque, Anubis baboon are more prevalent on the chest, where
and Sykes’ monkey. Like the red-mantled one gland is associated with each hair.
tamarin, squirrel monkey, white-browed Comparable apocrine accumulations were
capuchin, golden spider monkey and pig- observed in the chest of the red uacari,
my bushbaby (Machida et al., ’66),apo- Anubis baboon, Sykes’ monkey and whitecrine secretory coils in the general body browed gibbon.
surface are intensely reactive for alkaline
Confined to palmar and plantar friction
phosphatase.
surfaces, eccrine sweat glands contain
Eccrine sweat glands are confined to small amounts of glycogen dispersed
the friction surfaces of the pes and manus. throughout clear and dark cells. OccasionThe cells of the secretory epithelium, al excretory ducts commence spiraling
which contain glycogen, are so poorly dif- only upon entering the stratum corneum,
ferentiated that they are reminiscent of a characteristic previously noted in the
those in the Philippine tarsier, slow loris, squirrel monkey and chimpanzee. While
black lemur and ring-tailed lemur. Like the innervation of eccrine glomeruli by
the tarsier, however, secretory coils are rich numbers of acetylcholinesteraseconinvested by moderate numbers of acetyl- taining nerves is not unusual in the Order
and butyrylcholinesterase-reac tive nerves. Primates, the absence of phosphorylase
The eccrine glands of the red uacari are from secretory segments is. The only other
clearly the most primitive of any observed primate to share this trait is the red-manthus far in the Cebidae.
tled tamarin.
The authors (Perkins et al., ’68) sugThe authors (Perkins and Ford, ’69)
gested that the skin of the uacari is one concluded that the skin of the whiteof the more primitive among the Cebidae, browed capuchin most closely resembles
and possesses many cutaneous features that of allied Cebinae.
that resemble those of the Callithricidae.
Cottontop pinch6 (Saguinus oedipus)
White-browed capuchin (Cebus albifronsj
The following pigmentary peculiarities
Other than the ventral friction surfaces, are unique to the pinche: (1) the epidermis
mucous membranes, facial disk and scalp, is so deeply pigmented that the stratum
the skin of the white-browed capuchin con- corneum is laden with malanin granules,
tains little pigment.
and (2) many body regions contain large
Only a moderately thickened epidermis, bipolar melanocytes throughout the entire
an intense localization of acid phosphatase upper one-half or three-fourths of the
in the stratum corneum, and an absence dermis.
of apocrine glands attest to the function
Hair follicles are arranged in “linear
of the white-browed capuchin’s peculiarly perfect sets.” Because the presence of
hirsute, prehensile tail (fig. 10). Its skin glycogen and phosphorylase in the epitheis nowhere glabrous and no specialized lial sac of quiescent follicles is characternerve end-organs can be demonstrated in istic of man and primates but unlike all
the haired, ventral surface. This is sur- other mammals studied (Montagna, ’63),
prising and unlike the numerous Meiss- the unusually weak glycogen and phosner’s and Vater-Pacini corpuscles in the phorylase acitivites in the pinches quiesglabrous prehensile tails of golden spider, cent hairs are somewhat puzzling.
woolly and howler monkeys.
An elevated cluster of sinus hairs occurs
Like the Philippine tarsier, red uacari, on the ventral wrists of lemurs (Montagna
silvered sakiwinki, squirrel monkey, stump- and Yun, ’63b) and each of the following
402
EDWIN M. PERKINS
callithricids: the cottontop pinche, redmantled tamarin, white-shouldered marmoset (fig. 7) and pigmy marmoset. Histologically, such localizations are composed
of several large sinus hair follicles and
medium-sized apocrine glands. The apocrine glands are associated in a 1: 1 ratio
with the vibrissae; although moderately
large, they are often better developed in
other body regions, e.g., the sternal and
suprapubic aggregations. Cholinesterase
and alkaline phosphatase preparations do
not reveal subepidermal nerve end-organs
or specialized capillary plexuses; only the
sinus hairs exhibit a vascular complex and
profusion of nerves.
The suprapubic glands or “pubic cushions’’ of the cottontop pinche (Wislocki,
’36), composed of gigantic multiacinar
sebaceous glands and apocrine secretory
coils (fig. l l ) , are homologous to those
glandular concentrations previously noted
in the red-mantled tamarin and pigmy
marmoset.
One or two apocrine glands occur with
each hair follicle grouping in the chest.
Comparable concentrations of apocrine
glands have been observed in the chest
of the following New World monkeys: the
golden spider monkey, white-browed capuchin and red uacari; true sternal aggregations, composed of gigantic apocrine
glands that dwarf each of their respective
follicles, have been noted in the red-mantled tamarin and pigmy marmoset.
The terminal portion of apocrine excretory ducts is heavily pigmented in only
three other species of primates: the golden
spider monkey, howler monkey and Philippine tarsier.
Eccrine sweat glands reside in the volar
friction surfaces only. Glycogen is completely absent from the glandular unit,
and only the coiled excretory duct demonstrates phosphorylase reactivity.
The skin of the cottontop pinche (Perkins, ’69a) is basically similar to that of
the red-mantled tamarin .
Goeldi‘s monkey (Callimico goeldii)
The various aspects of the skin of C.
goeldii concur with Thomas’s conclusion
(’13) that “On the basis of preserved skin,
there is nothing sufficiently striking to
distinguish this animal from a marmoset.”
However, several distinct cutaneous
traits distinguish it from the family Cebidae.
Most hairy regions are characterized by
an epidermis heavily laden with melanin,
and a dermis whose upper levels contain
scattered numbers of melanotic melanocytes. This distinctive trait is shared with
only six of 56 species of subhuman primates: the white-shouldered marmoset,
pigmy marmoset, red-mantled tamarin,
red-handed tamarin, Spix‘s pinche and
cottontop pinche. Each of these species
belongs to the family Callithricidae; the
other 50 represent most prosimian families
as well as tarsioids, other platyrrhines and
the catarrhines (Machida and Perkins,
’67).
The hair follicles of Goeldi’s monkey,
like all callithricid species examined, are
arranged in “linear perfect” fashion (Perkins et al., ’69).
Delicate, subepidermal, cholinesterasepositive nerve fibers in the gular papillae
lend support to the possibility that comparable papillae in the silver marmoset
and red-mantled tamarin are tactile or
sensory in function.
Although single tufts of sinus hairs occur on the flexor surface of the forearm
of lemurs (Sutton, 1887; Pocock, ’18; Hill,
’53), circumscribed aggregations of sinus
hair follicles per se are characteristically
restricted to the ventral ulnar wrist of
the tarsier, Goeldi’s monkey and all callithric id s.
Basing their classification upon the gross
morphology of glandular sternal fields,
Epple and Lorenz (’67) placed Aotus, Callimico and six callithricid genera and subgenera into one category, and nine genera
of the family Cebidae into six other categories. The arrangement of the sternal
gland of a tamarin, marmoset or pinche
is distinctive; that of Callimico (fig. 12)
has each of the three typical components
described by Epple and Lorenz and is indistinguishable from the callithricid-type
marking gland. Similarly, the anogenitopubic glandular field of Callimico most
closely resembles that of a callithricid.
The eccrine sweat glands of Callimico,
like those of all Cebidae (except the prehensile-tailed genera) and C allithricidae,
are confined to the volar friction surfaces.
THE SKIN OF N E W WORLD MONKEYS
The secretory epithelium of C. goeldii,
unlike that of all Cebidae, contains no
glycogen; in this respect, Goeldi’s monkey
resembles only the red-mantled tamarin
and cottontop pinche.
Based upon these cutaneous characters,
Perkins (‘69b) concluded that the skin of
C. goeldii most nearly resembles species
belonging to the callithricid genus, Saguinus.
Silver m a r m o s e t (Callithrix argentata)
The skin of the silver marmoset is very
thin. A one to two cell-layered epidermis,
poorly-defined papillary body and meager
reticular layer overlie an extensive field
of subcutaneous fat. Like that of the lorisoids, the general body surface is free of
epidermal and dermal melanotic melanocytes. The silver marmoset’s diminution
of epidermal monoamine oxidase activity
appears to be a characteristic enzyme signature that is shared with a variety of
platyrrhines: the pigmy marmoset, redmantled tamarin, cottontop pinc he, owl
monkey and white-browed capuchin.
The occurrence of keratinized spines
on the corpus penis is noted in a variety
of primates: the common marmoset, whiteshouldered marmoset (fig. 13), squirrel
monkey, spider monkey, vervet, rhesus
macaque, Celebes macaque, Anubis baboon, lutong and others (Wislocki, ’36).
As Hill (’58) states: “A specialization of
the epithelium of the glans, or of the pars
intrapraeputialis of the corpus, or both,
is the tendency for local keratinization
giving rise to horny papillae (e.g., in langurs), spicules (e.g., in the chimpanzee)
or even quite large recurved hooks (e.g.,
in Galagidae and Indriidae).” Comparable
keratinized spines were histologically demonstrated on the glans penis of the howler
monkey and stump-tail macaque (Machida
and Giacometti, ’67).
One of the outstanding features of the
skin of the silver marmoset is an extensive
neurovascular plexus that accompanies
the hair follicle in all hirsute body regions.
Particularly well-defined in the scalp, eyebrow, cheek, chest, belly, back and tail,
such plexuses constitute the Haarscheibe
of Pinkus and contain components identical to those described by earlier investigators (Pinkus, ’04; Tamponi, ’39).
403
Hair follicles are disposed in “linear
perfect sets.” Grouping of follicles occurs
on the cheek, and ulnar vibrissae are
clearly demonstrated. The localization of
alkaline phosphatase-reactive cells on the
outer root sheath and epithelial sac of active and quiescent hair follicles is another
outstanding feature of the skin of the silver marmoset (fig. 14). These amelanotic,
stout, stellate cells are confined to the
cephalic and ulnar body regions, and resemble those cells formerly thought to be
unique to the African Lorisidae.
Distributed throughout the hairy skin,
apocrine glands are usually associated
with each hair grouping in a 1 : l ratio.
Notable variations occur, however. For
example,’ the glands are relatively scarce
on the head, but occur in a 2-3:l ratio
with hair groupings on the chest. This
sternal concentration of apocrine glands
parallels similar localizations in some
tamarins, marmosets, capuchins, the owl
monkey, uacari and titis, and the intermixed apocrine-eccrine sternal aggregations in some of the Old World macaques,
baboons and Sykes’ monkey. In the silver
marmoset, the presence of one large apocrine gland with each hair follicle in the
suprapubic skin is comparable to the inguinal gland of the relatively primitive
potto; on the other hand, the ratio in the
axilla resembles that of the gorilla and
man (Montagna, ’64).
Eccrine sweat glands are confined to
the volar friction surfaces. The sporadic
localizations of glycogen and phosphorylase
in the secretory segments of the glomeruli
is similar to that observed in the red
uacari.
The skin of the silver marmoset (Perkins, ’69c), although typically callithricid,
exemplifies both primitive and advanced
cutaneous traits common to other primate
taxa.
Synthesis
Some of the major diagnostic skin characteristics of each of the eight monophyletic taxa have been itemized in table 1 to
show the distinctive combination of cutaneous traits of each taxon.
An examination of skin characteristics
reveals that the eight taxa may generally
be reduced to four distantly related taxa,
404
EDWIN M. PERKINS
TABLE 1
Comparative cutaneous characteristics of major taxa in the Order Primates
Tupaiiformes
Lemuriformes
Lorisiformes
Glabrous specializations 2
Epidermal thickness
Alkaline phosphatase cells
Epidermal melanin
Dermal melanin
Adnexal blood supply
Defined papillary body
Abundant elastic fibers
Hair groupings 3
Number of hairs per group
Sinus hairs present
Ulnar vibrissae
Arrector pili muscles occur
Admixed suprapubic glands
Sebaceous gland size
Numerous apocrine glands
Apocrine ducts open at 4
Sternal apocrine glands
Axillary organ
Eccrine glands. . . . . .
confined to volar surfaces
throughout hairy skin
ratio to apocrine glands
differentiated secretory cells
phosphorylase and glycogen
Tarsiiformes
1
Platyrrhini
Cercopithecoidea
Pongidae
PT
rc
-
+
*
***
t+i
*
+- +
-
i
++
+
L
k
f
LPI
+
+
+
+
t
+
PO
+i
+
-
E<A
i
i
<7
++
+
+ +- +
+ +- +
+
++
+
LI
<5
Hominidae
-
+ +- +
+ +- +
+++
+++
++
N
N
5
+++-
++ +- +
PO
PO
PC
-
*
i
-
-
+
ESA
+
+
+
++
EbA
+
+
-
-
-
++
-
+++
E>A
+
+
I The eight monophyletic taxa are arranged with the suborder Prosimii to the left (four infraordinal taxa) and the suborder Anthropoidea to the right (one infraordinal. one superfamilial and two familial taxa: the latter three = the Catarrhini).
2 PT, prehensile tails; IC, ischial callosities.
3 CCI, independent circular clusters; CCS, circular clustered sets; LPS, linear perfect sets; LPI, independent perfect lines;
LI, imperfect lines.
4 PC, pilary canal; SS, skin surface; PO, pilary orifice.
on the basis of their common integumental
traits: the Prosimii (Tupaiiformes, Lemuriformes, Lorisiformes, and Tarsiiformes),
Platyrrhini, Cercopithecoidea, and Hominoidea (Pongidae and Hominidae).
Basic, underlying cutaneous patterns
also exist throughout the entire primate
order (table 1). Various trends are noted:
e.g., degree of epidermal thickness; a reciprocal relationship between the occurrence of epidermal and dermal melanocytes; amount of epidermal melanin tending
to increase concomitantly with phylogenetic ascension; definition of dermal papillary body and abundance of elastic fibers;
hair groupings becoming less organized
and smaller in numbers of comprising
follicles; increasing size and numbers of
sebaceous glands, but diminishment of alkaline phosphatase reactivity; numbers
and distribution of apocrine glands, with
excretory ducts opening at the skin surface, pilary orifice, or into the pilary canal;
development of sternal and suprapubic
glands, and axillary organ; and the distribution of eccrine sweat glands, including
their ratio to apocrine glands, degree of
secretory cell differentiation, and glycolytic reactivities.
The infraorder Platyrrhini (New World
monkeys) contains a highly variable number of cutaneous traits, many of which its
members share with other non-platyrrhine
taxa. For example, most subhuman monophyletic taxa can be characterized by one
type of hair grouping configuration; the
New World monkeys contain at least five.
Generally, each member in the other taxa
is pigmented like all other members in its
taxon. In the platyrrhines, however, melanocytes are almost always present and
occur in any combination: small or large
numbers may reside in the epidermis, the
dermis or both layers (tables 1-3). Hence,
in cutaneous terms, New World monkeys
represent the most variable monophyletic
primate taxon. For this reason, the following discussion will deal specifically with its
405
THE SKIN OF NEW WORLD MONKEYS
TABLE 2
Comparative cutaneous characteristics of species in the Callithricidae and Callimiconidae
~
C. pygmaea
Amount of epidermal pigment
Alkaline phosphatase cells
Penile spines present
“Tactile” papillae present
Amount of dermal pigment
Hair groupings *
Hairs grouped on cheek
Pigmented hair follicles
Ulnar vibrissae present
Glycogen and phosphorylase
in sebaceous glands
Suprapubic gland 3
Sternal gland development
Few apocrine glands dorsally
Pigmented apocrine glomeruli
Eccrine glands. . . . . .
confined to friction surfaces
phosphorylase activity
glycogen in clear cells
glycogen in dark cells
+- +
-
-
+
LP s
-
-
+
C . humeralifer
+- +
++
LP s
+
+
+
C. argentata
S. fuscicollis
S . oedipus
C. goeldii
-
+ -+ +
+ +- +
+ -+ +
-
-
+
+
++
+
-
-
-
S
A
f
A
f
-
-
+
+ +- +
+
+
+
?
-
+
+
+
LPS
+
++
+
+
S
+
f
+
LP s
-
+
I
~~
2
-
+
++
t
f
-
~~
++
LPS
-
++
+
+
S
+
’’
+
-
-
-
-
~
-
-
-
+
+
LPS
+
++
+
+
S=A
+
+
-
+
++
++
-
~ _ _ _ _ _ ~
I The marmosets, tarnarins and pinches. and Goeldi’s monkey are arranged according to their generic taxa: Callithrix to
the left; Saguinus in the center; Callimico to the right.
2 LPS, linear perfect sets.
3 S , predominantly sebaceous; A, predominantly apocrine.
various genera, subfamilies and families
rather than with the infraorder Platyrrhini per se.
The synonymic reductions of the genera
[Hapale], [Mico] and [Cebuella] to Callithrix by Simpson (’45) and [Tamarin],
[ Tamarinus] and [ Oedipomidas] to Suguinus by Hershkovitz (’58) are substantiated by an appraisal of the cutaneous
characteristics of these respective taxa.
Within limits, their degrees of homology
are proportional to their degrees of affinity. A comparison of cutaneous data in
table 2 confirms that the genera Cullithrix
and Saguinus are quite distinct.
Members of the genus Callithrix are
characterized generally by widespread, relatively inconspicuous sternal glands; admixed suprapubic glands, predominantly
apocrine in type; slight or moderate epidermal, dermal and adnexal pigmentation;
commonly occurring penile spines; sebaceous glands lacking glycogen and phosphorylase; and eccrine secretory epithelium containing moderate phosphorylase
activity and glycogen (when present) that
concentrates in the dark cells. By contrast,
members of the genus Saguinus generally
possess well-developed, prominent sternal
glands; admixed suprapubic glands, pre-
dominantly sebaceous in type; intensely
pigmented skin and appendages; an absence of penile spines; large sebaceous
glands containing both glycogen and phosphorylase in the peripheral acini; and eccrine secretory epithelium that contains
neither phosphorylase nor glycogen.
Another outcome of this survey is the
more detailed appraisal of that position
assigned the taxonomically long-disputed
Callimico goeldii (Hershkovitz, ’70b). By
cutaneous definition, it more closely resembles members of the family Callithricidae, not the family Cebidae; more specifically, it most closely resembles the
genus Saguinus (table 3).
Certainly the cheiridia and recent karyological evidence (Egozcue et al., ’68) support this impression, but the cebid-like
skull and dentition cannot be ignored. At
best, C. goeldii should not be considered
a member of the family Cebidae, nor
should its assignation to the Callithricidae
be warranted as the only alternative action. Perhaps the interpretation and treatment of C. goeldii by Hershkovitz (‘70) is
the most accurate proposed to date: it “has
been variously treated as a large marmoset
(or tamarin), as a small peculiar cebid,
and as a link between callithricids and
406
EDWIN M. PERKINS
TABLE 3
Comparative cutaneous characteristics of grnera and subfamilies in the Platyrrhini
Callithrix
Prehensile tail. haired
Prehensile tail, glabrous
Epidermal M A 0 activity
Epidermal thickness
Epidermal melanin
Dermal melanin
W ell-developed d eri-nis
“Tactile” papillae
Hair groupings 2
Hairs grouped on cheek
Ulnar vibrissae
Suprapubic gland
Large sternal gland
Few apocrine glands
dorsally
Eccrine glands. . . . . .
confined to friction
surfaces
phosphorylase activity
glycogen in clear cells
glycogen in dark cells
Saguinus
Cullimico
Aotinae
Pitheciinae
-
++ + S
*
LPS
+
+
+
+
+++
+*
LPS
-
+- +
+
t
-
+++
+
2
LPS
+
+
+
CCI
___
CE
Cebinae
*++
-
+- +
++
-
-
-
LPS
-
LPI
+
++
2
*
+
++
+
+
1
Atelinae
-
Alouat
tinae
+
+++
+
+ -+ +
+
-
+
+++
+
+ +- +
+-
LI
LI
-
LPI
CCI
+
+
+- +
+
+
+- +
-
+
+++
+
+
-
+ +- +
-
-
+++
+
+
1 The New World monkeys are arranged with the families Callithricidae (two generic taxa) and Callimiconidae (one
generic taxon) to the left, and the family Cebidae (five subfamilial taxa) to the right.
2 LPS, linear perfect sets, CCI, independent circular clusters; CE, elongated clusters; LPI. independent perfect lines,
LI, imperfect lines.
cebids. Any of these arrangements depends
on the assumption that the greater the
resemblances between platyrrhines of a
given size class evolving in a common arboreal habitat, the nearer the relationship.
Callimico is. . . .seen instead, as the lone
survivor of a lineage which parallels those
of marmosets and small primitive cebids. . . .In this light there is no need to
fit Callimico into either or between the
classic platyrrhine families, Callithricidae
and Cebidae. Instead, Callimico is recognized as type of a parallel family, the
Callimiconidae.”
Simpson (’62) suggested that the subdivision of New World monkeys into two
closely related families may only exaggerate their differences. However, the findings cited in this study suggest that Swainson (1835) and Thomas (‘03) might have
been even more confident of their familial
designations (Cebidae and Callithricidae,
respectively) had they been aware of the
dissimilar cutaneous qualities possessed
by the two groups (table 3 ) .
The skin of marmosets, tamarins and
pinches (family Callithricidae) may be
distinguished from that of the Cebidae
and all other primates by the following
cutaneous characteristics (occasional, noncallithricid genera which share some of
these characteristics are indicated in
brackets): abundant epidermal melanin,
concomitant with scattered melanocytes
in upper dermal levels; diminished epidermal nionoamine oxidase activity [ Pithecia] ;
grouped hairs often present on cheeks
[Pithecia]; eccrine glands confined to
friction surfaces (except Saguinus fuscicolis) and apocrine glands common throughout entire hairy skin, but often quantitatively diminished or totally absent on
dorsum [ Pithecia] ; eccrine, secretory clear
cells always, and dark cells frequently
devoid of glycogen; grouped sinus hairs
on ventral ulnar wrist [Tarsius and Lem u r ] ; “tactile” papillae often present in
specialized regions; prominent sebaceousapocrine suprapubic glands [ Perodicticus] ;
extensive or well-developed apocrine sternal glands [Tarsius and Aotus] ; and
hair follicles arranged in “linear perfect
sets” [ Pithecia and Tarsius] .
A comparison of cutaneous traits also
affords perspective regarding hierarchy
within the family Callithricidae (table 2).
For example, the amount of epidermal pigment, occurrence of alkaline phosphatase-
THE SKIN OF NEW WORLD MONKEYS
positive cells, absence of glycogen and
phosphorylase in sebaceous glands, absence of dorsal apocrine glands, and confinement of eccrine glands to volar friction surfaces are all traits that suggest
the genus Callithrix to be least cutaneously advanced of the callithricid genera.
The study of cutaneous properties also
permits comparable characterization and
appraisal of each of the five cebid subfamilies. Their outstanding characteristics
have been listed in table 3. Within the
family Cebidae, the cutaneous characters
of any one genus in a given subfamily
more closely resemble those of another
genus in that subfamily than they do
genera of other subfamilies. For example,
the hair follicle groupings of Saimiri and
Cebps (subfamily Cebinae) are both in the
form of independent perfect lines, whereas
those of Aotus and Callicebus (subfamily
Aotinae) are both arranged in circular
clusters. Similarly, Ateles and Lagothrix
(subfamily Atelinae) both possess glabrous
prehensile tails; Cacajao and Pithecia (subfamily Pitheciinae) are both distinguished
by poorly-differentiated eccrine sweat
glands.
It should also be noted that the subfamilies Aotinae and, to a lesser extent,
Pitheciinae are certainly the most cutaneously primitive of the Cebidae; in some
ways, their integumental characteristics
more closely resemble the family Callithricidae than they do other subfamilies of the
Cebidae (table 3 ) . Conversely, the highlyspecialized, glabrous prehensile tail, degree of epidermal development and pigmentation, well-developed dermis, and
distribution of eccrine sweat glands (including their glycolytic reactivities) would
all indicate that the subfamilies Atelinae
and, particularly Alouattinae, are the most
cutaneously advanced of the Cebidae.
Historically, fossil evidence indicates
that the early Tertiary prosimians radiated in the Paleocene, some 60 million
years ago. The resulting prosimian forms
became more highly diversified during the
Eocene; some inhabited Madagascar, others ventured from North America into the
tropics, and still others remained in the
Old World. During an equivalent time in
the late Oligocene or early Miocene ( 2 5
35 million years ago), four distinct groups
underwent separate, adaptive radiation:
407
the modern prosimians, including the
Malagasy isolate; New WorId monkeys;
Old World monkeys; apes and man (Simpson, ’49).
Of the latter three primate groups, fossil evidence is most wanting in the New
World monkeys. Only four main Tertiary
forms have been discovered: Homunculus
(Ameghino, l S 9 l ) , Neosaimiri (Stirton,
’51), Cebupithecia (Stirton and Savage,
’51), and Stirtonia (Hershkovitz, ’70). Unearthed in Patagonia and Colombia, they
date back to the late Oligocene or Miocene. That typically structured platyrrhines were in South America during this
time is therefore substantiated.
It is presumed that their varied and successful divergence occurred exclusively in
the moist rain forests of South America,
whose climate discourages the discovery
and study of fossilization processes. Hence,
it is possible that a lemuroid stock underwent greater adaptive radiation in the
early Tertiary than is generally reflected
by today’s New World forms. Indeed,
Hershkovitz (’70a) states: “The evidence
indicates that platyrrhines were considerably more diversified, at least in terms of
generic and supergeneric categories, during the Tertiary than they are now.”
Hence, present groups of platyrrhines
may be but extant fragments of an earlier
and more extensive radiation. Therefore,
the Callithricidae, Callimiconidae, Aotinae,
Pitheciinae, Cebinae, Atelinae and Alouattinae may each represent independent
lineages of, as yet, unknown or partially
unknown New World ancestry.
One point remains to be addressed:
namely, the sometimes disconcerting degrees of morphological parallelism exeniplified by the platyrrhines and catarrhines.
As Hershkovitz (’69) states: “Kinship between New and Old World monkeys is
remote and resides in a common early
Tertiary lemuroid stock. The remarkable
parallelism in the evolution of platyrrhines
and catarrhines derives from the conservation of primitive lemuroid traits, primate
evolutionary tendencies in general, and
exposure to similar selective factors in
tropical arboreal habitats.”
CONCLUSIONS
Because the observations presented in
this study have been cited and summarized
408
EDWIN M . PERKINS
in table-form, and their significance considered, the reader is referred to tables
1-3 and the DISCUSSION, respectively.
One may draw the following conclusions:
(1) the results define a baseline regarding
the normal histology and histochemistry
of the skin of most genera and many species of New World monkeys; (2) intrageneric and intraspecac subtleties in
cutaneous variation exist in primate integument; ( 3 ) single and multiple cutaneous traits contribute to the characterization and accurate identification of most
levels of taxa within the Order Primates;
(4) some traits negate recent taxonomic
practices, e.g., the familial position of
Callimico; (5) basic cutaneous patterns
generally confirm currently accepted concepts of taxonomy and phylogeny; (6) the
skin of the New World monkeys reflects
their history of adaptive radiation in isolation, and suggests that the designation
of at least two distinct families is warranted; and (7) the combined histological
and histochemical properties of a given
cutaneous system, like other characters
classically employed by systematic zoologists, are useful criteria in the assessment
of primate taxonomy and phylogeny. They
add much value to the systematist’s outlook in assessing relationships between
taxa.
The survey of skin characteristics in the
New World monkeys is far from complete.
Information regarding three of the 15 presently recognized genera (Leontopithecus,
Chiropotes and Brachyteles) is totally lacking. Even if these genera had been available, however, our knowledge would still
be fragmentary. Although certain underlying patterns indicate the relatedness of
a given species to other systematic categories, the total complement of its cutaneous traits serves only to set it apart from
all other primates assigned a higher-ranking taxon. If more species had been available, the preceding synthesis would have
been more thorough, and its discussion
more compendious. The present work, however, is a beginning.
ACKNOWLEDGMENTS
The author is indebted to the following
individuals for their contributions and encouragement, which have made this work
possible: B. C. Abbott, F. Allegra, T. Aoki,
T. Arao, F. Baden, R. Bils, L. Bishop, R.
Chew, E. H. Dolnick, J. Egozcue, R. A.
Ellis, J. F. Emmel, D. M . Ford, L. Giacometti, G. Hanson, F. Hu, M. J. C. Im, J.
Ito, H. Machida, R. Mita, W. Montagna,
P. Parakkal, W. C. Quevedo, N. A. Roman,
J. Savage, F. S. Shininger, A. F. Silver,
A. A. Smith, H. Uno, K . Ysauda and J. S.
Yun.
Particular appreciation is extended to
Philip Hershkovitz, Mammal Division, Field
Museum of Natural History, Chicago, Frederick Hulse, Department of Anthropology,
University of Arizona, Tucson, and David
Morafka, Department of Biological Sciences, California State College, Dominguez
Hills,: for generously donating their time
in reviewing this manuscript and offering
constructive suggestions.
LITERATURE CITED
Arao, T., and E. Perkins 1968 The nictitating
membranes of primates. Anat. Rec., 162: 53-70.
1969 The skin of primates. XLIII. Further observations on the Philippine tarsier (Tar sius syrichtcc). Am. J . Phys. Anthrop., 31: 93-96.
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1970b Cerebral fissure patterns in platyrrhine monkeys. Folia primatologica (Basel),
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24: 3 0 9 3 2 0 .
1967 The distribution of melanotic melanocytes in the skin of subhuman primates. I n :
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Machida, H., E. Perkins and W. Montagna 1964
The skin of primates. XXIII. A comparative
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453-466.
Machida, H., E. Perkins, W. Montagna and L.
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1972 The skin of nonhuman primates.
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Acta Anat., 32: 256-261.
~
409
Montagna, W., and R. A. Ellis 1959 The skin
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1960 The skin of primates. 11. The skin
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1962b The skin of primates. X. The
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J . Phys. Anthrop., 20: 95-118.
1962c The skin of primates. VIII. The
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J . Phys. Anthrop., 20: 131-142.
1963a The skin of primates. XV. The
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1966b The skin of primates. XXXIII.
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The skin of primates. 111. The skin of the slow
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1961b The skin of primates. V. The skin
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The skin of primates. XVIII. The skin of the
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41-70. [NOTE: The subjects of this study were
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Saguinus [ = Tamarinus] fuscicollis i l l i g d commonly called red-mantled tamarins. Author.]
- 1968 The skin of primates. XXXVI. The
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410
EDWIN M
skin of t h e cottontop pinche (Saguinzcs [ =Oedipomidas] oedipus). Am. J . Phys. Anthrop., 30:
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1969b T h e skin of primates. XXIV. T h e
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1961
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PLATE 1
EXPLANATION
O F FIGURES
1
Subcaudal field of the owl monkey (inset), demonstrating cytochrorne
oxidase activity in both sebaceous and apocrine glands. Note apocrine
excretory duct opening at skin surface, near pilary orifice (arrow).
ca. x 25.
2
Heavily pigmented epidermis and eccrinc gland excretory duct from
the external genitalia of a woolly monkey (inset). Note absence of
dermal rnelanocytes in this untreated preparation. ca. x 530.
THE SKIN OF N E W WORLD MONKEYS
E d w i n M. Perkins
PLATE 1
411
PLATE 2
E X P L A N A T I O N OF F I G U R E S
412
3
Linear perfect sets of hair follicles from the lurnbar back region of the
red-mantled tarnarin (inset). Succinic dehydrogenase. ca. X 40.
4
Butyrylcholinesterase-reactive papillary nerve end-organs (arrows).
situated at bases of epidermal ridges in fingerball of squirrel monkey
(inset). ca. X 100.
THE SKIN OF N E W WORLD MONKEYS
E d w i n M. Perkins
PLATE 2
413
EXPLANATION OF FIGURES
414
5
Large melanotic, dendritic rnelanocytes situated in the stratum basale
of the thickened epidermis of the howler monkey's (inset) prehensile
tail. Verhoeff elastic stain. ca. X 570
6
Eccrine sweat gland secretory coil and excretory duct associated with
a hair follicle in the proximal tail of the golden spider monkey (inset).
Phosphorylase. ca. X 50.
THE SKIN OF NEW WORLD MONKEYS
Edwin M. Perkins
PLATE 3
415
PLATE 4
EXPLANATION
416
O F FIGURES
7
Transmitted and incident light microphotograph of ulnar vibrissae
in the white-shouldered marmoset (inset). Note large blood sinuses
and relatively glabrous. unpigmented, circurnscribed field around sinus
hairs. Untreated. ca. X 25.
8
Alkaline phosphatase-positive hair follicle nerve end-organ in the
external genitalia of the pigmy rnarrnosct (inset). ca. x 220.
THE SKIN OF N E W WORLD MONKEYS
E d w i n M. Perkins
PLATE 4
417
PLATE 5
EXPLANATION OF FIGURES
418
9
Subepidermal. vascular sinuses in the frontal scalp of the red uacari
(inset). Hernatoxylin and eosin. ca. X 325.
10
Acid phosphatase preparation of ventral, distal tail of the white-browed
capuchin (inset). Note thickened stratum corneum. and absence of
apocrine secretory apparatus. c a X 60.
THE SKIN O F N E W WORLD MONKEYS
Edwin M. Perkins
PLATE 5
419
PLATE 6
EXPLANATION
420
OF F I G U R E S
11
Cytochrorne oxidase preparation of suprapubic glands in fernale cottontop pinche (inset). Note that the gigantic sebaceous glands contain
large amounts of the enzyme. but most apocrine secretory coils (lower
left) are only weakly reactive. ca. X 50.
12
Manubrial tuft from sternal field of a male Goeldi’s monkey (inset).
Note intense alkaline phosphatase activity in both sebaceous acini
and apocrine glorneruli. ca. X 25.
THE SKIN OF N E W WORLD MONKEYS
E d w i n M. Perkins
PLATE 6
42 1
PLATE 7
E X P L A N A T I O N OF F I G U R E S
422
13
Proxirnally-directed spine overlying spongy dermis of the white-shouldered marmoset’s corpus penis. P. A. S. ca. x 140.
14
Numerous alkaline phosphatase-positive cells surrounding the epithelial sac of a quiescent hair in the ternporal scalp of the silver marmoset
(inset). ca. x 170.
THE SKIN OF N E W WORLD MONKEYS
Edwin M. Perkins
PLATE 7
423
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