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AMER. ZOOL., 25:365-374 (1985)
Research in Mammalian Mastication1
KENNETH E. BYRD 2
School of Physical Therapy, Texas Woman's University, Houston, Texas 77030 and
Department of Physiology, University of Texas Health Science Center
at Houston Dental Branch, Houston, Texas
SYNOPSIS. Ongoing research efforts in mammalian mastication have defined several broad
areas of mutual interest to workers in the discipline. They are (1) interrelationships
between masticatory movements, (2) actions of the masticatory muscles, (3) comparisons
between masticatory structures and functions, (4) developmental aspects, (5) comparisons
between limbs and jaws, and (6) neurophysiologic considerations. The roles (potential and
actual) of masticatory central pattern generators, cerebral "mastication areas," different
neural mechanisms between mammalian taxa, neurophysiologic/morphologic interactions, and biochemical factors within the total milieu of mammalian mastication are discussed.
INTRODUCTION
Almost 20 years have elapsed since the
beginning of detailed studies of mammalian mastication (Hiiemae, 1978). These
studies have typically combined electromyographic (EMG) data from the muscles
of mastication with patterns of mandibular
movement during the act of chewing. The
oral behaviors of several mammalian
taxa during mastication have now been
described using varied methodologies
(Hiiemae, 1967; Hiiemae and Ardran,
1968; Crompton and Hiiemae, 1970; Hiiemae and Crompton, 1971; Kallen and Gans,
1972; DeVree and Gans, 1973; Herring
and Scapino, 1973; Hiiemae and Kay, 1973;
Weijs, 1973,1975; Gans and DeVree, 1974;
Kay and Hiiemae, 1974; Luschei and
Goodwin, 1974; McNamara, 1974; Weijs
andDantuma, 1975; Crompton et al, 1977;
DeVree, 1977, 1979; Gorniak, 1977; Byrd
etal, 1978; Tal and Goldberg, 1978, 1981;
Franks, 1979; Gorniak and Gans, 1980;
Byrd, 1981; Byrd and Garthwaite, 1981;
Fish and Mendel, 1982; Mendel and Fish,
1983; Thomas and Peyton, 1983).
Despite these past and continuing studies, the amount of detailed masticatory
EMG and mandibular movement data for
the Mammalia is relatively very little. The
purpose of the American Society of Zoologists symposium "Mammalian Mastication: An Overview" was to allow participants to appraise past and current research
efforts in the general area of mammalian
mastication and also to suggest areas for
future research.
The purpose of this article is to introduce and comment upon the areas of
research interest as presented at the symposium. Hopefully, this article will "seduce
and induce" the reader into reading the
following contributions as well as providing an appreciation of current problems in
the discipline of mammalian mastication.
INTERRELATIONSHIPS BETWEEN
MASTICATORY MOVEMENTS
As documented in Dr. Karen Hiiemae's
presentation,3 masticatory movements are
not limited to only the mandible and temporomandibular joint (TMJ). Movements
of the mandible during mastication may be
viewed as the outcome of several additional
"masticatory subsystems." The suprahyoid
musculature, infrahyoid musculature,
hyoid bone, and the tongue all play important roles in the masticatory act.
Mastication can be denned as "mechanical
digestion" of foodstuffs prior to
1
From the Symposium on Mammalian Mastication: "chemical digestion" which occurs in the
An Overview presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December gastrointestinal tract (Hiiemae et al., 1978).
Mastication can also be viewed as a phe1983, at Philadelphia, Pennsylvania.
!
Present address: Department of Basic Sciences,
School of Dentistry, University of Southern California, University Park—MC 0641, Los Angeles, California 90089-0641.
* Dr. Hiiemae's paper was presented at the Philadelphia meeting, but is not included in this volume.
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KENNETH E. BYRD
nomenon largely resulting from the actions
of the classically defined "muscles of mastication" (masseter, temporalis, lateral
pterygoid, medial pterygoid, anterior
digastric). On the other hand, movements
of the hyoid and tongue are largely involved
with intraoral food transport (Hiiemae et
al., 1981).
Normal mammalian feeding patterns use
both intraoral food transport and mastication systems. As Dr. Hiiemae's article
shows, both systems are synchronized and
modulated by complex neural mechanisms. The role of the nervous system in
effecting and affecting both these systems
is probably more important than previous
studies have imagined.
ACTIONS OF THE MASTICATORY MUSCLES
Dr. Gary Gorniak outlines the current
knowledge base concerning the action of
masticatory muscles within the Mammalia.
As he asserts, despite studies drawn from
most mammalian orders, the total range of
diversity in form and function of the mammalian masticatory apparatus is still largely
unknown.
Traditional studies of the mammalian
masticatory apparatus have concentrated
upon morphological aspects of the skull,
dentition, masticatory muscles, and vector
analyses of mastication. These studies continue to be of great importance in the documentation of mammalian masticatory
structures. Without such documentation,
the physiological data are in limbo and
unable to allow precise correlations
between structure and function.
Electromyography (EMG) and computerized data acquisition systems have allowed
more efficient collection of masticatory
movement and muscle activity data. Dr.
Gorniak provides an overview of the different techniques used; each has its advantages and disadvantages, not to mention
the inherent difficulties in comparing data
obtained by different methodologies.
Despite methodological dissimilarities
between different studies, certain communalities emerge from the pooled mammalian masticatory studies. Certain muscles are associated with specific mandibular
movements during mastication. These sim-
ilarities provide an evolutionary "touchstone" by which researchers may yet determine phylogenetic relationships through
careful comparison of mammalian masticatory patterns.
COMPARISONS BETWEEN
STRUCTURE AND FUNCTION
The methodological and conceptual difficulties in making valid comparisons
between mammalian masticatory structures and functions are discussed by Dr.
Carl Gans. As Dr. Gans points out, a major
difficulty in attempting any comparison is
how one separates and then measures masticatory structure, function, and their
development (ontogeny).
The problem is made more difficult due
to the mosaic nature of biologic systems:
Different systems within an organism are
now known to evolve at different rates
(Cherry et al., 1978). The addition of
homoplastic structures and functions further complicates the picture.
Dr. Gans makes the point that masticatory functions are made up, in part, of
"biological roles." These masticatory biological roles would be important recipients
of any selective processes. In other words,
structure subserves function in an evolutionary sense. A major concern for the evolutionary biologist is to precisely identify
which part, or parts, of masticatory functions are actually biological roles.
As Dr. Gans mentioned in his presentation in the symposium, the actual role of
food items upon the mammalian masticatory apparatus is not to be neglected. Food
item influences may be either long term
(phylogenetic) or relatively short term
(ontogenetic). Research in this area has
been of prime interest to physical anthropologists in past and recent years (Molnar,
1972; Kay and Hiiemae, 1974; Hylander,
1975, 1977, 1979; Swindler and Sirianni,
1975; Kay, 1977a, b; Molnar and Gantt,
1977; Sheine and Kay, 1977; Walker et al.,
1978; Beecher, 1979; Hinton and Carlson,
1979; Corruccini, 1980; Beecher and Corruccini, 1981; Fish and Mendel, 1982; Gordon, 1982; Molnar et al., 1983; Gordon,
1984). More data on nonprimate taxa need
to be collected, however.
RESEARCH IN MAMMALIAN MASTICATION
DEVELOPMENTAL ASPECTS
Dr. Sue Herring's contribution outlines
the importance of ontogenetic factors in
mammalian mastication. Analyses of the
shift from suckling to chewing oral behaviors in most mammals (exceptions: precocious taxa like Cavia) may prove very useful
in understanding the evolution of different
masticatory specializations. In this sense,
altricial mammals may serve as models for
the study of development of mammalian
mastication.
Previous ideas concerning the shift from
suckling to chewing oral behaviors have
generally fallen into two camps: (1) that
mastication gradually develops from a previously established suckling neuromuscular network (Dellow, 1969; Sessle, 1976),
or (2) mastication arises de novo with development of completely separate neuromuscular elements associated with dental eruption (Bosma, 1967; Moyers, 1973). Dr.
Herring presents new data on this problem.
The possibility exists that developmental
timing of masticatory muscles, nerves, and
neurons is the critical factor in the ontogeny of mammalian mastication. Such differences in development sequencing may
account for the suppression of those neural
mechanisms responsible for suckling and
their replacement by adult ingestive behaviors (Hall, 1979; Epstein, 1984). It would
appear that ontogenetic changes in mastication and deglutition are part of the normal aging process in all mammals. Within
aged humans, however, significant differences exist between males and females in
terms of their respective oral behavior patterns (Baum and Bodner, 1983).
Recently, the hypothesis that mammalian mastication develops from previously
established suckling mechanisms received
support from a nonmammalian source. In
frogs, it has been documented that no new
trigeminal motoneurons appear during
larval maturation or metamorphosis (Alley
and Barnes, 1983). In addition, there is a
90% retention of primary trigeminal motoneurons between larval and adult nervous
systems (Barnes and Alley, 1983). The idea
of "respecification" of trigeminal motoneurons to different peripheral targets was
367
proposed to explain these data (Alley and
Barnes, 1983). A similar developmental
mechanism may exist in mammals which
could account for the neuromuscular shift
between suckling and mastication.
LIMBS AND JAWS
Dr. Art English compares and contrasts
data from mammalian jaw and limb muscles in his contribution. As he points out,
mechanical models have been used to
explain the diversity of both mammalian
masticatory and locomotive specializations. Many of these studies, however, have
not integrated available models or tested
actual mechanisms of mammalian jaw and
limb functions.
Anatomical studies have suggested that
jaw muscle fiber architecture exhibits
"functional localization" while limb muscle fiber architecture suggests more uniformity in its functional manifestations.
Muscle histochemistry, however, has demonstrated that within both jaw and limb
muscles, there is considerable functional
heterogeneity (Burke et al., 1973; Maxwell
et al, 1973; Kugelberg, 1976; Maxwell et
al, 1979; Clark and Luschei, 1981). These
studies indicate that within individual jaw
and limb muscles there is considerable heterogeneity of fiber types and distribution
patterns; these fiber types and distribution
patterns are also influenced by the age and
sex of the individual (Maxwell et al, 1979).
Related to muscular heterogeneity is the
concept of neuromuscular compartments.
As Dr. English explains, intramuscular
motor units tend to operate in functionally
distinct groups called neuromuscular compartments (NMC). Jaw and limb NMC
appear similar in their basic architecture
as indicated by preliminary data at this time.
The anatomical presence of NMC is important because it implies that there are multiple, independent functional subdivisions
within both jaw and limb muscles. NMC
might account for the variability of intramuscular EMG data reported by individual
researchers.
NEUROPHYSIOLOGIC CONSIDERATIONS
Much like muscular heterogeneity, neuromuscular compartments, ontogenetic
368
KENNETH E. BYRD
sents the repository of distinct oral movement patterns (gnawing, unilateral chewing on right, unilateral chewing on left,
suckling, etc.). It can be considered a hypothetical neural network that sets up a
mechanical template for various oral
movement patterns. The level B interneurons act as the pathway by which the distinct motor programs are provided to the
program selector while the level A interneurons provide feedback to the motor
programmer (Fig. 1). The oscillator/timer
serves much like an "idle" or "internal
drive" as defined by Tatton and Bruce
(1981) and is responsible for the repetitive,
Central pattern generators
Central pattern generators (CPGs) rhythmic nature of the selected oral movelocated within the central nervous system ment pattern.
The program selector is connected to
and capable of generating rhythmic motor
activities have been defined in many organ- the actual motor subroutines by the selecisms (Delcomyn, 1980). CPGs are capable tor interneurons (C in Fig. 1); these output
of generating properly timed and some- neurons specify a series of motor subroutimes complex rhythmic movements in the tines necessary to complete a particular oral
absence of peripheral nervous system feed- movement pattern. Motor subroutine neuback. A masticatory CPG can be defined rons code for specific mandibular moveas one which produces rhythmic alternat- ment patterns (elevate, depress, lateral
ing activity in the motoneurons innervat- movement, medial movement, retrude,
ing the closing and opening muscles of the protrude) while level A' and B' interneujaw (Luschei and Goldberg, 1981). The rons allow feedback between the motor
complex nature of mandibular movement programmer and motor subroutines. Level
and muscle activity patterns that occur 2 and 5a interneurons allow feedback
during mammalian mastication strongly between the motor subroutines and the
suggests that the masticatory CPG is more sensory processing network (thalamus, sensory cerebral cortex, cerebellum, etc.);
than just a "neural oscillator."
these interneurons provide the appropriate input to advance the program to the
A new masticatory CPG model
Figure 1 depicts a proposed hypothetical next subroutine. It should be noted that
model for the mammalian masticatory the program selector determines the actual
CPG. This model is modified from one order (sequence) in which each motor subprovided by Tatton and Bruce for loco- routine occurs, however.
motor movements (1981). The model
The level D interneurons, or command
shown in Figure 1 assumes that the mas- interneurons of Kennedy (1969,1976), are
ticatory CPG is located somewhere within the output neurons of the motor subrouthe pontine reticular formation and is tine "directory." Each level D interneuron
therefore subcortical in nature. In this model would enable a single motor subroutine to
(Fig. 1), the actual masticatory CPG is made be translated by the STST. The STST genup of functionally distinct groups of neu- erates both spatial and temporal comporons which comprise a motor programmer, nents of the motor program instructions
program selector, oscillator/timer, motor that actually pattern motoneuron activity
subroutines, and STST (spatial and tem- (Tatton and Bruce, 1981). In other words,
poral sequence translator) together with STST neurons "decide" when it is behavtheir respective connecting interneurons.
iorally appropriate to inhibit those motoThe motor programmer (Fig. 1) repre- neurons effecting certain undesired moveshifts, form/function interactions, and
physiologic data, the neurophysiology of
mastication is becoming more complex with
continued research efforts. The reader is
invited to read a recent review of masticatory neurophysiology research by Luschei and Goldberg (1981) in order to obtain
an appreciation of previous research efforts
and models of masticatory motor control.
This section will concentrate upon some
aspects of masticatory neurophysiologic
research since Luschei and Goldberg's
review article.
369
RESEARCH IN MAMMALIAN MASTICATION
ments. The STST is equivalent to the
switching and sequencing network of Tattonand Bruce (1981).
Driver neurons (Kennedy, 1976) are
concerned with nontemporal alteration of
the selected oral movement pattern. For
example, they would cause one chew cycle
to become more narrow while the next
cycle might be wider. Driver neurons are
therefore directly connected and relay
activity patterns to individual masticatory
motoneurons. Level 3 interneurons
between the sensory processing network
and the driver neurons serve to modify the
manifestation of specific subroutine
instructions during their actual execution.
The magnitude or "gain" of driver neuron
signals are relayed to both the central sensory processing network and peripheral
sensory afferents by level 5b interneurons.
Individual motoneurons then effect individual muscle units within the muscles of
mastication in whatever order specified by
the CPG and a given oral movement pattern results. It should be noted that the
sensory processing network interfaces with
the motor programmer, program selector,
and motor subroutine elements of the masticatory CPG (Fig. 1). Level 4 interneurons
reaffirm the actual profile of the programmed movement to the motor programmer while level 1 interneurons initiate the proper motor program in response
to the relevant portion of sensory input.
Evidence for the proposed model
Although a masticatory pattern generator has been suspected for almost 100
years (Ferrier, 1886; Rethi, 1893; Economo, 1902), the location of a masticatory
CPG within the brainstem was not hypothesized until the 1920s-1930s (Bremer,
1923; Magoun et al, 1933; Rioch, 1934).
Recent physiologic and anatomic research
has provided additional data regarding the
nature of the masticatory CPG as outlined
in Luschei and Goldberg (1981) and
described earlier here.
Lund et al. (1983) have provided data
which indicate that anterior digastric reflex
amplitude and latency are cyclically modulated by the masticatory CPG and not by
MOTOR
PROGRAMMER
( Unilateral Cycles)
OSCILLATOR
TIMER
MOTOR SUBROUTINES
( A a ) elevate mandible
(Bb) move mandible medially
( C c ) depress mondible
( Dd) move mandible laterally
( E e ) move mandible anteriorly
( F f ) move mandible posteriorly
SPATIAL and TEMPORAL
SEQUENCE TRANSLATOR
DRIVER NEURONS
( Nontemporal Alteration of Cycle; Alters
Gain of Motor Subroutines) eg - make
cycle narrow, wide, etc.
FIG. 1. Hypothetical model for generation of mammalian masticatory patterns as modified from Tatton
and Bruce (1981). The labeled arrows represent interneuronal pathways (either mono- or polysynaptic)
between functional neuronal networks. Arrows labeled
by letters (A-E) represent interneurons concerned
with generation and execution of oral motor programs; number labeled arrows (l-5b) represent interneurons connecting sensory and motor networks.
Motor subroutines (Aa-Ff) represent discrete mandibular movement patterns. The proposed system
would effect unilateral chewing (as depicted here) by
the program selector first selecting the unilateral cycle
"template" from the motor programmer "repository" (arrows A and B). The program selector then
specifies a series of motor subroutines by the selector
interneurons (arrow C). For unilateral cycle mastication on the left, the hypothetical order of motor
subroutine activation enabled by the spatial and temporal sequence translator (STST) would be (Cc Ff)(Cc Dd Ff)-(Aa Dd Ee)-(Aa Ee)-(Aa Bb Ee)-(Bb Cc
Ee)-(Cc Ff). Therefore, in this model (Aa Bb Ee) and
(Bb Cc Ee) respectively effect the buccal and lingual
phases of power stroke; (Cc Ff) and (Cc Dd Ff) effect
opening stroke; (Aa Dd Ee) and (Aa Ee) effect closing
stroke. See text for additional detail.
peripheral sensory feedback. They suggest
that masticatory reflex circuits are cyclically modulated by either CNS interneurons or primary afferents. The existence
370
KENNETH E. BYRD
of the STST postulated here is strength- damage to their respective trigeminal
ened by data reported by Hellsing and motor nuclei demonstrates the importance
Lindstrom (1983) which suggested that jaw of CPGs in the manifestation of mammaelevator synergists alternate or "rotate" lian patterns of mastication.
their activity patterns during sustained isometric contractions in order to prevent Role of cerebral cortex
muscular fatigue.
Lesion studies of the sensorimotor corInjection of horseradish peroxidase tex in mammals suggest that the the cere(HRP) into the trigeminal motor nucleus bral cortex plays a role in the control of
of cats has allowed recent identification of mastication (Luschei and Goldberg, 1981).
premotor interneurons which connect with The cerebral cortex seems to be involved
the trigeminal motor nucleus (Mizuno et in the voluntary modification of basic chew
al., 1983). These interneurons are likely cycles manifested by the CPG. A "masticandidates for the driver neurons and level cation area" of the cerebral cortex has been
3 interneurons shown in Figure 1. Most of identified for several mammals and appears
the HRP labeled interneurons were in the to be important in the voluntary control/
bilateral parvocellular reticular formation; modulation of mastication although not
many were in the contralateral rostral- essential for the actual initiation of mastimost-cervical and caudalmost-medullary cation (Luschei and Goldberg, 1981).
reticular formation (Mizuno et al., 1983).
Recent research has provided evidence
Some of these labeled interneurons were that the cerebral motor cortex, although
determined to project to the ipsilateral not essential for mastication, allows the
mesencephalic nucleus, contralateral tri- manifestation of the masticatory CPG to
geminal sensory nucleus, contralateral tri- be modified in some manner (Chandler and
geminal motor nucleus, and bilateral spinal Goldberg, 1982; Goldberg et al., 1982;
trigeminal nucleus.
Lund et al., 1982). In the guinea pig, the
Siegel and Tomaszewski (1983) have cortical mastication area can activate both
obtained single unit activity data from the (1) a polysynaptic pathway from cortex to
medial reticular formation in unrestrained trigeminal motoneurons innervating mascats. They identified 6 cells, located within ticatory muscles, and (2) the brainstem
the medial pontine and midbrain regions masticatory CPG (Chandler and Goldberg,
of the reticular formation, that were most 1982).
active during crushing of food pellets but
Nozaki et al. (1983) have identified that
were inactive during rhythmic chewing of portion of the reticular formation in cats
ground meat and other soft foods. These involved with the pathway between ceredata further suggest that the masticatory bral motor cortex and trigeminal motoCPG is indeed located within the reticular neurons. HRP injection into the bulbar
formation as do connections between the reticular formation revealed two types of
ventral-medullary reticular formation and interneurons: inhibitory neurons projecttrigeminal motor nucleus in sheep (Jean et ing to masseter motoneurons and excitaal, 1983).
tory neurons projecting to anterior digasElectrolytic lesioning of the trigeminal tric motoneurons. Intracellular recording
motor nucleus in guinea pigs alters the revealed that these neurons were active
manifestation of their masticatory CPG during stimulation of cortical mastication
(Byrd, 1983, 1984). Despite their ability to areas and suggested that cortical control
exhibit unilateral chew cycles, the lesioned of trigeminal motoneurons modulated by
guinea pigs continued to produce the rel- these particular reticular formation interatively more complex bilateral chew cycles. neurons is separate from reflex control by
Significant shifts in EMG activity durations peripheral inputs (Nozaki et al., 1983).
occurred between working and balancing
Ohta (1984) has recently stated that, in
side muscles, however (Byrd, 1984). The rats, frontal cortex and central amygdaloid
fact that the lesioned animals continued to nucleus have "convergent control" of
produce complex bilateral chews after mandibular depression due to the contra-
RESEARCH IN MAMMALIAN MASTICATION
371
lateral activation of jaw opening motoneurons and inhibition of jaw closing ones.
Ohta points out, however, that the lateral
amygdaloid nucleus is active during jaw
closing in cats and rabbits.
of morphologic alterations due to changed
CPG manifestation is limited by both
genetic (individual genome) and environmental (nutritional status, diet, etc.) factors.
Different neural mechanisms between taxa
Biochemical considerations
Ultimately, the basis for all aspects of
Ohta's paper illustrates an important fact
to students of mammalian mastication: Sig- masticatory activity patterns is on the
nificantly different neural mechanisms molecular or biochemical level. Microineffecting mastication can occur across jection of glutamic acid into the periformammalian taxa. For example, ablation of nical region of the hypothalamus in cats
the cortical mastication areas in dogs and elicits jaw opening (Bandler, 1982). Masmonkeys revealed that dogs recovered ticatory activity of the gastropod Aplysia is
much faster than their monkey counter- apparently modulated by a serotonergic
parts (Frank, 1900). Rabbits can eventually neuron (Rosen et al., 1983). The role of
recover from bilateral lesions of the cor- chemical neurotransmitters in control of
tical mastication area (Bremer, 1923) while masticatory activity patterns has not yet
guinea pigs cannot and are unable to feed been defined.
themselves (Rioch, 1934; Byrd and LusDIRECTIONS FOR FUTURE RESEARCH
chei, unpublished data). Conversely, rats
recover from such bilateral ablations of the
It is safe to say that not one area of
cerebral cortex and can feed themselves research within the broad discipline of
quite effectively (Castro, 1972).
"mammalian mastication" has been
Detailed maps of trigeminal motoneu- exhausted. Precise anatomical studies are
rons specific for each masticatory muscle still needed for the majority of mammalian
continue to be compiled for various mam- masticatory specializations. Accurate and
malian taxa. Recent examples are Tal precise physiologic studies have only been
(1980), Mizuno et al. (1981), Jacquin et al. accomplished for relatively few mamma(1983), and Kemplay and Cavanagh (1983). lian taxa as have masticatory muscle hisThese maps show significant differences tochemistry, ontogenetic, neurophysiobetween mammalian taxa not so much in logic, and functional morphology studies.
the topographic distribution of motoneu- Additional data for the role of masticatory
rons, but in the extent of motoneuron rep- CPGs in the determination of craniofacial
resentation for each muscle (Tal, 1980). form and function need to be collected.
These differences also suggest important Precise identification of the components
neurophysiologic differences between taxa. within the brainstem reticular formation
making up the masticatory CPG need to
Interactions between CPGs and craniofacial
be identified for mammalian taxa. The role
morphology
of neuromuscular compartments and the
Significant morphologic changes of the functional heterogeneity of masticatory
craniofacial complex caused by altered muscles in the determination of masticamanifestation of the masticatory CPG in tory activity patterns need to be correlated
guinea pigs suggest that intra- and inter- with both neurophysiologic and morphospecific differences in craniofacial form may logic data.
be due, in part, to different CPGs within
A new and potentially very important
the Mammalia (Byrd, 1983, 1984). Altered area for research is the area of biochemical
manifestation of respiratory CPGs has also factors mentioned previously and illusproduced profound morphologic alter- trated by Bandler (1982) and Rosen et al.
ations of the craniofacial skeleton in rhesus (1983). Just as the discovery of DNA had
macaques (Miller, 1978; Miller et al., 1982; tremendous impact upon all facets of biolVargervik etal, 1984). In such studies, the ogy, future identification of biochemical
assumption is made that the actual amount factors affecting the various components
372
KENNETH E. BYRD
of mammalian mastication will also have
great importance.
Frog perspective on the morphological difference between humans and chimpanzees. Science
200:209-211.
Clark, R. W. and E. S. Luschei. 1981. Histochemical
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SCIENCE AS A WAY OF KNOWING
An Ongoing Project of the
Education Committee
of the
American Society of Zoologists
Cosponsored by
The American Society of Naturalists
The Society for the Study of Evolution
The Biological Sciences Curriculum Study
The American Institute of Biological Sciences
The American Association for the Advancement of Science
The Association for Biology Laboratory Education
The National Association of Biology Teachers
The Society for College Science Teachers
The Ecological Society of America
The Genetics Society of America
and the
University of California at Riverside
II
SCIENCE AS A WAY OF KNOWINGHUMAN ECOLOGY
CONTENTS
John A. Moore
Science as a way of knowing—Human ecology. Opening
remarks
377
Paul R. Ehrlich
Human ecology for introductory biology courses: An
overview
379
Anne H. Ehrlich
The human population: Size and dynamics
395
John L. Fischer
Science as a way of knowing: Man and food
407
James N. Pitts, Jr.
On the trail of atmospheric mutagens and carcinogens:
A combined chemical/microbiological approach . . . 415
Trends in health—Ecological consequences for the human
Lester Breslow
population
433
Robert M. May
Ecological aspects of disease and human populations . . 441
G. Carleton Ray
Man and the sea—The ecological challenge
Garrett Hardin
Human ecology: The subversive, conservative science . . 469
Gary Anderson and
Films and videotapes in human ecology
477
Science as a way of knowing—Human ecology
483
Index
639
451
Nathan H. Hart
John A. Moore