NABIL N. YOUSS Topograp hy of the

Cephalic Musculature

and Nervous System

W of the Honey Bee

Apis mellifera Linnaeus

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY NUMBER 99
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SMITHSONIAN CONTRIBUTIONS TO

ZOOLOGY

NUMBER 99

Nabii N. Youssef Topography of the

Cephalic Musculature

and Nervous System

of the Honey Bee

Apis mellifera Linnaeus

SMITHSONIAN INSTITUTION PRESS

CITY OF WASHINGTON
ABSTRACT

Youssef, Nabil N. Topography of the Cephalic Musculature and Nervous System

of the Honey Bee Apis mellifera Linnaeus. Smithsonian Contributions to Zoology,

number 99, 10 figures, 5 tables, 54 pages. 1971.—Fixed heads of workers, drones,

and queens of Apis mellifera Linnaeus were dissected under distilled water for the

study of two tissues: the musculature and the nerve mass.

Musculature: The movable and fixed points of muscle attachment were utilized

in establishing a nomenclature for muscles to replace the systems in current usage,

which depend on various combinations of topography, function, and numerical sequence. The present system proved to be consistent and useful for demonstrating the

criteria of homology among muscles. Names were devised in classical Greek and

Latin for international usage. For establishing muscle homology, every cephalic

muscle of the three castes was compared with its homolog in other studied taxa of

Hymenoptera and Neuroptera. The labial and epipharyngeal muscles are degenerate

and the antennal muscles maintain primitive features. The mandibular complex

consists of two well-developed muscles and a degenerate muscle which is probably

modified to serve as a stretch organ. The maxillary muscles maintain the same points

of attachment as in primitive insects, although the musculus tentorio-cardinalis has

shifted its point of movable attachment to the stipes in the female bees to meet a

change in function. The maxillary palpal muscles have disappeared as a result of

the reduction of the palpus itself. Many of the labial muscles have shifted one or

both points of attachment as a result of the specialization of the labium. The musculus postoccipiti-prementualis even has different points of fixed attachment among

the different castes.

As a result of simplification of the "hypopharynx," many of its muscles have

shifted their points of attachment. The musculature of the clypeal walls are well

developed to accommodate the enlargement and specialization of the cibarium.

In this study the following undescribed muscles were found and named: musculus

tentorio-mandibularis, m. stipiti-maxillopalpualis, m. oriscuto-supensorialis, and m.

fronti-pharyngealis III (only in the drone).

Nerve Tissue: Existing literature indicates that only a few of the cephalic nerves

have been named. Accordingly, a new system was developed under which the name

of each nerve or nervule is based on the structure it innervates. Main ganglia are

named according to their locations, rather than following the traditional inconsistent

nomenclature. The names are in classical Greek or Latin form for international usage.

Every cephalic nerve or nervule was followed to its termination. When sufficient

literature was available, the criteria of nerve homology were examined. Nerve topography follows a similar plan in the gnathal segments of the three castes, except that

the Nervus Mandibularis is degenerate in the drone. It was noted that variation in

the topographical plan of a particular nerve is very small, even among members of

different castes.

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Contents

Page

Introduction 1

Materials and Methods 2

PART I. MUSCULATURE

History 5

Methods of Nomenclature 8

Methods Used in Previous Studies 8

Methods Used in the Present Study 10

Topography and Homology of Musculature 10

Labral Muscles 11

Epipharyngeal Muscles 13

Antennal Muscles 13

Mandibular Muscles 14

Maxillary Muscles 15

Labial Muscles 18

Hypopharyngeal Muscles 20

Anterior Cibarial Wall Muscles 22

Pharyngeal Muscles 23

Dorsal Muscles of the Pharnyx 23

Ventral Muscles of the Pharnyx 24

Circular Muscles of the Pharnyx 24

PART II. NERVOUS SYSTEM

History 25

Methods of Nomenclature 25

Main Ganglia and Their Divisions 25

Nerves and Their Branches 28

Topography and Homology of the Cephalic Nerve Tissue 29

Location and Topography of the Ganglion Hyperoesophagale 29

Ganglion Proto-Hyperoesophagale 30

Lobus Opticus 30

Nervi Optici 30

Nervi Ocellares 31

Ganglion Dejtto-Hyperoesophagale 31

Nervus Antennalis 31

Ganglion Trito-Hyperoesophagale 33

Nervus Ganglii Pharyngealis 33

Nervus Labrualis 35

Nervus Corpoallatialis 36

Commissura Gangliorum Trito-Hyperoesophagalium 36

Nervulus musculi Tentorio-oriscutarius 36

Location and Topography of the Ganglion Hypoesophagale 36

Nervus Mandibularis 37

Nervus Maxillaris 38

Nervus Labialis 40

Nervus Tegumentualis 41

Nervus Postoccipitalis 42

Nervus Posterior 42

Acknowledgments 42

Literature Cited 42

Nabil N. Youssef Topography of the

Cephalic Musculature

and Nervous System

of the Honey Bee

Apis mellifera Linnaeus

Introduction

The concept of homology, which expresses the continuity of structure in phylogeny, can be approached

in many ways: comparisons of external elements,

examinations of embryonic and postembryonic structures, and by following the topography and innervation of muscles. The occurrence of one of the

following phenomena limits the validity of any single

approach: the loss of external structures in some

groups; the presence in others of secondary splits in

the embryo, suggesting ancestral structures or segmentation; the tendency of some muscles to shift

their points of attachment; or the innervation of a

single muscle from more than one ganglion. Consequently, a valid study of homology in insect morphology requires the use of as many lines of evidence

as possible.

Many morphologists and taxonomists have studied

primarily the external structures, especially those

tending to be the least consistent (genitalia, thoracic

sclerites, mouthparts). The result is a vast amount of

literature emphasizing diversity rather than homology,

although the latter has not been entirely neglected.

Embryological studies have lagged for various

reasons, including the following: (1) embryological

stages in insects are often of such short duration that

the succession of forms is hard to define, (2) larvae

are generally too advanced in development to be

Nabil N. Youssef, Department of Zoology, Utah State University, Logan, Utah 84321.

considered truly embryonic and can in no sense be

attributed to "early hatching" of the embryo, (3) the

small size of insect eggs limits flexibility in experimental methods, (4) adequate techniques for tissue

culture of insect embryos have yet to be developed.

Topographical studies of insect musculature have

been more numerous than those of the nervous system; however, attempts to examine the criteria of

muscle homology have been made only recently. Matsuda (1965) is probably the first and only one to

review this subject in detail.

The nervous systems of insects in general have

been extensively and intensively studied. The gross

anatomy of the "brain" and "ventral nerve cord"

and the diversity exhibited by these structures have

been described for many species. We have few detailed studies (Holste 1910, Denis 1928, Maki 1936,

and Chaudonneret 1950-1951), however, of topographical nerve patterns and the actual innervation

of muscles.

Although the honey bee, Apis mellifera, has had its

share of morphological studies relative to external

structure (Snodgrass 1910, 1925, 1956) and embryology (Nelson 1915), the study of muscle homology

between its different segments and between its musculature, as a whole, and those of other insects is

still in its infancy. The topography of the honey bee

nervous system is in the same situation. Although

there has been intensive histological work on the

so-called brain of the honey bee (Kenyon 1896,

Jonescu 1909, Jawlowski 1958, and Satija 1958), the

1
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

only publication dealing with the innervation of the

cephalic muscles seems to be a skimpy one by Rehm

(1939) describing the innervation of the musculus

cranio-intramandibularis.

A few workers have studied muscle-nerve patterns

in insects, but attempts to compare the patterns in

order to establish segmental homology or to identify

segmental features common to several orders have

been generally fragmentary. This is largely because

of difficulties in recognizing homologous nerve groups,

due in part to the current unsuitable nomenclatorial

systems for insect muscles and nerves, and in part

to the bundling of the proximal portion of many

nerves in different ways in different segments and in

different taxa.

The principal objective of the investigation reported here was to develop a complete account of the

topography of nerve tissues and musculature of the

honey bee head. A second objective was to determine,

with a reasonable degree of accuracy, the probability

of homology by comparing the topography of cephalic

nerves and muscle arrangements of the honey bee

with those of previously studied groups, especially

the ones related and supposedly ancestral to it.

The current multifarious nomenclatorial systems

for nerves and muscles create a difficult obstacle in

comparative morphology. A modified system, approaching most closely that of Hannemann (1956),

for naming the muscles and a new system of naming

nerves were developed for this study in the hope that

they would set a consistent pattern which could be

used without extensive modification in future work.

In the course of the study several other members

of the superfamily Apoidea, as well as the vespid

Vespula maculata (Linnaeus), were dissected for

comparison.

Materials and Methods

Adult workers, drones, and queens of the honey bee

were provided by the Federal Wild Bee Pollination

Investigations Laboratory at Logan, Utah. The bees

were immobilized with carbon dioxide and injected

with picroformalin until their abdomens expanded

slightly. The injected bees were stored in picroformalin for at least 48 hours before being dissected.

Eventually, it was discovered that if the injected

bees were simmered in the fixative for three minutes,

they could be dissected without further delay.

In the study of head muscles and nerve tissues, it

was found convenient to isolate the head from the

rest of the body and bisect it medially. Each half was

glued (with the cut side up) to the bottom of a plastic container (l

/% X 2 X 1 l/i inches), using Sticky Wax

supplied by Kerr Manufacturing Company.

With the aid of a dissecting stereomicroscope

(4O-120X), with the focusing mechanism adapted

to foot manipulation, the muscles and nerves were

revealed by dissecting downward, layer by layer,

from the median section. To obtain a true picture of

the relationships of different tissues, each muscle,

nerve, and nervule was observed from various aspects

and followed to its termination. For this purpose,

other types of specimen orientation were used, such as:

(1) embedding the head laterally and exposing one

half for dissection; (2) gluing the head on its occipital

aspect to present a frontal view of the nerve tissues

and the prepharyngeal and pharyngeal muscles;

(3) isolating the labium, antenna, and maxilla from

the head to study their muscles and nerves separately;

(4) embedding the head laterally to the level of the

antennae for a study of the head glands and their

innervation, and of the antennal muscles and their

innervation.

Dissections were performed under distilled water

after the specimens were washed several times with

70 percent alcohol. Bee's heads were dissected with

knives made of razor blade edges, with needles made

of ground-down "minuten nadeln" (Stajanovich

1945), and with ground-down jeweler's forceps. In

the course of study, about 2,000 workers, 200 queens,

and 500 drones were dissected.

A differential staining technique was developed for

tissues found in the head (nerves, muscles, glands,

etc.). After reaching a preliminary stage of dissection,

the specimens were washed with 70 percent alcohol

for one minute. The excess alcohol was drained and

a drop of acetocarmine and another of iron hydrate

(0.25 percent in 50 percent acetic acid) were applied

directly to the specimens. Staining time varied from

two to five minutes for different specimens, depending upon the duration of storage in the picroformalin.

When necessary, the same technique was repeated for

different stages of dissection.

For the preservation of dissected specimens, a mixture of one part U.S. P. glycerol and one part distilled

water was found to be superior to different dilutions
NUMBER 9 9 3

of ethanol. Dissected specimens preserved in this mix- of nerve and muscle tissues proved more suitable. The

ture since September 1963 are still in excellent con- staining schedule followed that already described

dition as this manuscript is written. (Youssef 1964).

Staining with acetocarmine and iron hydrate was Drawings for different stages of dissection were

unsatisfactory for the study of nerve endings or re- made with the aid of an ocular grid. The illustrations

ceptors other than the compound eyes. Palmgren's were designed to show the precise arrangement of

silver pyridine technique (1955) for whole mounts nerves, muscles, and other tissues.

PART I. MUSCULATURE

History

Although the order Hymenoptera is the second

largest in number of species, investigations dealing

with its body musculature, in general, and its head

musculature, in particular, tend to be scarce and incomplete. This review is mainly concerned with those

articles investigating the cephalic musculature of

Hymenoptera.

In the Symphyta the Tenthredinidae has been

given more attention than other families, probably

because of its primitive nature. Taylor (1931) worked

on the morphology of a few species but his work is

far from complete.

Matsuda (1957) studied the cephalic external and

internal morphology of Macrophya pluricincta Norton is an attempt to correlate it with that of higher

groups of Hymenoptera. He also attempted to test

several theories with regard to the external morphology of the facial region. In his descriptive section,

he classified the muscles into groups but gave each

muscle a separate number. In the illustrations, however, he devised names for some muscles by hyphenating the two names of the structures to which they are

attached. He derived the first part of the name from

the point of fixed attachment (point of origin), e.g.,

frons-epipharynx, vertex-stomodaeum, etc. Matsuda's

nomenclature, based on a different number for each

muscle, was occasionally inaccurate. For example, he

gave the numbers "22-23" to both flagellar muscles

(p. 105, pi. Ill : fig. E) and mandibular muscles (p.

103, pi. II: fig. B). Although he used consecutive

numbers for the most part, he skipped numbers "17"

and "18" for no apparent reason. According to Matsuda, muscle "26" comes from the ventral side of the

composite tentorial bar and inserts on the base of the

lacinia. On page 105, plate III: figure F, he identifies

this muscle as "Tentorium-Lacinia," whereas the

drawing itself shows that its movable point of attachment is on the stipes rather than the lacinia. If it is

assumed that this muscle shifted its movable point of

attachment to the stipes (although remaining in reality a "tentorio-lacinial muscle"), there is still a contradiction with Matsuda's later work (1965:268) in

which he states that "the tentorio-lacinial muscle has

been found in Machilis only." It seems strange that

muscle "35" (t-s) of Macrophya has no homolog

in the other groups of insects he studied. Matsuda's

general plan for labial muscles (1965), which he

based on the available literature of cephalic muscles

of insects, indicates that such a muscle does not exist

in insects.

In the Apocrita the cephalic muscles of four genera have been studied in detail: Stenobracon (Braconidae), Lasius (Formicidae), Vespula (Vespidae),

and Apis (Apidae).

Alam (1951) studied the cephalic muscles of

Stenobracon deesae Cameron. He followed the pattern of nomenclature used by Duncan (1939) and

Snodgrass (1942) and tried to homologize many

muscles with those of other Hymenoptera and with

those described for Gryllus by Duporte (1920). Apparently Alam did not believe that muscles are plastic

enough in phylogeny to shift their points of attachment or combine with other muscles. For details see

his discussion on page 15 (1951) in regard to the

"flexor of maxilla" (musculi tentorio-stipitales) and

the "second flexor of lacinia" (musculus stipiti-laciniaris).

Janet (1905) studied the cephalic musculature of

the ant Lasius niger Reine by means of longitudinal

sections. Although this technique is practical for

studying small organisms, it hinders the investigator

from determining exact locations or functions of

muscles. His study is nearly complete but his illustrations are difficult to follow. In some instances he

described muscles in detail but in others he merely

named them.

Duncan (1939) studied and illustrated the musculature of Vespula pensylvanica Saussure in an essentially complete fashion. However, I discovered two

pairs of muscles in the head of Vespula maculata

which Duncan must have missed because of their

smallness. Duncan adopted the nomenclatorial system

proposed by Berlese (1909), Bauer (1910), and

others which is based largely on function rather than

exact position.
Hymci

Apisn

Wolff.

Name

levjtor

lellifera

1875

— ^

Linn.

Abr.

Hymer

Apis n

Moriso

Name

levjjor

levjto.

lellifera Linn.

n. 1927

labri

vel, plant.

Abr.

Hvi

Api

Snc

Nar

add

1 rr

idgr

ne

ucti

optera

lellifera Lin

ass. 1942

or of labrui

n.

n

Abr.

1

Hyme,

Apis n

Presen

Name

fronti-!

clypeo

loptera

ncUifcra Linn.

t Study

ibralU

epipharyngeahs

Abr.

m. fron-labr.

General

Matsuda. 196S

Name

posterior fronto-labral

anterior fronto-labral

labro-epipharyngeal

anterior clypeo-epipharyngeal

Abr.

61

62

63

abductor irluuli secundi

teniorio-scapualis I m. tent leap

4 tentorio-scapualis TTl nK tent-scap. H|

5 tentorio-tcapualis IV n± tenl-scap. IV

levator of antennal 6 scapo-pedicularis I m. scap-pioicrT

flagellum

depressor of antennal 7 scapo-pedicularis II m. scap-pedic. II

flaaellurn

abductor of the mandible 8 cranio-ex trarnandibularis m. cran-extrarnarid lergo-nisndibulsr

adductor of the mandible 9atb cranio-intramandibularis m. cran-intramand. tergo-mandibular

a, b " —— -

tentorio-mandibularis m. tent-mand. tentorio-mandibula

promotor of the maxilla 10 geno-cardinalis m. geno-cafd. tergo-cardinal

or cardinal protractor

of proboscis

adductor of the maxilla 11 tentorio-cardinalis rn. lenl-tard. tentorio-cardinal

adductor of maxilla 12 lentorio-stipitalis I m. tent-»tip. I

tentorio-stipilal

adductor of maxilla 13 tenlorio-stipilalis II m. tent-slip. II

terfo-lacinial

flexor of lacinia 16 stipili-laciniaris m. slip-lac. stlpito-lacinial

flexor of galea IS stipili-galearis m stip-'taT t tlplto-galeal

stipiti-maxillopalpualis U m. stip-maxpalp. U antagonistic muscle

muscle of maxillary 14 stipiti-maxillopalpualis I m. «ip-m»xpalp. I palpus from stipes

protractor cardinis vel

maxillae inferior extern us

protractor cardinis vel

innlllae inferior inlcrnus

flexor labi exte

menti

retractor linguae brevis

retractor linguae bicepia

ligula

flexor of the glo

muscle of 2nd seg. of

labial palpus

flexor of labial palpus

premento-paragloss

prenxnto-glosiarls

; postiKcip-prement. postoccipito-prerner

m. prement-paragloss. premento-ligulai

premento-gloual

submento-premental

lahiopalp 111

tentorio-paraglossal

protractor linguae

retractor linguae bicepis

etractor pharyngis infei

dll

ret

P"

pos

racti

>trai

am

teri

i>r p

TT!F

pulla

or

harv

"pharyri

alrt

IS

.ps

retractor of oral plate

protractor of oral pla dypeo-hy pophar> ngeal

pharynx

irio^uspensorialif

03 dilator pha dilators of thesuctoriun

(5- 7 muscles)

ngiludinal muscle of the

pharynx

precerebral dilator of

pharynx

clrculopharyng»ali«

. frun phar. I

. fron-phar. II

. fron-phar. Ill

pt>sterior dorsal dilator of

pharynx

ring muscle
TABLE 1.—Cephalic musculature of some representatives of hymenopteroid and neuropteroid insects

Order

Author

Muscle

Labral

Epipharyngeal

Nei

Kd

N a i

t r n

rrti

e n ,

fin

iropte

sey. 1

T i e

m , | m

factor

npress

ra

954

usele of the labrum

of the labrum

or of the labrum

t dorsal dilator of cibarium

Abr.

3

2

1

35

Hvn

Mai

Nan

Iron

fron

lahr

lenoptera

suda. 1957

l e

um-epipharynx

Abr.

1

2

3&4

HynwnoDWn

Alam. 1951

Name

abductor of the labrum

retractor of the epipliarynx

Abr.

1

•

2

Hynwimpi*n

Duncan. 1939

Name

clypeo-dilator of the nloulh

Ahr.

cdmth

Antennal first promotor of the antenna 4 19 external depn

second promotor of the antenna 4a tentorium-antenna 20 internal depressor

first retractor of the antenna 6 21 external levator

second retractor of the antenna 6a internal levator

levator of flagellum 7 2 2 levator of flagellum

muscles of the flagellum

depressor or flagellum 8 23 daprassor of flagallum

adductor of the mandibla 10 adductor of the mandible 23 adductor of the m.ndibl.

nternal antennal tevator

Maxillary abductor of the csrdo first protractor of the ~22 prnduclor of the cardo

proximal adductor of car*

distal adductor of cardo

compressor of the cardo

adductor of stipes

abductor of stipes

cranial flexor o

lacinia

stipttal flexor a

flexor of gales

levator of maxillary palpus

depressor of maxillary palpus

muscle of 1st segment of

maxillary palpus

muscle of 2nd segment of

maxillary palpus

muscle of 3rd segment of

maxillary palpus

muscle of 4th segment of

maxillary palpus

stipes-lacinia

stipes-galea

stipes-palpus

slipes palpus

II

\»

n

n

:cond flam

exoroflac

exorofgal

IXIIIM

>r of lacinia

Inia

at

sors of palpus

of palpal segment

of palpal segment

of palpal segment

23 extensor of the maxilla

~34~ flexor of stipes

2 5 flexor of lacinia

27 flexor of galea

28 anterior depressor oi

maxillary palpus

29 posterior depressor (

maxillary palpus

If

ads*

pdm:

levator of paraglossa

depressor of prementi

36 posterior adducto

anterior adductor

14 flexor of paraglossa

13 posterior labial adduct>

levator of the palpus

abductor of labial palpu

muscles of labrial palpu:

prementum-paragloa

prementumglossa

prementum-palpus

muscles of labial

palpus

39

4I&43

38

04

42

44.45

46

48

48

9

12

13

14

ligular flexor

lingual flexor

flexor of the palpus

flexor of the palpus

flexor of the palpus

salivarlum

posterior dilator of

salivarium

frontal dilator of

pharyngeal diverticula

tentorial dilator of

pharyngeal diverticula

second ventral dilator of

anterior pharynx

Tint ventral dilator of

anterior pharynx

17 anterior flexor of lingula

16 posterior flexor of lingula

18 depressor of labial palpu

-lypopharynfeal dorsal muscle of salivary pump

ventral muscle of salivary pump

retractor of the mouth angle

first lateral dilator of

pharynx

second lateral dilator of

pharynx

ventral dilator of cibarium

ventral dilator of anterior

pharynx

tint ventral dilator of

posterior pharynx

second ventral dilator of

posterior pharynx

third ventral dilator of

posterior pharynx

ventral constrictor of cibarium

frons-stomodaeum

tentoriuni'Stomodaeum

T3 dilator of salivaris

I*

t e

ntoriu

ntoriu

m-sto

m.s,o

modaeum

modaeum

37

36

posterior d

ventral dila

postern

• pharyn)

lor of

• r pharyn

luscle

t

X

36 clypeus-stomodaeu

clypeal dilator of

phary

uscle)

atrictor of cibariun

pharyngeal and

Pharyngeal dilator of

atitn

pdmth_

first dorsal dilator of

posterior pharynx

second dorsal dilator <

posterior pharynx

dorsal dilators of anterio

pharynx

constrictors of the pharyn

39-40-41 vertex-stomodaeun

52 53

Tint frontal dilator o

anterior pharynx

second frontal dilato

anterior pharynx

third frontal dilator <

anterior pharynx

occiptal dilator of

posterior pharyn)

32 frontal dilator of

anterior pharyn

38 dorsal dilator of

posterior pharynx

intrinsic muscle of the
8 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Wolff (1875) was among the first to describe and

illustrate cephalic muscles of the honey bee. These

muscles were mainly those associated with what he

called "the sucking organs." He also studied the

pharynx and its muscles in great detail. His illustration of the muscles extending between the clypeus

and the upper cibarial wall is very clear and generally more accurate than those made by later

investigators.

Braints (1884) illustrated a few of the mouthpart

muscles. Although he ascribed function to each muscle, he used only Arabic numbers for naming them.

Morison (1927) reviewed the fragmentary preceding work on the honey bee musculature. Following

this he studied the musculature intensively and missed

only several very small muscles. Although the points

of attachment indicated by him are not always accurate, his study formed the basis for subsequent

investigations on honey bee musculature, including

those of Snodgrass (1942-1956).

Snodgrass (1942), in his study of the skeleto-musculature mechanisms of the honey bee, was the first

to correlate carefully the findings on musculature with

those on the endo- and exoskeletal structures. In the

course of reviewing the musculature, he corrected a

few errors committed by Morison and others. However, his study of the muscles attached to the upper

wall of the cibarium is inaccurate. He stated that

there were five pairs of cibarial muscles, but his

drawing (p. 31, fig. 10c) showed only five unpaired

ones. These muscles are attached to the cibarial wall

in the manner described by Wolff (1875, pi. II: fig.

9) rather than Snodgrass (1942, 1956).

Since only the fragmentary investigations made by

Snodgrass (1942), Alam (1951), and Matsuda (1957,

1965) have been reported, we have no complete

study of muscle homology between the head of the

honey bee and that of other insects.

Methods of Nomenclature

Although insect musculature has been investigated

intensively, its nomenclature is still a challenge to

the morphologist.

Table 1 compares nomenclatorial systems as they

have been used by various authors for the cephalic

muscles of a neuropteran and several species of Hymenoptera. It also indicates the different systems of

nomenclature applied by different authors (Wolff,

Morison, and Snodgrass) for the cephalic muscles

of the honey bee.

METHODS USED IN PREVIOUS STUDIES

Methods used in the past for naming insect muscles

(Table 1) are as follows: (1) by arbitrary reference

number; (2) according to function; (3) according

to location on the main axis; and (4) according to

the points of fixed and movable attachment. The

first system is noncontroversial, but the names themselves are morphologically meaningless and hard to

remember. The second system is misleading in relation to muscle homology. The traditional method of

determining the function of each muscle is to use

micromanipulation. The function of smaller muscles

can only be determined by deduction, and this is

often actually an "educated guess." Table 1 shows

that different functional names have been given by

different workers for the same muscles of Apis mellifera. Furthermore, it is difficult and often impossible

to identify corresponding muscles on a functional

basis. For example, a muscle may be a retractor in

one species but its homolog in another may be an

abductor because of a slight change in the point of

fixed or movable attachment, or both. The musculus

gena-cardinalis of the honey bee was designated by

Snodgrass (1942) as "promoter of the maxilla" or

"cardinal protractor of the proboscis"; whereas it is

a "productor" in Vespula, according to Duncan

(1939); and an abductor in the megalopteran,

Corydalus, according to Kelsey (1954).

The third system is simple and precise, but unfortunately it is hard to apply to complicated structures

such as the head, thorax, and genitalia. Nuesch

(1953) adopted the "purely" morphological system

utilized by Weber (1928, 1933) because, as he stated

(p. 591), ". . . it seems to me to be more suitable

than those which also consider the function, as in

the case of the nomenclature of Snodgrass ('35) and

Maki ('36)." Accordingly, Nuesch arranged the muscles (e.g., dela deib de2 and de3) of a location into

a group named according to its placement (i.e.,

"dorsolongitudinal muscles").

The final system, that depending on the points of

movable and fixed attachment, is flexible and makes

it possible to locate quickly any muscle in a dissected

specimen. It can be criticized, however, on the basis

of arguments concerning the homologies of sclerites
NUMBER 99

in different orders and also because of the tendency

of some muscles to shift their points of fixed or movable attachment, or both. Actually, muscles may be

of more help in establishing the homology of sclerites

than vice versa. There are two schools of thought

regarding the value and reliability of muscles for

establishing the homology of the skeletal parts to

which they are attached, and contradicting claims

have been made (Snodgrass 1935, 1942; Ferris 1942,

1944). If the muscles in question are serially repeated

and their points of fixed and movable attachment are

constant, however, their points of fixed attachment

may be used with considerable assurance. Unless it

is realized that musculature is a plastic system and

that each muscle can shift its point of fixed attachment, as well as its movable one within certain limits,

it becomes very difficult for the morphologist to establish any homology between different muscles in

different segments of the same insect and between

muscles in different groups of insects.

Many morphologists have attempted to name the

muscles according to their points of fixed and movable

attachment. Chaudonneret (1950-1951), in his study

of the cephalic morphology of Thermobia domestica

Packard, tried a combination system. He named each

muscle according to its function; however, he grouped

the muscles and named each group according to the

points of fixed and movable attachment of its

members.

Hannemann (1956), in his study of the cephalic

musculature of Micropteryx calthella (Linnaeus),

utilized the points of fixed and movable attachment

in naming the muscles. The name of a given muscle

was composed of the latinized name of the fixed

attachment point, hyphenated to that of the movable

attachment point, and followed in some instances by

a general descriptive term to show the location of the

muscle. This system has considerable merit, but the

descriptive terms are misleading since they do not

indicate the exact locations of the points of attachment. A muscle may have its point of fixed attachment in a lateral position and its point of movable

attachment in a ventral position, as in the case of

the musculus fronti-labrualis in the honey bee which

has a median point of fixed attachment and a lateral

point of movable attachment.

Matsuda (1956:8) avoided naming the muscles

according to their function on the basis "that the

primary concern of the comparative morphologist

should be the morphological origin of musculature

in relation to the external structure, regardless of its

function." Although Matsuda made this statement

at the time of his study, he failed to apply "morphological" names to every muscle. Instead, he placed

the muscles into groups and gave each group a

morphological name. Even so, he was inconsistent in

naming the muscle groups. In some cases he named

groups of muscles according to their placement

(ventral muscles, spiracular muscles, etc.), and at

other times according to the structures between which

the muscles stretch (muscles from the notum to the

lateral jugular membrane, muscles inserted on the

coxal margin and on the membrane near the coxal

margin, etc.).

Chad wick (1957), in his study of the intersegmental muscles of cockroaches, gave each morphologically distinct muscle a designation formed by

hyphenating the accepted abbreviations for the skeletal parts between which the muscle stretches. According to this system, if an attachment is segmental,

it is identified by an Arabic or Roman subscript for

the thorax or abdomen, respectively. He designated

the intersegmental structures by an Arabic numerical

prefix beginning with "0" for the cervical intersegment. However, he used the customary abbreviations

lev, 2cv, . . . and lax, 2ax, . . . for the cervical sclerites

and the axillary sclerites of the wing, respectively.

Cross-shaped muscles with "origin" and "insertion"

on opposite sides of the longitudinal body axis were

distinguished by adding "x" to the usual designation.

Although Chadwick's method of naming muscles is

in full agreement with that of naming them according to the points of fixed and movable attachment,

it defeats its purpose by depending on morphologically meaningless abbreviations. Also, the names are

difficult to follow or apply in studies dealing with

homology.

Daly (1963, 1964) adapted Chadwick's system for

naming the close-packed and fibrillar muscles of some

representatives of Hymenoptera and also for his study

on the morphogenesis of the honey bee thorax.

Matsuda (1965), in his comparative study of the

musculature of the insect head, utilized extensively

the points of fixed and movable attachment. Unfortunately, he did not name all the muscles of the!

head. Furthermore, he combined purely morphological and functional names for certain muscles ("the
10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

posterior dorsal dilators of the pharynx, the ventral

dilators of the pharynx, etc.").

METHOD USED IN PRESENT STUDY

In this investigation every muscle is named according

to its points of fixed and movable attachment. Such

a system seems reasonable, especially in the light of

Matsuda's study (1965), which demonstrated that (at

least in the head) homology between muscles of different insects can be established. Before naming each

muscle, the available literature was studied to compare the points of fixed and movable attachment of

the honey bee muscles with those of the homologous

muscles in other insects. Because of the tendency of

some muscles to shift either their points of fixed or

movable attachment, or both, generalized rather than

precise topographic terminology would have, in most

cases, resulted in even more cumbersome names than

those chosen. For international usage, it was decided

to use classical Greek and Latin forms for these

names. The name of the point of fixed attachment

is placed in front of that of the point of movable

attachment and hyphenated with it.

A few muscles are stretched between two movable

points of attachment. In such cases, points of fixed

or movable attachment are not differentiated. Instead,

the prefix "inter" is added to the composite word

formed by the names of the two points of movable

attachment. A muscle with no definite points of fixed

or movable attachment (ring type) is designated as

a circular muscle of the structure it ensheaths.

For the sake of brevity and clarity the segments

of segmental structures are designated by the suffix

"mere"1 and are given Roman numerals to indicate

their position in the series (for example, labiopalpomere II, maxillopalpomere III, etc.).

The principal value of the present nomenclatorial

system is that a person can locate a particular muscle

without having to read a long topographic description, interpret functions, or trace evolutionary

changes. To maintain this value, it would seem advisable to base such names solely on the attachment

points of the insect being studied.

The morphologist may be tempted to change the

name of a muscle when it is obviously homologous

1

 The current usage of the term "mere" is incorrect, but it

has become widespread and well established throughout the

scientific world. Therefore, I decided not to introduce the

very unfamiliar (though correct) form "mercikalis."

with one given a different name in another insect.

For example, Stajanovich (1945) found that in

Anoplura the "antennal muscles" "originate" on the

dorsal wall of the antennal segment instead of on

the tentorium as the same muscle does in most other

insects. Since the Anoplura lack a tentorium, the

"antennal muscles" had to shift their points of fixed

attachment. Obviously, to use a homologous term

incorporating the term tentorium would only confuse someone making a dissection of an anopluran.

Nevertheless, it is apparent that homology should

not be ignored. To many students homology is the

principal issue involved in morphological work.

Originally I had hoped to set up a parallel but

homologous nomenclatorial system. This was to be

done by dividing all of the cephalic muscles into

groups representing the main structural areas with

which they were associated and giving them an anterior to posterior sequential numbering system within

each group. This abbreviated name was to be used

in the illustrations and supplemented with the full

topographic name in the text. The advantage of

such a system, besides that of brevity in illustrations,

would be that the same abbreviations could presumably be used for all insects, since shifts in points

of attachment would not have to be taken into

account.

I finally decided that such a system, however

desirable, should await a detailed study of the sclerites, muscles, and nerves of many representative

insects and be based on a hypothetical "primitive"

insect with a "complete" muscular system. Following

this the same grouped numbering system could be

followed for any insect, with changes in the names

occurring only when a primitive muscle appeared

to have divided (in which case letter subscripts

could be added) or when fusion seemed to have

occurred (in which case two or more numbers could

be combined). Naturally, there would be many cases

of omitted numbers. Nevertheless, mandibular muscle

" 5" would always be "5" in whatever insect it occurred, even if it represented the only mandibular

muscle remaining in the insect in question.

Topography and Homology of Musculature

Although the musculature of the honey bee, Apis

mellifera, exhibits sexual dimorphism, all of the muscles in the head of the male (drone) can be homologized with those in the female (worker and queen).
NUMBER 99 11

An intensive study of both sexes indicates that the

male musculature has followed a pattern of degeneration in certain muscles and a retention of primitive

features in others.

Musculature of the head in general tends to be

more standardized than that of any other part of

the insect body, in spite of great specialization in

structure and function between different orders and

families. The cephalic muscles are readily classifiable

under the following groups: labral, clypeal, antennal,

mandibular, maxillary, labial, hypopharyngeal, cibarial, and pharyngeal muscles.

In this study, the muscles of the three castes of the

honey bee are compared with their homologs in the

various groups of Hymenoptera and Neuroptera that

have been studied. Table 2 gives names of major

contributors, years of publication, and the insects

that have been studied (in phylogenetic order). In

many instances, the comparisons include other kinds

of insects, especially when they deal with more generalized features. In these cases, the names of the

contributors are mentioned in the text.

This study is strictly morphological, no attempt

has been made to study the function of muscles except for those not previously described. Consequently,

most of the functions mentioned in the text have

been proposed by various authors. The points of

fixed and movable attachment of the cephalic musculature in the honey bee are summarized in Table 3.

LABRAL MUSCLES

The labrum in most higher insects has three pairs of

muscles, two extrinsic and one intrinsic. The extrinsic ones are median and lateral, and the intrinsic

ones are median.

The musculus fronti-labrualis (m. fron-labr.) (Figure 4)

The point of fixed attachment of this muscle is

located medially on the frons between the musculi

fronti-suspensoriali. It attaches laterally on a long

tendonlike apodemal growth from the base of the

labrum (tromal area) which serves as a point for

movable attachment. The m. fron-labr. is better developed in the queen than is its homolog in the

worker or drone. It is absent in Vespula pensylvanica

(Duncan 1939) and in Vespula maculata. In Lasius

niger Reine (Janet 1905) it is well developed and

has similar points of attachment to those of the

honey bee. Alam (1951) described an "abductor" of

the labrum in Stenobracon deesae, which he claimed

served the same function as the m. fron-labr. in the

honey bee but is probably a homolog of muscle "1 "

in Macrophya pluricincta, which Matsuda (1957)

reported to have its movable attachment located

submedially rather than laterally as in the honey

bee. According to Snodgrass, it functions as an abductor in the honey bee, although Maki considered

it to be a posterior retractor to the labrum in

Corydalus.

It seems that in the honey bee this muscle has

maintained its primitive points of attachment, whereas in Macrophya the movable attachment has shifted,

and in Vespa and Stenobracon it has disappeared.

TABLE 2.—Major contributors to the cephalic musculature of Hymenoptera and Neuroptera

Order

Neuroptera

Family

Corydalidae

Sialidae

Species

Corydalus cornutus Linn.

Chauliodes formosanus Peterson

Author

Kelsey

Maki

Year

1954

1936

Hymenoptera

Tenthredinidae Macrophya pluricincta Norton

Stenobracon deesae Cameron

Lasius niger Reine

Vespidae

Vespula pensylvanica Sauss.

Apidae

Apis melllfera Linn.

Apis me 11ifera Linn.

Snodgrass

Morison

1942

1927
12

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 3.—Points of fixed and movable attachment of the cephalic musculature in the honey bee

Name Abbreviation Point of fixed attachment Point of movable attachment

musculus fronti-Ubrualis

musculus clvpeo-epipharvngealis

musculus tentorio-scapualis 1

musculus tentorio-scapualis II

musculus tentorio-scapualis III

musculus ten torio-scapualis IV.

musculus scapo-pedicularis 1

musculus scapo-pedicularis II

musculus cranio-extramandibularis

musculus cranio-intramandibularis I

musculus cranio-intramandibularis II

musculus tentorio-mandibularis

musculus gena-cardinalis

musculus tentorio-cardinalisa

musculus tentorio-stipitalis I

musculus tentorio-stipitalis II

musculus stiplti-laciniaris

musculus stipiti-galearis

musculus stipiti-maxillopalpualis I

musculus stipiti-maxillopalpualis II

musculus postoccipiti-prementualis"

musculus tentorio-prementualis

musculus premento-paraglossaris

musculus premeqto-glossaris

musculus premento-labiopalpualis

musculus labiopalpomere I-H

musculus dorsopremento-salivarius

musculus basipremento-salivarius

musculus fronti-suspensorialis

musculus clypeo-juspensofialis

musculus tentorio-oriscutorius

musculus tentorio-suspensorialis

musculus oriscuto-suspenaorialis

musculi dypeo-ciberioparietales

musculus intersuspensorialis dorsualisc

musculus frontj-pharyngealis ]_

musciiltK fronti-pharyngealis II

musculus fronti-pharyngealis 111°

musculus cranio-pharyngealis

musculus crrcuk>pharyngealise

m. fron-labr.

m. clvp-epiph

m. tent-scap. 1

m. tent-scap. H

m. tent-scap. Ill

m. tent-scap. IV,

m. scap-pedic. I

m. scap-pedic. H

m. cran-extramand. I

m. cran-intramand. I

m. cran-intramand. 1^

m. tent-mand.

m. gena-card.

m. tent-card

m. tent-stip. j_

m. tent-stip. II

m. stip-lac.

m. stip-gal.

in. stip-maxpalp. I

m. stip-maxpalp. H

m. postoccip-prement.

m. tent-prement.

m. prement-paragloss.

m. prement-gloss.

jn. prement-labiopalp.

m. labiopalp. l-jl

m. dorsoprement-saliv.

rn. basipremento-saliv.

m. fron-susp.

m. clyp-susp.

m. tent-oriscut

nj. tent-susp.

m. oriscut-susp.

m. clyp-cibpariet.

m. intersusp. dors.

m. fron-phar. I

m. fron-phar. II_

m. fron-phar. III_

m. cran-phar.

m. circulophar.

medially on frons

on distal portion of clypeus

dorsally on pretentorium

on dorsal wall of antenna! scape

on ventral wall on antenna! scape

on gena

on post gena

on top of cranium

on the anterior end of

pretentorium

on inner wall of post gena

anteriorly on pretentorium

anterorly on pretentorium

anteriorly on pretentorium

on base of stipes

posteriorly on stipes

anterio -laterally on outer wall

of stipes

anterio-medially on outer wall

on occiput adjacent to the base

of tentorium

anteriorly on pretentorium

laterally on base of prementum

posteriorly on base of prementum

on lateral side of prementum

on base of first labiopalpomere

anteriorly on edge of prementum

on base of prementum

medially on frons

on inner lateral side of

pretentorium

medially on the tentorial bridge

laterally on the tentorial bridge

medially on the oral plate

on the cranial wall of clypeus

medially on the frons

on the frons, above fron-phar. 1^

on the frons, submedially to

fron-phar. H

submedially on the top of

cranium

on lateral base of labrum

on inner wall of epipharyngeal lobe

on base of antennal scape

on dorsal base of antennal pedicel

on ventral base of antennal pedicel

on outer articulating mandibular

membrane

on inner articulating mandibular

membrane

on inner articulating mandibular

membrane

on inner articulating mandibular

membrane

anteriorly on outer wall of canto

anteriorly on base of stipes

medially on base of stipes

medially on base of stipes

on base of licinia

on base of galea

on base of maxillary palpus

on base of maxillary palpus

on ligula on pretentorium

on base of prementum

on ligula of prementum

laterally on glossal rod

posteriorly on palpiger

on base of second labiopalpomere

medially on salivary syringe

laterally on salivary syringe

dorsally on hypropharyngeal suspensorial node

ventrally on hypopharyngeal suspensorial node

medially on the oral plate

ventro-laterally on hypopharyngeal

suspensorium

laterally on hypopharyngeal suspensorium

on inner wall of clypeus

anteriorly on anterior pharynx

posteriorly on anterior pharynx

laterally on anterior pharynx

dorsally on posterior pharynx

"in the drone the point of movable attachment is located on the end of the cardo.

In the worker the point of fixed attachment is located dorsally on the cranium.

cMuscIe with no definite point of attachment.

This muscle is found in the drone only.

eMuscle with no definite point of attachment.
NUMBER 99 13

EPIPHARYNGEAL MUSCLES

The term "epipharynx" is applied to the anterior

wall of the preoral cavity, the inner surface of the

labrum and clypeus. Consequently, this term is a

misnomer since it has no relationship with the

pharynx, which is a part of the stomadaeum. The

term "epipharynx" is used in this investigation for

lack of a substitute.2

Matsuda (1965) included the "epipharyngeal muscle" with the pharyngeal muscles. For the reasons

indicated above, however, I consider it more logical

to group them separately. An examination of the

epipharyngeal muscles in the lower and higher insects (including Thysanura and Diptera) revealed a

maximum of two muscles belonging to this group,

one anterior and the other posterior. The honey bee

has only one epipharyngeal muscle.

The musculus clypeo-epipharyngealis (m. dyp-epiph.)

(Figures 1, 3)

This is an unpaired muscle, probably of a fusiform

type. Its point of fixed attachment is located distally

on the clypeus close to the margin of the clypeolabral suture. Its point of movable attachment is on

the median inner wall of the epipharynx. It is about

the same size in the different castes.

Although Duncan (1939) considered m. clyp-epiph

to be absent in Vespula pensylvanica, it is probably

the "clypeo-dilator of the mouth" he described as

"originating" on the clypeus and "inserting" on the

anterior pharyngeal wall immediately above the

mouth. Examination of this muscle in Vespula

maculata revealed that its point of movable attachment is on the upper epipharyngeal wall rather than

the pharyngeal wall.

Duncan made his position ambiguous by stating

that the "clypeo-dilator" may be the homolog of

the "dilator cibarii" of generalized insects (described

by Snodgrass 1935), thus indicating that it is attached

to the cibarial wall (epipharyngeal wall) which belongs to the preoral cavity rather than the true

pharynx. Janet (1905) did not describe any epipharyngeal muscle in Lasius. According to his illustration

(p. 3, fig. a) and innervation plan, however, it would

seem that the musculus clypeo-epipharyngealis is ho-

' Perhaps the term "extra-internolabrum" or upper internal lip could be used as a substitute.

mologous to the pair of muscles he called "retractors

of the buccal tube." In Stenobracon, this muscle is

paired (Alam 1951). Matsuda (1957) considered

muscles "3 " and "4" in Macrophya to be homologs

of this muscle, although their points of fixed attachment are on the upper surface of the labrum.

The musculus clypeo-epipharyngealis is probably

the homolog of a "cibarial" muscle in Corydalus (the

first dorsal dilator of the cibarium). According to

Kelsey's description, it extends between the clypeus

and the lateral portion of the epipharyngeal plate

(as in Stenobracon). The same situation was reported for Chauliodes. Reports in the literature indicate that this muscle has the same points of attachment in lower and higher insects, except for Macrophya (described by Matsuda 1957).

Snodgrass and Alam considered m. clyp-epiph. to

be the retractor (levator) of the epipharynx. Yet

Duncan, Janet, Kelsey, and Maki stated that it is a

dilator (protractor) of the cibarium.

ANTENNAL MUSCLES

This group is treated rather superficially because topographic work on antennal muscles, especially the

intrinsic ones, has been fragmentary.

Imms (1939) classified antennae into two major

groups: the "segmental" type in which each segment

has intrinsic muscles moving the next segment, and

the "annulated" type in which the muscles are located

mainly in the basal segment (scape). Insects, except

Diplura and Collembola, have antennae belonging to

the latter type. The number of the extrinsic antennal

muscles varies greatly among primitive insects. Studies

of the lepidopteran Micropteryx calthella Hannemann (1956) and the thysanuran Machilis species

(Bitsch 1963) suggest that primitive insects had four

intrinsic muscles of the scape. However, according

to Matsuda (1965), the typical number of intrinsic

muscles is two.

The musculus tentorio-scapualis I (m. tent-scap. I)

(Figure 4)

This muscle has its point of fixed attachment on the

inner margin of the concave surface of the pretentorium (anterior tentorial arm) lateral to that of

the m. tentorio-scapualis II. The point of movable

attachment is located medially and dorsally on a
14 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

tendonlike apodemal growth of the base of the antennal scape.

The musculus tentorio-scapualis II (m. tent-scap. II)

(Figure 4)

The point of fixed attachment of this muscle is on

the outer posterior margin of the concave surface of

the pretentorium. Its point of movable attachment

is located laterally and dorsally on the apodemal

growth of the base of the scape.

The musculus tentorio-scapualis III (m. tent-scap.

Ill) (Figure 4)

This muscle has its point of fixed attachment on the

inner margin of the concave surface of the pretentorium under that of m. tent-scap. I. Its point of

movable attachment is located ventrally and laterally

on the apodemal growth of the base of the scape in

the opposite position to that of m. tent-scap. II.

The musculus tentorio-scapualis IV (m. tent-scap. IV)

(Figure 4)

The fixed point of attachment of this muscle is on

the outer margin of the concave surface of the pretentorium under that of m. tent-scap. II. Its point

of movable attachment is located ventrally and medially on the apodemal growth of the base of the

scape in the opposite position to that of m. tent-scap. I.

According to Duncan four extrinsic antennal muscles in Vespula are arranged in the same manner as

in the honey bee. Alam found the same situation in

Stenobracon. Matsuda found only three extrinsic

antennal muscles in Macrophya, all of which have

their fixed attachment on the "dorsal arm and upper

portion of the composite tentorial bar." However, I

found four extrinsic muscles in the antenna of the

tenthredinid, Tenthredo maxima Norton. According

to Maki, only three extrinsic muscles are in the antenna of Chauliodes. His first "levator of the antenna" and "second levator of the antenna" are

probably the homologs of m. tent-scap. I and m. tentscap. II. Unfortunately, Maki did not describe the

exact location of the attachments of what he named

"depressor of the antenna."

By comparing the points of movable attachments

of the extrinsic antennal muscles of the honey bee

with those of the hypothetically primitive antenna

as proposed by Matsuda (1965), it appears reasonable

to assume that the honey bee has retained primitive

features with regard to the points of movable attachment. On the other hand, it is evident that m. tentscap. I and m. tent-scap. II have shifted their points

of fixed attachment from the metatentorium (primitive feature) to the pretentorium owing to a degeneration of the metatentorium. According to the literature, m. tent-scap. I and m. tent-scap. II (dorsally

located) act as levators; m. tent-scap. Ill and m.

tent-scap. IV (ventrally located) are supposed to act

as depressors.

The musculus scapo-pedicularis I (m. scap-pedic. I)

(Figure 10)

This muscle's point of fixed attachment is located

dorsally on the inner wall of the scape near its base.

Its point of movable attachment is located on a

short, dorsal apodemal growth at the base of pedicel.

It is presumed to act as a levator of the flagellum.

The musculus scapo-pedicularis II (m. scap-pedic. II)

(Figure 10)

This muscle has its point of fixed attachment on the

inner ventral wall of the scape. Its point of movable

attachment is located on a short, ventral apodemal

growth at the base of the pedicel. It apparently

functions as a depressor of the flagellum.

MANDIBULAR MUSCLES

Mandibular muscles of insects are classified into two

groups: the dorsal (attached to the cranium and the

mandible) and the ventral (attached to the tentorium

and the mandible). According to Matsuda (1965),

one muscle of the ventral group is generally adductor

in function and the other is abductor. In higher

Pterygota the dorsal group is always retained but the

ventral group is often degenerated or lost.

The musculus cranio-extramandibularis (m. cran-extramand.) (Figure 2)

This muscle has its point of fixed attachment on the

genal and postgenal areas of the cranium behind the

compound eye in the worker and queen. In the drone

the point of fixed attachment is limited to the lower
NUMBER 9 9 15

part of the gena. In all three castes, the point of

movable attachment is located on a strong apodemal

growth (small in the case of the drone) of the articulating membrane at /the outer side of the base of

the mandible between the latter's base and the malar

area. The muscle is very small in the drone but well

developed in both worker and queen.

The m. cran-extramand. is the homolog of what

has been called the "abductor muscle of the mandible" in various groups of insects such as Vespula,

Lasius, Stenobracon, Chauliodes, Corydalus, and

others.

The musculus cranio-intramandibularis (m. cran-intramand.) (Figure 2)

In the worker and queen this muscle has two

branches, I and II. Branch I has several groups of

muscle fibers, some of which have their point of

fixed attachment on the occipital area and the

others on the postgena below the foramen. Branch II

has its point of fixed attachment on the vertex behind the Lobus Opticus and next to the point of

fixed attachment of the musculus postoccipiti-prementualis. The articulating mandibular membrane

at the inner margin of the mandible (next to the

mesal wall of the mandibular gland) gives rise to a

very stout apodeme splitting into two apodemal

growths. One is short and stout and bears the point

of movable attachment of m. cran-intramand. I. The

other is long (about four times as long) and thin on

which branch / / has its point of movable attachment.

In the drone m. cran-intramand. is very small in

comparison to its homolog in the worker and queen.

It has its point of fixed attachment only on the postgena and its point of movable attachment on a short

growth arising from the same location as described

for the worker and queen. Evidently branch II of

this muscle has degenerated completely in the drone,

although the apodemal growth still exists as a loose

thread.

M. cran-intramand. is the homolog of what has

been named the "abductor muscle of the mandible"

in other insects.

The musculus tentorio-mandibularis (m. tent-mand.)

(Figure 2)

This muscle has not been described before in the

honey bee or any other aculeate hymenopteran. In

the honey bee it is a very small muscle consisting of

one or two fibers, which I originally thought to be

a nerve fiber because of its close association with the

mandibular nerve. Examination under the compound

microscope, however, revealed it to be composed of

muscle tissue. It has its point of fixed attachment

on the extreme anterior end of the outer wall of the

pretentorium and extends cephalad with its movable

attachment on the inner articulating membrane

close to the apodemal growth associated with m.

cran-intramand. It probably represents the remains

of the ventral mandibular muscles. According to

Duncan, no such muscle exists in Vespula pensylvanica, but I found it even more developed in V. maculata than in the honey bee. In V. maculata it is

composed of four to six muscle fibers and has its

fixed attachment on the pretentorium, as does its

homolog in the honey bee. On the other hand, its

movable attachment is located on the inner wall of

the mandible, near its base. Janet did not find it in

Lasius, Alam in Stenobracon, nor did Matsuda find

it in Macrophya. Careful examination of other Hymenoptera may be necessary to clarify its status. It is

probably the homolog of the muscle described as the

"tentorial adductor of the mandible" by Maki in

Chauliodes. At any rate the points of attachment of

the latter are similar to those of the honey bee.

By comparing m. tent-mand. of the honey bee with

that of primitive insects, its point of movable attachment seems to have shifted from the inner wall

of the mandible to the inner articulating membrane.

Its function is supposed to be adduction of the mandible when it is well developed, as in Chauliodes. In

Apis (and probably in Vespula), however, where the

m. tent-mand. is reduced to only one strand of muscle

fibers, it appears to be modified to function similar

to a stretch organ, especially since it is innervated in

much the same way as known stretch organs (Finlayson and Lowenstein 1958). These organs have been

described only from the abdomen of many insects.

Physiological and histological studies will be required

to verify its function.

MAXILLARY MUSCLES

Generally speaking, the maxilla and its associated

muscles have retained primitive features in most insect groups. The major change in many orders has

been limited to reduction of the palpus. Accordingly,
16 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

many of the maxillary palpal muscles have degenerated or disappeared.

The musculus gena-cardinalis (m. gena-card.) (Figures 4, 5)

This muscle has its point of fixed attachment on the

postgenal inflection adjacent to the proboscidial fossa.

Its point of movable attachment is located on the

small arm of the cardo beyond the articulating condyle. The m. gena-card. is equally developed in the

three castes but tends to have a wider point of fixed

attachment (fan shaped) in the drone. According

to Duncan, the homolog muscle in Vespula has similar points of attachment. Alam found that in Stenobracon the point of movable attachment is on the

outer margin of the cardo close to its articulation

with the "hypostomal rod." Matsuda (1957) did not

find this muscle in Macrophya, but in 1965 he stated

that "it may be present." Maki in Chauliodes and

Kelsey in Corydalus found that m. gena-card. has

a broad movable attachment extending along the

mesal and lateral side of the "abductor" apodeme

which, in turn, projects from the apex of the cardinal

process. In the primitive insects studied, it has its

points of fixed and movable attachment, respectively,

on the side of the occipital foramen and the internal process of the cardo.

The function of this muscle varies among insects

due to differences in the shape of the head (hypognathal or prognathal) and according to the location

of the points of attachment. In Corydalus it is supposed to be an adductor of the cardo, and the same

function was claimed for it by Janet in Lasius. Maki

referred to it as a promoter of the cardo in Chauliodes; Alam called it a protractor of the maxilla in

Stenobracon; Duncan termed it the productor of

the cardo in Vespula; and Snodgrass claimed that in

the honey bee it acts as a protractor of the maxilla,

probably because of a shift of the point of fixed

attachment from the sides of the occipital foramen to

the postgenal inflection.

The musculus tentorio-cardinalis (m. tent-card.)

(Figures 4, 5)

In the honey bee, this muscle has its point of fixed

attachment on the anterior ventral margin of the

pretentorium. According to Morison (1927) and

Snodgrass (1942), the point of movable attachment

is located on the proximal end of the stipes. Careful

examination of the worker and queen, however, revealed that its movable point of attachment is on

both the proximal end of the stipes and the distal

end of the cardo. In the drone it is only on the distal

end of the cardo, close to its articulation with the

stipes. Duncan stated that the homolog of m. tentcard, in V. pensylvanica "originates" on the clypeus

and "inserts" by a long tendon on the toothlike process of the cardo. I found that in V. maculata, however, its point of fixed attachment is on the

pretentorium.

In Lasius, Janet found one muscle of the pair,

which he named "adductrice maxillaire," to have its

point of movable attachment on the area of articulation between the cardo and stipes. Also, Alam found

that in Stenobracon this muscle attaches to the "hinge

line." Matsuda found muscle "24" in Macrophya to

have its point of movable attachment on almost the

entire cardo. In Chauliodes and Corydalus, homologs

of m. tent-card, have their points of movable attachment on the distal portion of the cardo. Accordingly,

it seems that this muscle usually has its point of

movable attachment on the cardo, but in Lasius,

Stenobracon, and the female honey bee it has shifted

to the articulation between the cardo and stipes and

in Vespula to the apex of the stipes. In the drone

honey bee this muscle has retained the primitive

feature of having its point of movable attachment

on the cardo. It is presumed to be the adductor of

the cardo in Corydalus and Chauliodes, the protractor of the maxilla in Stenobracon, and the extensor

of the maxilla in Vespula. Nevertheless, Snodgrass

considers it to be one of the stipital protractors of

the proboscis in the honey bee.

The musculus tentorio-stipitalis I (m. tent-stip. I)

(Figure 3)

This muscle has its point of fixed attachment on the

anterior ventral margin of the pretentorium under

that of m. tent-card. Its point of movable attachment

is located medially on the inner wall of the base

of the stipes.

The musculus tentorio-stipitalis II (m. tent-stip. II)

(Figures 3, 4)

The point of fixed attachment of this muscle is located laterally on the inner side of the pretentorium

above the combined points of fixed attachment of
NUMBER 99 17

m. tent-card, and m. tent-stip. I. Its point of movable attachment is on the inner wall of the base of

the stipes, just above that of m. tent-stip. I.

Since these two muscles have similar points of

attachment, they probably serve similar functions.

Accordingly, they may be named collectively as

musculi tentorio-stipitales.

In other groups of studied Hymenoptera {Vespula,

Lasius, Stenobracon, and Macrophya), the mi. tentstipitales are represented by a single muscle. The same

situation exists in the most primitive Lepidoptera,

such as Micropteryx calthella (L.) (Hannemann

1956). However, in Corydalus there are two muscles.

According to Matsuda (1965), primitive insects usually have more than one muscle belonging to this

group.

Dissection of V. maculata indicated that the homolog of this group of muscles has its point of fixed

attachment on the pretentorium and clypeus rather

than only the clypeus as stated by Duncan for V.

pensylvanica. According to Matsuda, the group does

not exist in Macrophya. He also indicated (1957)

that muscle "26" is a "Tentorium-Lacinia" muscle.

However, by examining his illustration (pi. Ill : fig.

F) and by considering the fact that the "tentoriolacinial" muscle "has been found in Machilis only"

(Matsuda 1965:268), it appears that muscle "26" of

Macrophya is the homolog of musculi tentoriostipitales.

This group of muscles is supposed to function as

an adductor of the stipes in Corydalus, Chauliodes,

and Lasius and as a flexor of the maxilla in Stenobracon and Vespula. Yet Snodgrass (1942) considered it, together with m. tent-card., as serving to protract the proboscis.

The musculus stipiti-laciniaris (m. stip-lac.) (Figure

5)

This muscle has its point of fixed attachment on the

outer wall of the base of the stipes. The point of

movable attachment is located on a small sclerite

("lever of lacinia," Snodgrass 1942) at the base of

the lacinia. It functions as a flexor in the honey bee

and in a majority of other insects. Although it has

similar points of attachment in all groups of insects

studied, it has also been reported to function as a

protractor of the lacinial stylet in Psocoptera, Thysanoptera, Mallophaga, and Siphonaptera and a

retractor for the maxillary stylet in Hemiptera.

The musculus stipiti-galearis (m. stip-gal.) (Figure 5)

This muscle has a broad point of fixed attachment on

the anterior and lateral inner wall of the stipes. Its

point of movable attachment is located on the long

tendonlike apodemal growth of the base of the galea

at the middle of a "leverlike" ridge. In some insects

the galea has no apodemal growth, so the muscle attaches directly to the galea. In many primitive insects

(Thermobia, Machilis, Campodea, Periplaneta, etc.)

and in primitive members of higher orders (Micropteryx, Macrophya, etc.) this muscle has its point of

fixed attachment on the stipes. In many higher groups

of insects, however, it has shifted its point of fixed

attachment to other areas. In higher Lepidoptera, for

instance, its point of fixed attachment is on the

tentorium, yet in the larvae of Trichoptera, Lepidoptera, Mecoptera, and Diptera it is on the cranium.

When m. stip-gal. has its point of fixed attachment

on the stipes, it functions as a flexor of the galea,

as in Thermobia and Machilis. In the honey bee it

folds the galea because of its attachment to the

"leverlike" ridge. According to Snodgrass (1942) its

tension, when contracted, first depresses the galea

and then turns it backward and outward. Continuous contraction finally turns the galea straight back

and folds it against the stipes.

The musculus stipiti-maxillopalpualis I (m. stip-maxpalp. I) (Figure 5)

The point of fixed attachment of this muscle is located anteriorly and laterally on the outer wall of

the stipes. The point of movable attachment is on

the ventral mesal base of the maxillary palpus. These

findings with regard to the point of movable attachment agree with those of Snodgrass (1942) and disagree with those of Wolff (1875) and Morison

(1927) who regarded it as a galeal muscle, based

on the argument that it attaches "near" the base of

the palpus. Examination under the compound microscope indicated that it attaches directly to the base

of the palpus.

The musculus stipiti-maxillopalpualis II (m. stipmaxpalp. II) (Figure 5)

This muscle has not previously been described in

the honey bee. It is a very small muscle, a single
18 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

fiber, embedded between the fibers of m. stip-maxpalp. I. It was observed for the first time by following

a parallel "nerve" that eventually diverges to innervate the stipital integument. Tracing this muscle

fiber to its termination indicated that it (m. stipmaxpalp. II) attaches separately but close to m.

stip-maxpalp. I, where its points of fixed and movable

attachment are on the base of the stipes (dorsally

and medially over m. stip-maxpalp. I) and the base

of the maxillary palpus, respectively. The pattern of

its innervation, the way it extends, and its being a

single fiber suggest that it may act in a fashion similar

to that of a "stretch organ." These two, m. stipmaxpalp. I and m. stip-maxpalp. II, can be grouped

as musculi stipiti-maxillopalpuales.

Two muscles belonging to the above group are

found in Vespula, Macrophya, Chauliodes, and Corydalus. In the first two genera, these muscles have

their points of movable attachment on the ventral

side of the maxillary palpus, but in the last two, the

point of movable attachment of one muscle is dorsal

and the other is ventral, as in primitive insects. Consequently, in the cases of Macrophya, Vespula, and

Apis, m. stip-maxpalp. II is believed to have shifted

its point of movable attachment from a dorsal to a

ventral location on the base of the maxillary palpus.

These muscles act as depressors of the maxillary

palpus when their points of fixed attachment are on

the ventral side of the base of the maxillary palpus,

as in Macrophya.

LABIAL MUSCLES

Probably the labium is the most specialized gnathal

segment. Hence, labial muscles have tended to change

the location of their points of attachment more than

the other gnathal segments. This tendency can be

seen even between members of primitive orders; for

example, the labial muscles of Machilidae are apparently more specialized than those of Lepismatidae

(both belong to Thysanura). Many labial muscles

found in primitive orders or in primitive groups of

higher orders have not been found in the honey

bee (Table 1). Some labial muscles have been treated

as hypopharyngeal muscles because they are closely

associated with the hypopharynx, which is a union

of several sclerites of more than one gnathal segment.

The musculus postoccipiti-prementualis (m. postoccip-prement.) (Figures 3, 6)

This muscle, the longest in the head of the worker

honey bee, has its point of fixed attachment on the

dorsal wall of the cranium next to branch II of m.

cran-intramand. In the drone and queen, however,

its point of fixed attachment is on the occiput adjacent to the posterior end of the tentorial body. In

all three castes, its point of movable attachment is

located on a long tendonlike apodemal growth arising

on the so-called ligular arm of the prementum. In

Vespula and Lasius the point of fixed attachment is

located on the tentorial body; in Stenobracon it is on

the clypeus. Matsuda (1957) regarded muscle "36,"

which "arises" from the hindmost end of the tentorium and "inserts" on the posterolateral angle of the

prementum, to be a homolog of this muscle. However,

when one compares the point of attachment of muscle "37" in Macrophya with m. postoccip-prement.

in the honey bee, these two appear to be homologs.

In Chauliodes and in Corydalus this muscle has its

point of fixed attachment on the posterior tentorial

arm and on the postgena, respectively, yet in generalized insects its point of fixed attachment is on the

postoccipital phragma. Apparently this muscle has

retained the primitive point of fixed attachment in

the drone and the queen honey bee but has shifted

it to the top of the cranial wall in the worker honey

bee, to the clypeus in Stenobracon, and t6 the posterior part of the tentorium in Macrophya and

Chauliodes.

The m. postoccip-prement. functions as a levator

of the paraglossa in Corydalus, a retractor of the

hypopharynx in Chauliodes, and a retractor or adductor of the labium in Lasius and Apis.

The musculus tentorio-prementualis (m. tent-prement.) (Figure 3)

The point of fixed attachment of this muscle is on

the anterior end of the pretentorium adjacent and

dorsal to that of m. tent-stip. II. Ahead of its point

of movable attachment it converges with its homolog

from the opposite side of the head and the two attach

to a single tendonlike apodemal growth arising medially from the proximal end of the prementum. According to Duncan, the homolog of this muscle in
NUMBER 99 19

Vespula has its point of fixed attachment on the

clypeus and remains paired. Accordingly, the points

of movable attachment of the pair are on separate

apodemal growths. In Lasius its point of fixed attachment is on the posterior end of the pretentorium but

its movable attachment is like that of the honey bee.

Stenobracon has almost the same attachment points

for this muscle as Apis. In Macrophya, Chauliodes,

Corydalus, and also primitive insects like Thermobia,

its fixed attachment is on the metatentorium. Apparently in Apis, Vespula, and Stenobracon, the fixed

attachment shifted to the pretentorium as the metatentorium was being lost. The m. tent-prement. acts

as a protractor of the labium in Vespula, Lasius,

Macrophya, Chauliodes* and Corydalus.

points of fixed and movable attachment of the

fused structure are, respectively, on the base of the

prementum and the posterior lingual plate. In Stenobracon this muscle is unfused and is attached as in

the honey bee. Matsuda (1957) stated that muscles

"41" and "43" of Macrophya are homologous to

this muscle, although he did not describe their points

of attachment. The m. prement-gloss. has not been

found in Chauliodes and Corydalus, but in several

primitive insects it attaches to the prementum and

the glossa. It appears that this muscle has shifted

is point of movable attachment from the glossa to

the side of its rods. In the honey bee, it is considered

to be a flexor of the glossa (retractor of the tongue)

as in other insects.

The musculus premento-paraglossaris (m. prementparagloss.) (Figures 6, 7)

This muscle has its point of fixed attachment on the

lateral base of the prementum. Its point of movable

attachment is on an apodemal growth arising from

the ligular arm of the prementum, just lateral to

that of m. postoccip-prement. In Vespula and Stenobracon, the points of movable attachment are on

the lingual plate and the basal sclerite of the paraglossa, respectively. According to Maki and Kelsey,

there is no homolog of this muscle in Chauliodes or

Corydalus, although it is rather commonly found in

lower pterygote insects. In the honey bee the points

of attachment seem not to have changed from those

found in generalized insects. The muscle acts as a

flexor of the entire ligula in Stenobracon and Vespula.

In the honey bee it was considered by Morison to be

a "flexor palpi maxillari," but Snodgrass (1942) referred to it as a retractor of the labium.

The musculus premento-glossaris (m. prement-gloss.)

(Figures 6, 7)

The point of fixed attachment is on the submedian

base of the prementum under that of the musculus

basipremento-salivarius. The point of movable attachment is on a long apodemal growth close to the

sides of the recurved basal part of the glossal rod.

In Vespula the same muscle is fused medially with

its homolog from the other side of the midline. The

The musculus premento-labiopalpualis (m. prementlabiopalp.) (Figure 6)

This muscle has its point of fixed attachment about

midway along the side of the prementum. The point

of movable attachment is located on a long tendonlike apodemal growth arising on a rod within the

basal lobe of the labial palpus (the palpiger). In

Vespula and Stenobracon the point of fixed attachment is located on the spatulate process of the prementum. Macrophya has two muscles that could be

designated as musculi premento-labiopalpuales. Their

points of fixed attachment are on the ventral side of

the base of the labial palpus. Chauliodes and Corydalus also have two muscles, differing from those of

Macrophya in being attached to the base of the

labial palpus on its ventral and dorsal sides. Primitive

insects also have two muscles attached in the same

manner as in Chauliodes. It appears that in Macrophya one of these muscles has shifted its point of

movable attachment from the dorsal side of the base

of the labial palpus to the ventral side, yet it has

disappeared completely in Stenobracon, Vespula, and

Apis.

This muscle is considered to be a flexor of the

palpus when its point of movable attachment is on

the ventral side of the base of the labial palpus. But

when this point is located dorsally on the base of

the palpus, the m. prement-labiopalp. is considered to

be a levator of the palpus.
20 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

The musculus labiopalpomere I-II (labiopalp. I-II)

(Figure 6)

The intrinsic labial muscles have not been as well

studied as other groups of muscles; consequently,

they will be treated rather superficially here.

Labiopalp. I-II has its point of fixed attachment

on the middle of the base of labiopalpomere I (first

segment of the labial palpus). The point of movable

attachment is located on an apodemal growth arising

from the base of labiopalpomere II. In Stenobracon,

Macrophya, and Corydalus there are two muscles in

labiopalpomere I. Matsuda (1957) found one muscle

in each of labiopalpomeres II and III in Macrophya.

The function of labiopalp. I-II apparently differs

among insects. For instance, in Grylloblatta the muscles of labiopalpomere I are extensors of labiopalpomere II (Walker 1931). On the other hand, Snodgrass considered it to be a flexor of the palpus in

the honey bee.

HYPOPHARYNGEAL MUSCLES

In generalized insects the hypopharynx forms the

ventral wall of the cibarium. The term "hypopharynx" is misleading since the structure itself is not related to the pharynx. It is a preoral structure, embryologically of composite origin. According to Matsuda

(1965), it is produced by the union of sclerites of

more than one gnathal segment. The term "lingue"

has been suggested as a replacement but such a

term is properly inter-oral. In the present investigation, the term hypopharynx is used because no proper

substitute is available.3

Some of the muscles classified under this section

were formerly classified as labial. Their close association with the hypopharynx, however, makes it less

confusing to consider them as hypopharyngeal.

The musculus dorsopremento-salivarius (m. dorsoprement-sal.) (Figure 6)

This muscle has its point of fixed attachment on the

anterior edge of the prementum and converges toward

the salivary syringe (a specialized salivarium). The

broad zone of its point of fixed attachment is located

3

 The term "inner internal lip" or "intra-internolabialum"

is suggested in this study as a replacement.

medially on the upper wall of the salivarium. In

Vespula, Stenobracon, and Macrophya it has the

same areas of attachment described for the honey

bee; however, in Chauliodes and Corydalus its point

of fixed attachment is on the mentum and the

pharyngeal plate, respectively. In more primitive insects (Thermobia, Periplaneta, Grylloblataria, and

others) it is located on the loral arm of the pharynx.

With the loss of the loral arm in various groups of

insects, this muscle had to shift its point of fixed

attachment to other skeletal areas, such as the

"ovoidal" sclerite in Psocoptera, the hind part of the

hypopharynx in Thysanoptera, or the anterior lateral

sides of the prementum in Hymenoptera. The m.

dorsoprement-sal. probably acts as a dilator of the

salivary syringe. According to Snodgrass (1942) it is

effective in the honey bee only when the proboscis

is in the protracted position.

The musculus basipremento-salivarius (m. basiprement-sal.) (Figure 6)

The point of fixed attachment is on the base of the

prementum above that of m. prement-gloss. The point

of movable attachment is located distally on the

lateral margin of the salivary syringe. Stenobracon,

Macrophya, and Chauliodes have approximately the

same points of attachment as the honey bee; however,

in Vespula the point of fixed attachment is within

the inflected apex of the lateral "spatulate process"

of the prementum, and that of the movable attachment is located partly on the proximolateral lobe of

the anterior lingual plate and partly on the margin

of the salivarium. Corydalus differs from other groups

studied by having its point of fixed attachment on

the ventromesal base of the palpiger. Although this

muscle is found in many groups of insects (Blattaria,

Isoptera, Orthoptera, Phasmida, Dermaptera, Ephemeroptera, and others), the primitive areas of attachment are difficult to determine because of their variability from group to group.

In Stenobracon and Vespula, m. basiprement-sal.

functions as a posterior dilator of the salivarium, but

in Corydalus it is considered to be a ventral dilator

of the salivary duct. Snodgrass suggestsd that it acts

as an expulsor of saliva by flattening the dilator

chamber. Apparently, in the honey bee it is effective

only when the proboscis is extended.
NUMBER 99 21

The musculus fronti-suspensorialis (m. fron-susp.)

(Figures 1, 3)

This muscle has its point of fixed attachment submedially on the frons below the median ocellus and

above m. front-labr. The point of movable attachment

is located dorsally on the nodelike process of the upper

portion of the hypopharyngeal suspensorium (pharyngeal arm of the oral plate). It is absent in Vespula.

In Stenobracon, Macrophya, Chauliodes, and Corydalus, and also in more primitive insects, m. fronsusp. has almost the same points of attachment.

Its function reportedly differs—it is a retractor of the

hypopharynx in Thermobia, Corydalus, and Apis

but a protractor in Periplaneta. Snodgrass considered

it to be a retractor of the oral plate, a part of the

hypopharynx.

The musculus tentorio-suspensorialis (m. tent-susp.)

(Figure 3)

This muscle has its point of fixed attachment on the

inner lateral side of the pretentorium. It is directed

toward the hypopharyngeal suspensorium and has its

point of movable attachment on the nodelike process,

opposite that of m. fron-susp. In both V. pensylvanica

and V. maculata this muscle has its point of fixed

attachment on a peglike process alongside the ventrolateral angle of the clypeus. In Stenobracon and

Macrophya it has the same points of attachment as

in the honey bee. In Chauliodes and Corydalus the

point of fixed attachment is on the metatentorium

and that of the movable attachment is on the posterior lateral portion of the anterior pharynx. This is

probably due to the undeveloped condition of the

hypopharyngeal suspensorium. In many orders this

muscle has its point of fixed attachment on the clypeus, rather than the tentorium. It even varies in

this regard between families of the same order. Accordingly, the name m. clypleo-suspensorialis has

been suggested. It functions as a suspensor in Thermobia and Corydalus but as a retractor in Periplaneta. According to Snodgrass it is a protractor of

the oral plate in the honey bee.

The musculus tentorio-oriscutarius (m. tent-oriscut.)

(Figure 3)

This has been classified by many authors (Janet, Duncan, Alam, Matsuda) as a stomodaeal muscle, probably on the assumption that the "functional mouth"

is a part of the stomodaeum. Since the basal part of

the anterior wall of the hypopharynx furnishes the

posterior wall of the cibarium, the oral plate in the

honey bee belongs to the hypopharynx and not to

the pharynx, as has commonly been thought. Consequently, the muscle that has its point of movable

attachment on the oral plate is actually hypopharyngeal.

The m. tent-oriscut. is an unpaired muscle probably resulting from fusion of an originally bilateral

pair. Its point of fixed attachment is on a tendonlike

apodemal growth arising from the median process

of the tentorial bridge. The broad point of movable

attachment is located medially on the oral plate.

Vespula, Lasius, Macrophya, and Chauliodes also

have this muscle unpaired and the points of attachment are similar to those of the honey bee. Stenobracon and Corydalus have it paired and attached

to the sides of the oral plate. The available literature

is fragmentary and misleading, owing to the misconception that the muscle is pharyngeal. Maki and

Kelsey, who classified it as belonging to the cibarium

or buccal cavity, considered it to be a dilator of

the cibarium. According to Duncan, Snodgrass, and

Alam, the m. tent-oriscut acts as a dilator of the

pharynx. Actually, when contracted, it pulls the oral

plate, which indirectly pulls the pharyngeal wall posteriorly, thus opening the mouth.

The musculus tentorio-suspensorialis (m. tent-susp.)

(Figure 3)

Since early entomologists usually considered the suspensorium and oral plate to be part of the pharynx,

I first devised the term "musculus tentorio-hypopharyngeosuspensorialis." For convenient usage, however,

it is probably better to limit the name of the movable

attachment to "suspensorium," especially since it has

been proved that the only suspensorium in the head

is of hypopharyngeal origin4 (Snodgrass 1956: Matsuda 1965).

This muscle has its points of fixed attachment on

the tentorial bridge, adjacent to m. tent-oriscut. It

spreads over the lateral and posterior walls of the

pharynx and runs beneath the musculus circulopha-

* Even as late as 1952, Alam used the term "pharyngeal

diverticulum" and "pharyngeal plate" for the hypopharyngeal suspensorium and the hypopharyngeal oral plate.
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ryngealis until it reaches the hypopharyngeal suspensorium on which it has its point of movable attachment. According to Duncan, its homolog in V.

pensylvanica is composed of short fibers which "insert

on the under side of the pharynx." In V. maculata, I

was able to trace a few muscle fibers to their attachment on the hypopharyngeal suspensorium. Matsuda

(1957) claimed that the homolog of this muscle is

absent in Macrophya but his muscle "14" which inserts on the "oesophageal" region, fits the description.

In Stenobracon it has the same points of attachment

as in the honey bee. The m. tent-susp. is probably

homologous to the "first ventral dilator of anterior

pharynx" in Chauliodes and Corydalus, which has

its point of movable attachment on the ventral wall

of the "anterior pharynx." In general this muscle

has been poorly studied. Consequently, I am unable

to determine whether the primitive point of movable

attachment is on the pharynx or hypopharynx. If it

proves to be the pharynx, the name should be changed

to "musculus tentorio-pharyngealis." On such a basis

the assumption would be that its movable attachment was shifted to the suspensorium as a later

development.

According to Snodgrass, m. tent-susp. functions in

the honey bee as a contractor of the pharynx. But,

judging from its action of pulling the suspensorium

backward, I suggest that it acts as indirect dilator of

the pharynx.

The musculus oriscuto-suspensorialis (m. oriscutsusp.) (Figure 3)

This fan-shaped muscle has not been previously described or illustrated in the honey bee. Its point of

fixed attachment is on the middle of the oral plate.

The m. oriscut-susp. lies adjacent to the anterior wall

of the pharynx and extends laterally toward the suspensorium, on which it has its broad point of movable

attachment. It is probably the homolog of the "posterior intrinsic muscle of the pharyngeal diverticulum" in Vespula, which extends transversely on the

upper half of the anterior pharynx, and is homologous to the "ventral constrictor of the cibarium" in

Corydalus. These are the only descriptions in the literature that seem to pertain to this muscle. Accordingly, for the time being, a sound homology is

impossible.

The m. oriscut-susp. may function as an indirect

dilator of the pharyngeal wall since it exerts direct

pull on the hypopharyngeal suspensoria.

ANTERIOR CIBARIAL WALL MUSCLES

These muscles are attached to the anterior cibarial

wall (the inner clypeal wall). Entomologists have

usually classified them as pharyngeal, but since they

are attached to preoral structures rather than the

pharynx, the traditional classification seems to be improper. Kelsey (1954) classified them as cibarial. The

term "cibarium" refers to the preoral food-receiving

pocket formed between the inner clypeal wall and

the base of the hypopharynx, but not to the wall itself.

Accordingly, the expression "muscles of the cibarium"

is not precisely accurate. My first thought was to

group these muscles as "inner clypeal wall muscles,"

but in many insects the inner clypeal wall also

enters into the formation of the epipharynx. Consequently, the expression "anterior cibarial wall muscles" is coined as a replacement.

The musculi clypeo-cibarioparietales (m. clyp-cibpariet.) (Figure 1)

The number of these muscles in the honey bee varies

from five to seven pairs; the usual number is six pairs.

Their points of fixed attachment are on the cranial

wall of the clypeus, parallel to the epistonaal sulcus.

They diverge internally toward the inner wall of the

clypeus (anterior cibarial wall), where they have

their points of movable attachment between the bundles of the musculus intrasuspensorialis dorsualis.

Snodgrass (1942) stated that "the lower part of the

organ [the sucking pump] has five pairs of large bundles of dilator muscle fibers attached on its anterior

wall . . . ." Yet his illustration (p. 31, fig. 10c) shows

only five bundles of muscle fibers. Also, his illustration of the points of movable attachment are not accurate (fig. 10D). Duncan stated that V. pensylvanica

has only one muscle pair, but I found two pairs in V.

maculata. This group of muscles is represented by

two pairs in Lasius and Corydalus, one pair in Stenobracon, and four pairs in Macrophya and Chauliodes.

In primitive insects, the number of these muscle bundles varies greatly. In all cases, however, they have

the same areas of attachment5 as in the honey bee.

5

 Unfortunately, the earlier entomologists gave the name

pharynx to the cibarium and consequently many authors

believed the cibarial muscles to be attached to the pharynx.

Their drawings, however, showed them attached to the

anterior cibarial wall.
NUMBER 9 9 23

The musculus intersuspensorialis dorsualis (m. intersusp-dors.) (Figure 1)

This muscle consists of many bundles, each extending between the two suspensoria. The different bundles can be classified into three groups: (1) those

running transversely just above the epipharynx, (2)

those running obliquely between the bundles of the

m. clyp-cibpariet. to form a net, and (3) those running transversely in the area between the level of the

Ganglion Pharyngeale and the first pair of m. clypcibpariet. Snodgrass (1942:103) made the following statement with regard to this muscle: "Five thick bundles

of fibers on the anterior wall of cibarial region of

sucking pump. The first transverse over the mouth,

the others oblique between the dilators, attached laterally on the oral plate." The findings of the present

study agree with those of Snodgrass with regard to

the first muscle bundle but not the other four bundles. At least thirteen muscle bundles extend obliquely

to form a net, and they are attached to the hypopharyngeal suspensoria rather than the oral plate. Snodgrass did not describe the third kind of bundle, although he illustrated it (p. 31, fig. 10c). The "upper

longitudinal muscle of the pharyngeal suspensorium"

of Lasius may be the homolog of the second and third

groups of muscle bundles in the honey bee. Also, these

two groups of muscle bundles are probably the homologs of the "anterior intrinsic pharyngeal muscle" and

the "pharyngeal dilator of the mouth" in Vespula.

Matsuda (1957) stated that there is no homolog of

this muscle in Macrophya. An examination of his

drawings (p. 103, pi. ILy, B) however, indicates that

muscle "16" may be its homolog. According to Kelsey, the only bundles represented in Corydalus could

be homologous to the third group described above.

Since descriptions are scarce, no practical homology

could be established for this composite muscle. The

m. intersusp-dors. probably acts as a constrictor of

the anterior cibarial wall.

PHARYNGEAL MUSCLES

Matsuda (1965) classified all the muscles attached

to the cibarial wall, oral plate (of hypopharyngeal

origin), and the pharynx as pharyngeal muscles. In

this study, only the muscles attached to the stomadaeum (the true pharynx) are considered as pharyngeal. The pharyngeal muscles can be classified under

three subgroups: dorsal, ventral, and circular.

Dorsal Muscles of the Pharynx

The musculus fronti-pharyngealis I (m. fron-phar. I)

(Figures 1, 3)

This muscle has its point of fixed attachment submedially on the frons below that of the musculus

fronti-pharyngealis II. The point of movable attachment is located on the pharynx beyond the

Ganglion Pharyngeale and in front of the movable

attachment of musculus fronti-pharyngealis II.

The musculus fronti-pharyngealis II (m. fron.-phar.

II) (Figures 1, 3)

The point of fixed attachment is on the frons, just

above that of the m. fron-phar. I and below the

median ocellus. The broad point of movable attachment is located on the pharynx posterior to that of

the m. fron-phar. I.

The musculus fronti-pharyngealis III (m. fron-phar.

Ill)

Although this muscle has not been described or

illustrated for any of the three castes of the honey

bee, I found it in the drone. It is a very small

muscle, about one tenth to one fifth the size of m.

fron-phar. II. It often extends over the pharynx,

making it hard to distinguish. Its point of fixed attachment is located submedially on the frons, dorsad to that of m. fron-phar. II. Its point of movable

attachment is on the anterior portion of the pharynx,

laterad and posterior to that of m. fron-phar. II. In

many instances, it was found to be loose from its

point of fixed attachment, suggesting that it is degenerating.

For convenience, these last three muscles are classified under a subgroup with the name musculi

fronti-pharyngeales. They have been found on all

groups of insects studied. Matsuda (1965) classified

them in primitive insects as anterior, posterior, and

lateral. In many cases each one is represented by

more than one bundle. The number of these muscles

varies among insects. As a general rule, they have

their points of fixed and movable attachment on

the frons and on the pharynx in front of the Ganglion Hyperoesophagale, respectively. In Stenopsocus

(Psocoptera), however, the fixed attachment is on

the clypeus (Matsuda 1965). In V. pensylvanica
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

this group is represented by a single muscle; in V.

maculata, I found two, the posterolateral one is

very small and degenerate. In Lasius there are three

well-developed muscles belonging to this group.

Stenobracon has only one, but Macrophya, Chauliodes, and Corydalus have two.

All authors agree that the musculi fronti-pharyngeales act as dilators of the anterior part of the

pharynx.

The musculus cranio-pharyngealis (m. cran-phar.)

(Figure 3)

In the worker and queen, this muscle has its point

of fixed attachment on the vertex. In the drone, it

is attached submedially on the inner lamella of the

compound eye.6 In all three castes, the point of

movable attachment is on the posterior portion of

the pharynx in front of the corpus cardiacum. In

the majority of the drones dissected in the course of

this study, this muscle was loose from its point of

fixed attachment or was attached with two to four

extremely small fibers. In other Hymenoptera and

Neuroptera, the m. cran-phar. has the same points

of attachment as that of the worker honey bee. In

a few insects, however, its fixed attachment has

shifted to the postoccipital area or vertex. In the

drone honey bee, the shift was probably necessitated

"Snodgrass (1956) only illustrated these lamellae and

named them the "midcranial ridge," on the assumption that

they comprise a single structure. Dissection, however, revealed that the inner margin of each compound eye is surrounded by a separate lamella. Because of the closeness of

the compound eyes at the top of the head in the drone, these

lamellae are approximate and appear as one ridge.

by the large compound eyes and their expansion

onto the postoccipital area. In all insects studied,

this muscle functions as a dilator of the posterior

pharynx.

Ventral Muscles of the Pharynx

These muscles have their points of fixed attachment

on the tentorium and their points of movable attachment on the pharynx. In the honey bee there

is no unequivocal ventral muscle, although the m.

tentorio suspensorialis (classified in the present investigation as a hypopharyngeal muscle) may belong to this group. More research is needed, however, to determine the primitive areas of movable

attachment before a definite assignment can be

made.

Circular Muscles of the Pharynx

The musculus, circulopharyngealis (m. circulophar.)

(Figure 3)

This muscle is composed of ring-shaped bundles

that ensheath the entire pharynx posterior to the

hypopharyngeal suspensoria and cover the musculus

tentorio-suspensorialis. Homologous muscles in other

insects are usually identified as ring or circular

muscles. In some insects (Psocoptera) the m. circulophar. is reduced to a series of transverse bundles

between the suspensoria. In larval Diptera, it is

well developed even though it is absent in the adults.

There is general agreement that it functions as a

constrictor of the pharyngeal walls.
PART II. NERVOUS SYSTEM

History

Nervous systems may be studied from various viewpoints. The basic questions, however, are always

those of homology and of the relationships between

nerve-structure, physiological, and behavioral patterns. Despite intensive histological studies, there is

still a surprising lack of information about both

functional nerve anatomy and nerve homology. To

some degree this is because of an insufficient knowledge of the detailed topography of the whole system.

Table 4 presents an annotated list of the more

important topographical and histological studies on

the nervous systems of insects. In the subsequent text,

references are made to nervous tissues of insects included in this table. The reader can refer to the

table to find the authors and dates and then to the

Literature Cited for complete citations. Physiological

studies are not included in the table since, for the

most part, they are not germane to this investigation. Articles dealing with each cephalic ganglion

and the main nerves emanating from them for insects in general, and Hymenoptera in particular, are

reviewed and comparisons are made with comparable structures in the topography section.

Methods of Nomenclature

MAIN GANGLIA AND THEIR DIVISIONS

Nomenclature for the insect nervous system has

lagged behind that of other systems. As Snodgrass

stated (1931:31), "The basic plan is found to be

simple; but, as so often occurs in insect morphology,

more difficulties are encountered in finding suitable

terms to express the facts than in discovering the

facts themselves." Some of the reasons for the difficulties are: (1) the belief that nerve homology is

not practically possible because of the diversity of

patterns in different insects; (2) a standard terminology would imply homology that often does not

exist because of differing degrees of bundling of

nerve axons; and (3) detailed topographical studies

of the cephalic nervous system of insects are scarce

(Table 4).

In spite of the extensive morphological, histological, and physiological investigations of the socalled brain (Bullock and Horridge 1965), the study

of nerve topography in the insect head and its relationship with other tissues is still fragmentary. Even

so, the nomenclature of the "brain" and its different

divisions is misleading and sometimes inaccurate.

Table 5, an analysis of the literature, shows the

different systems of nomenclature devised by different authors (and followed by others) for the

various nerves and divisions of the "brain."

The term "brain," according to the current usage

for insects, means "the cephalic nerve mass situated

above the stomodaeum, including the primitively

postoral second antennal ganglia" (Snodgrass 1935:

507). This belief probably dates back to the time of

the discovery of the microscope. Some authors, however, have questioned which parts of the nerve mass

should be included under the "brain." Binet (1894)

and Kenyon (1896) applied the term "brain" to

the whole neural mass found within the head execpt

for what they called the "stomogastric ganglia."

Others have avoided using the term "brain" by

using noncommittal expressions. Crauss, as early as

1884, used the term supraoesophageal ganglia.

Kenyon (1896) designated. nerve tissues above the

stomodaeum as "the superintestinal portion or

dorso-cerebron." Jonescu (1909) considered the

nerve mass above the oesophagus as a single ganglion, which he named "the supraoesophageal

ganglion."

In the present investigation the term "Ganglion

Hyperoesophagale" is used for the following reasons:

(1) it does not infer a close homology or analogy

with the "brain" as found in vertebrates, (2) it does

not indicate any function and is strictly morphological, (3) the prefix "hyper" (of Greek origin) fits

better than "supra" (of Latin origin) for usage with

the Greek term oesophagus, and (4) the term ganglion

refers to a composite structure and does not need

a plural ending even though more than one neural

25
26

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 4.—Major investigations on the cephalic nerve tissues of insects

Author Year Order Family Species Major contribution in relation to present study

Newton

Packard

Crauss

Vallianes

Kenyon

Janet

Hammar

Jonescu

Holste

Peterson

Mclndoo

Swainc

Nelson

James

Denis

Hillcman

Hanna

Snodgrass

Graichen

Maki

Marquadrat

Rehm

Nesbitt

Power

Bucher

Cliaudcnncrct

Snodgrass

Jawlowski

Sahja

Buckup

1879

1880

1884

Orthoptera

Orthoptera

Neuroptera

!S8 7a,b General

1896

1905

1909

1909

1910

1912

1914a

1920

1924

1926

1928

1933

1935

1935

1936

1936

1939

1939

1941

1943

19481

Hymenoptera

Hymnoptera

Neuroptera

Hymenoptera

Coleoptera

Lepidoptera

Hymenoptera

Lepidoptera

Hymenoptera

Hymenoptera

Collembola

Lepidoptera

Hymenoptera

Orthoptera

Hemiptera

Neuroptera

Phasmida

Hymenoptera

Orthoptera

Diptera

Hymenoptera

1950-51 Thysanura

1956

1958

1958

1959

Hymenoptera

Hymenoptera

Hymenoptera

Mallophaga

Blattidae

Acrididae

Corydalidae

-

Apidae

Formicidae

Corydalidae

Apidae

Dytiscidae

Sphingidae

Apidae

Hepialidae

Apidae

Eurytomidae

-

Papilionidae

Chalcididae

Acrididae

Nepidae

Sialidae

Lonchodidae

Apidae

-

Drosophilidae

Torymidae

Lepismatidae

Apidae

Apidae

Apidae

Amblycera

Blatta oriental is Linn.

Melanoplus femurrubrum PeGeer

Corydalus comutus Linn.

General

Apis mellifera Unn.

Lasius niger Reine.

Corydalus comutus Linn.

Apis millifera Linn.

Dytiscus marginalis Linn.

Protoparce sexta Johan.

Apis mellifera Linn.

Sthenopis thule Strecker

Apis mellifera Linn.

Harmolita graminicola Giraud.

Various species

Papilio polyxenes Fab.

Euchalcidia caryobori Hanna

Dissosteira Carolina Linn.

Nepa cinerea

Chauliodes formosanus Peterson

Carausius (Dixippus) morosus Br.

Apis mellifera linn.

Various species

Drosophila melanogster Meigen

Monodontomerus dentipes Boh.

Thermobia domestica Packard

Apis mellifera Linn.

Apis mellifera Linn.

Apis mellifera Linn.

Myrsidea cornicis Degeer

Gross anatomy of main nerves, general histological studies on the adult

Gross anatomy of main nerves of Ganglia Hyper- and Hypoesophagalia

in the adult

Gross anatomy of the main nerves of Ganglia Hyper-and Hypoesophagalia in tl

larvae

Histology of the Ganglia Hyper- and Hypoesophagalia of the adults

Mainly gross anatomy of the nerves of Ganglia Hyper- and Hypoesophagalia

in the adult

Topography of the main nerve tissues found in the head, innervation of some

muscles in the adult worker

Incomplete topography of the nerve tissue found in the head, innervation of

a few muscles in the larva

Detailed histological studies of the Ganglion Hyperoesophagale in the adult

(three castes)

Nearly complete topography of the cephalic nerve tissues and innervation of

its muscles in the adult

Gross anatomy of the main nerves of the Ganglia Hyper- and Hypoetophagalia

in the larva

Sense organs associated with the mouthparts in the adult (worker)

Gross anatomy of the main nerves of the Ganglia Hyper- and Hypoesophagalia

in the larva

Grot* anatomy of the Ganglia Hyper- and Hypoesophagalia in the larva

Gross anatomy and rather incomplete histology of the Ganglia Hyper- and

Hypoesophagalia in the adult

Topography of the cephalic nerve tissues and innervation of other tissues

found in the head of the adults

Gross anatomy of the Ganglia Hyper- and Hypoesophagalia in the adult

Gross anatomy of the Ganglia Hyper- and Hypoesophagalia in the adult

Gross anatomy of the Ganglia Hyper- and Hypoesophagalia and their main

nerves in the adult

Detailed histological study of the Ganglion Hyperoesophagale in the adult

Topography of the cephalic nerve tissue, innervation of some muscles found

in the adult

Incomplete topography of the cephalic nerve tissue, innervation of some

muscles found in the adult head

Study of muscles innervated by Nervus Mandibularis and Ncrvus Posterior

in the adult (worker)

Gross anatomy of the Ganglia Hyper- and Hypoesophagalia of the adults

Detailed histological study of the Ganglion Hyperoesophagale of the adult

Gross anatomy and histology of the Ganglia Hyper- and Hypoesophagalia in

the adult

Rather complete topography of the cephalic nerve tissues, following each

nerve to its termination

Gross anatomy and histology of the Ganglia Hyper- and Hypoesophagalia in

the adult (general)

Detailed histological study of the Ganglion Hyperoesophagale in the adult

(worker)

Detailed histological study of the Ganglion Hypcroesophagalc in the adult

(worker)

Gross anatomy of the Ganglia Hyper- and Hypoesophagalia and their main

nerves in the adult

'"Brain" of other authors

"Subocsophagcal ganglion" of other authors

mass may be included. Viallanes (1884), independently of embryological data, divided the Ganglion

Hyperoesophagale into three regions: "protocerebron," "deutocerebron," and "tritocerebron" which

he later (1893) found to correspond with the three

"primitive elements of neuromeres." Since that time

morphologists have used these terms or modifications

of them. For the reasons given previously, these terms

are respectively changed to Ganglion Proto-hyperoesophagale, Ganglion Deuto-hyperoesophagale, and

Ganglion Trito-hyperoesophagale.

The nerve mass usually found beneath the stomodaeum in the head is generally known as the "suboesophageal ganglion" (the cerebellum of Crauss

1884; the ventrocerebron of Kenyon 1896). According to Snodgrass (1935) the so-called suboesophageal ganglion is a composite of three ganglia of

the ventral nerve cord belonging to those segments
NUMBER 99 27

TABLE 5.—Nomenclature of cephalic nerve tissues used by different authors

Order

Nerve tissue/Author

Ortho

Me Ian

Packa

ptera

oplus

rd (1880)

Meg

Cor

Cra

aloptera

yd"!""

uss (1884)

Hymenoptera

Apis

Kenyon (1896)

Hymen

Lasiu

Janet

8 niger

(1905)

Corydali.

Hamnar

-

(1908)

Discoste

Snodgrao s (1935)

Hymenoptera

A£iS

Present study

Ganglion Hyperoesophagale

(Br.ln)

Optic lobe Ganglion ProtoByperoesophagale

Optic ganglion

Ocellar nerve Optic ne

Ocullar nerve

Ganglion of the Ocellur nerve

Antennal olfactory Cephalad tract Atennal lobe Deutocerebro

lobe

Antennal nerve Antennal nerve Antennal nerve Antennal nerve

Oesophageal lobe Tritocerebron Tritocerebron

Nervus ocellaris

Nervus antennalls

Tri tocerebrum

frontalis

Nerve

labrun

Labral nerve

ntal ganglio

Sensory nerve of

ganglio

the two hemisphere a

Transverse

oesophagus

connective

Clypeo-labral Labral nerve

nerve

Suboesophageal Suboesophageal comGanglion DeutoHyperoesophagale

Nervus Antennalis

Ganglion TritoHyperoesophagale

Nervus GangliPharyngealis

Comnissura Gang 11-

orum Trito-Hyperoesophagalium

Ganglion Hypoesophagale

(Suboegphageal

ganglion)

mlssure to the

•uboesphageal

ganglion

Nerve to the

mandible

Maxillary nerve

Labial nerve

Mandtbular nerve

Maxillary nerve

Labial nerve

commissure

Mandibular

Maxillary

Labial ner

nerve

nerve

ve

connective

Nerve to the

mandibular

metamere

Nerve of the

maxillary

metamere

Nerve of the

labial metamere

Salivary nerve? Salivary nerve Salivary nerve Nerve of the

labial gland

Mandibular nerve Mandibular nerve

Gustatory nerve Rypopharyngeal

nerve

Maxillary nerve Maxillary nerve

Labial nerve Labial nerve

Salivary nerve Salivary nerve

Connective GangHorum Hyper-Hypoesophagallum

Nervus Mandibularis

Nervus Maxillarls

Nervus Labrualis

Nervulus Glandulaw Thoraclcalis

that became the gnathal region of the insect head.

For these two reasons the name Ganglion Hypoesophagale is used as a replacement.

The commissure that extends between the pair of

Ganglia Trito-hyperoesophagale has been given several names (Table 5) : "commissure between the

two hemispheres," "transverse commissure of the

oesophagus," "suboesophageal commissure," and

"tritocerebral commissure." Unfortunately, these

names (except the last, coined by Snodgrass 1935)

are misleading because they do not accurately describe either the function or the position of this

commissure. The last name (tritocerebral commissure) is accurate, but the term "cerebral" is questionable for reasons already given. Accordingly, the

term Commissura Gangliorum Trito-hyperoesophagalium is used here as a replacement.

Nerve cords connecting the Ganglion Hyperoesophagale to the Ganglion Hypoesophagale have

been variously named as follows (Table 5) : (1) "oesophageal commissures to the suboesophageal ganglion," (2) "oesophageal commissures," (3) "circumoesophageal connectives," (4) "crura cerebri"

and (5) "cerebrognathal connectives." The first

name does not indicate what is connected to the

"suboesophageal ganglion." The second and third

are incomplete, and they emphasize the oesophagus

rather than nerve tissues. The fourth name is misleading since the word "crura" is derived from the

Latin word "crus" or "cruris" which means leg.

The fifth name (proposed by Janet 1905) is more

descriptive than the others. However, it does not

indicate to which gnathal nerve tissue the "cerebron"

is connected. Following the same pattern used by

Janet, the term Connectivi Gangliorum Hypo-hyperoesophagalium is proposed as a replacement.
28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

NERVES AND THEIR BRANCHES

Earlier authors investigating main nerves innervating the gnathal segments of the head have named

each nerve according to the segment it innervates,

e.g., "mandibular nerve," "maxillary nerve," etc.

Some investigators put the names in their native

languages and others combined Latin and the native

language. In the present investigation terms based

on classical Greek or Latin are used.

Studies of the topography of the branch nerves,

which eventually subdivide into nervules innervating

the cephalic tissues, have been infrequent and usually fragmentary. The paucity of published information and questions concerning the homology of this

branching make it inadvisable to attempt a homologous system for these branches at this time. Bullock

and Horridge (1965:869), after reviewing almost

all of the available literature, concluded that "a

standard terminology which suggests that a nerve

of one species is the same as a nerve in another

species is in detail misleading because the axon

constituents are almost certainly different." Their

statement refers particularly to the main- and

branch-nerve level rather than the nervule (innervation) level. The principal problem with the nerves

seems to be the coalescence or the bundling of

axons that has taken place to varying degrees in

different orders. However, as Bullock and Horridge

(p. 876) admitted, "the physical condition that

governs the growth of axons and their grouping into

nerve bundles is believed to be of similar pattern

in a large range of insects."

According to my observations in the Hymenoptera,

good homology can be ascertained at the branch

level by working carefully from one related group

to the next. Where large evolutionary gaps are

unavoidable, probably histological and physiological

studies could be required.

Homology is easier to establish for the terminal

branches that actually innervate the tissues than for

the more proximal branches or the main nerves.

Reasons for this will be presented later. Although

Janet (1905) did not study innervation of muscles

or follow each nerve to its termination, he named

three "nerves" according to the muscles they innervate (nerf du muscle dilatateur inferieur du pharynx,

nerf moteur des muscles clypeopharyngiens, and nerf

moteur du muscle adducteur du labre). Hammar

(1908), in his fragmentary work in Corydalus,

designated the branches of each main nerve with

Arabic numerals, i.e., branch 1, branch 2, etc. Holste

(1910) modified this system by adding the abbreviated form for a main nerve (maxillary nerve equals

nmx) to an Arabic numeral, i.e., nmxl, nmx2, etc.

According to the available literature, Denis

(1928), Maki (1936), and Chaudonneret (1950-

1951) are probably the only morphologists who

followed each nerve, branch, or subbranch to its

termination. Unfortunately, their systems for nerve

nomenclature (combinations of letters and numbers)

are difficult to follow, morphologically meaningless,

and are not adaptable for studies of nerve homology.

In the present investigation, nerves leaving the

Ganglion Hyperoesophagale and the Ganglion Hypoesophagale are named according to the segment

or major area they innervate (ocular, ocellar, mandibular, maxillary). If only one pair of lateral

nerves7 innervates a certain segment or area, each

lateral nerve is recognized as a Nervus. If one of

the pair branches, however, it is designated as a

Nervus and each branch as a Nervus Lateralis. If

a Nervus Lateralis branches, each branch is recognized as a Nervus Sublateralis provided it does not

innervate any tissue before dividing. The portion of

the neural mass that innervates a muscle or other

type of tissue is designated as a Nervulus, which may

be a branch of a nerve, a lateral nerve, or a sublateral nerve. Each Nervulus is named after the tissue

it innervates for the following reasons:

1. No standardized system is in use, and the systems that have been used are generally composed of

meaningless letters and numbers arbitrarily chosen

for each insect studied.

2. As stated previously, homology usually is not

difficult to perceive at the nervule level. This is because each nervule supplying a tissue has a limited

number of axons (usually two or three per muscle

[Bullock and Horridge 1965]), whereas the more

proximal nerves have variable and larger numbers

of axons, depending upon the number of structures

innervated. Unless a structure is innervated from

more than one source, its neural supply will be es7

 In some insects nerves innervating the mouthparts are

not exactly lateral in position. This can be explained, however, by the assumption that the ancestral insect was annelidlike with no head appendages and with circular segmental muscles innervated by lateral nerves. (Snodgrass

1935:475).
NUMBER 9 9 29

sentially the same as that of its homolog in other

insects. In a few cases a single muscle in the head

is innervated by more than one nervule arising from

the same ganglion. Assuming that the homolog muscle in some other insect has only one nervule, it is

not possible to establish a clear homology without

histological work. In such cases these nervules are

given a collective term, Nervuli.

3. In the thorax a muscle appearing to be an

integral part of one segment may be innervated by

two coalesced Nervuli, one arising from its segmental

ganglion and the other from a different ganglion.

This has been shown experimentally by Niiesch

(1954) in the thorax of Telea polyphemus Cr.

(Saturniidae) and histologically by Pipa and Cook

(1959) in the thorax of Periplaneta americana

Linnaeus (Blattidae). In such situations, more comparative investigations on muscle and nerve homologies between closely related genera, rather than

orders, should clarify the problem to some extent.

Histological and electrostimulation techniques may

also become necessary. Despite the above problems,

the proposed system of nomenclature can be a

useful tool for understanding muscle homology and

the shifting of either the point of fixed or of movable

attachment, or both. The ability of the imaginal

buds of holometabolous insects (at least in Lepidoptera) to develop muscles depends on the presence of

their nerve supply (Kopec 1918, 1922; Richards and

Miller 1937). Niiesch (1952) and Williams and

Schneiderman (1952) demonstrated that the extirpation of a ganglion or cutting off a single nerve

in the thorax of a diapausing pupa of Telea polyphemus results in an adult lacking the group of

muscles normally innervated by the eliminated ganglion or nerve. Their facts indicate that the muscle

anlagen of the pupa requires innervation in order

to develop normally during the formation of the

adult. Accordingly a nervule of a hypothetical "muscle X" is essential for the development of this muscle, whether the gross anatomy shows that this nerve

arises from the first or second ganglion. If the investigator suspects that "muscle X" is homologous

in the various species under study, he can verify

his suspicion by histological studies of the nerve

tissues involved.

4. Comparative studies of the cephalic musculature in insects (Matsuda 1965) revealed that homology can be established between muscles of different species. This seems to indicate that homology

can be reached between Nervuli of different muscles,

when complete data on the innervation of the

muscles are available.

Topography and Homology of the Cephalic Nerve

Tissue

In this investigation, the cephalic nerve tissue is

described with regard to its gross anatomy and topography and to its relationships with other tissues

(muscular, glandular, integumental, and stomodaeal)

in adult queen, worker, and drone honey bees. It

also includes a comparison between the nerve patterns of honey bees and those of related pterygotes.

The following are the principal cephalic nerves

listed under the ganglia with which they are

associated:

Ganglion Hyperoesophagale

Nervi Optici and Nervi Ocellares

Nervus Antennalis

Nervus Ganglii Pharyngealis

Nervus Labrualis

Nervus Musculi Tentorio-oriscutarius

Nervus Corpoallatialis

Ganglion Hypoesophagale

Nervus Mandibularis

Nervus Maxillaris

Nervus Labialis

Nervus Tegumentualis

Nervus Postoccipitalis

Nervus Posterior

LOCATION AND TOPOGRAPHY OF THE Ganglion Hyperoesophagale

Many early investigators studied this structure with

the assumption that it is similar to the brain of

vertebrates, but more recent physiological as well

as morphological studies have shown that it is only

crudely analogous at most.

Its principal nerves are essentially the same among

different insects, but some obvious differences are

related to the shape of the head, the position of the

eyes, and the arrangement of such internal structures

as the tentorium, muscles, glands, and stomodaeum.

In the honey bee the Ganglion Hyperoesophagale

is a composite nerve mass occupying almost the entire

upper portion of the head cavity. It is surrounded

by muscles beneath, glands above and at the sides,

and fat bodies and tracheae in between. The position
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of this nerve mass varies among the three castes as

dictated by differences in the shape of the head,

the size of the compound eyes, and the location of

the simple eyes. The Ganglion Hyperoesophagale

in the honey bee occupies a location similar to that

in Lasius, as shown in Janet's drawings (figs, F, G,

H, i) and in Vespula maculate.

In the worker honey bee the Ganglion Hyperoesophagale (Figure 1) lies directly against branches

I and II of the m. cranio-intramandibularis, the

m. postoccipiti-prementualis, and parts of the salivary gland. Between the frontal surface of this nerve

mass and frons is an area as broad as the nerve

mass itself, which is occupied by the pharyngeal

gland. The anterior and posterior surfaces of the

ganglionic mass are parallel to each other. The

ocelli are arranged in a triangle at the vertex of

the worker's head, causing their field of vision to

be directed vertically upward. Accordingly, the median part of the Ganglion Hyperoesophagale is at

a higher level than the dorsal part of the compound eyes (frontal view, Figure 1). In sagittal

view, the ganglion follows a vertical axis which is at

a 90-degree angle to that of the ventral nerve cord

(Figures 2, 3).

In the queen this ganglionic mass occupies a

more central position than in the worker, and the

anterior surface of the Lobus Opticus is nearly

covered with the enlarged mandibular glands. The

mass is similar in shape to that of the worker but

is somewhat wider. The ocelli, forming a triangle,

are located on the slope of the vertex, causing their

field of vision to be directed upward at an angle

of approximately 45 degrees. Consequently, the median part of the ganglionic mass is at the same level

as the dorsal part of the compound eyes. Its inclination (using the same axis as that of the worker)

is approximately 110 degrees. The queen's Lobus

Opticus is smaller than in the other castes, but its

shape and orientation are similar to those of the

worker.

In the drone the Ganglion Hyperoesophagale is

almost adjacent to the frons. This location may be

dictated by the highly developed compound eyes.

The area between the posterior surfaces of the

median part of this ganglion is tightly packed with

tracheae. The ocelli are in completely different locations from those of the queen or worker. According to Jonescu (1909), however, the Nervi Ocellares

have the same origin in the Ganglion Hyperoesophagale in the three castes. The ocelli of the drone are

arranged in a triangle, but on the frontal side of

the head, causing the field of vision to be directed

forward. Accordingly, the median part of the Ganglion Hyperoesophagale is lower than the tips of

the compound eyes and inclined about 130 degrees,

which is greater than in the other castes. The

drone's Lobus Opticus is strikingly the largest of

the three castes, due without doubt to its exceptionally large compound eyes. This lobe differs in the

drone from its homolog in the worker and queen

by being bent apically toward the rear.

The Ganglion Hyperoesophagale of insects can

be divided into three portions: Ganglion ProtoHyper oesophagale, Ganglion Deuto-Hyperoesophagale, and Ganglion Trito-Hyper oesophagale. Each of

these ganglia gives rise to several nerves.

Ganglion Proto-Hyperoesophagale

Lobus Opticus.—'Leydig (1864) probably was the

first author to use "sehlappen" (optic lobe) for the

lobes that represent lateral elongations of the "protocerebrum" in which the optic centers are located.

The size of the Lobus Opticus differs among insects. In many cases, as in Corydalus (Crauss 1884),

it is rudimentary. Its size and shape sometimes differ

between the sexes, as in the honey bee (Jonescu

1909). Ehnbom (1948) found that the exterior

structure of the "cerebrum" varies considerably in

different lepidopterous groups depending upon the

development of the Lobus Opticus. He classified

this structure in Lepidoptera into four types:

(1) Rhopalocera types, with a square cross section;

(2) Macrofrenatae type, constricted into two distinct parts; (3) Tineoidea type, separated ventrally

from the "protocerebrum" but merging dorsally with

the protocerebral lobe; and (4) Micropterygidae

type, essentially like that of a Trichoptera.

In the honey bee worker the Lobus Opticus,

which constitutes a great portion of the Ganglion

Hyperoesophagale, is intermediate in size between

that of the drone and queen. A horizontal section

indicates that in the worker this lobe is in the same

plane as the Ganglion Proto-Hyperoesophagale.

Nervi Optici.—These are the retinal neurites of

the compound or simple lateral eyes and are received

in the outer end of the optic lobes (Lobi Optici).
NUMBER 9 9 31

Therefore, the Nervi Optici are generally very short.

The Nervi Optici differ, however, in caterpillars

which have rudimentary optic centers.

Crauss (1884) and Hammar (1908) observed the

Nervi Optici in Corydalus. Both authors stated that

the main "optic nerve" is divided into seven

branches even though the larva has six ocelli.

Viallanes (1887a) described the Nervi Optici in

Vespa crabro Linnaeus and called them "la couch

post-retinienne" (the postretinal layer).

Jonescu (1909), in his histological study of the

drone honey bee, followed the terminology proposed

by Viallanes and stated that the structure of the

Nervus Opticus layer is the same as in the other

two castes.

According to Holste (1910), Dytiscus marginalis

Linnaeus has a single Nervus Opticus, which he

described (p. 424) as "Dieser ist bei weitem der

starkste alien Nerven" (This is by far the strongest

of all nerves). Peterson (1912) stated that the

"optic nerve" in the larva of Protoparce sexta is

very small and extends laterally without branching

until it reaches the area where the lateral simple eyes

are located. Swaine (1920) and Hilleman (1933)

found almost the same situation in the larvae of

Sthenopas thule and Papilio polyxenes, respectively.

According to Ehnbom's histological studies (1948),

Trichoptera larvae have no Nervus Opticus.

Nervi Ocellares.—According to Snodgrass (1935:

479) "the slender ocellar pedicels uniting the facial

ocelli with the brain are commonly called the ocellar nerves." Cajal (1918), however, has shown that

the primary ocellar center is located in an enlarged

outer end of what has been called the "ocellar

nerve." Therefore, Nervi Ocellares are those groups

of "retinal fibers" that terminate in the distal ends

of the so-called ocellar stalks.

The available literature on ocellar nerves is very

meager. However, a few authors have described the

"ocellar pedicel" corresponding to the Lobus Opticus

in many insects (Maki 1936; Ehnbom 1948).

In the honey bee the ocellar nerves have their

centers in the Ganglion Proto-Hyperoesophagale,

which is the most anterior structure of the composite

Ganglion Hyperoesophagale as in other studied

groups of insects. Since the gross anatomy and

histology of the Nervi Optici and the Nervi Ocellares

have been studied extensively in the honey bee, there

is no need for a detailed description at this time. The

reader is referred to the works of Kenyon (18%),

Jonescu (1909), Snodgrass (1956), Jawlowski

(1958), and Satija (1958).

Ganglion Deuto-Hyperoesophagale

Nervus Antennalis (N. Anten.) (Figures 2, 4, 10)

The Nervus Antennalis innervates the extrinsic and

intrinsic antennal muscles and the various sense

organs found in the antenna. Newton (1879) was

the first to observe a fine branch arising from the

antennal nerve and innervating the antennal muscles within the head of the cockroach. Crauss (1884)

reported that this nerve in Corydalus divides into two

branches, the cephalic entering the antenna and the

caudal innervating the antennal muscles in the head.

However, he did not mention which nerve innervates the intrinsic muscles of the antenna. He also

stated that the "antennal nerve" gives rise to a

small branch which bifurcates and innervates the

area near the eyes.

Viallanes (1887a) found a "branch" leaving the

"antennal nerve" in Vespa crabro which he named

"nerf antennaire accelsoire" and correlated it with

that described by Newton for Blatta, although he

did not trace it to its termination in the muscles. In

the honey bee worker, Kenyon (1896) stated that

a nerve innervating the extrinsic antennal muscles

arises from the lower surface of the "antennal

nerve." He named this nerve the "antenno motor

internus" and considered it as a part of the "tritocerebron." He also gave the name "antenno motor

externus" to the main nerve, although he did not

trace it to its termination.

Janet (1905) was the first author to study the

topography of the Nervus Antennalis. He stated that

in Lasius niger it gives rise to five branch nerves:

(1) a small motor nerve dividing into four branches,

one for each of the four intrinsic muscles of the

antenna; (2) a small motor nerve innervating the

extrinsic muscles of the antenna; (3 and 4) two big

nerves entering the antenna; and (5) a "chordotonal

nerve" terminating in the integument. Jonescu

(1909) found the same nerves in the honey bee except for the "chordotonal nerve." Swaine (1920)

stated that the Nervus Antennalis appears to be

united at its base with the "fronto labral" nerve.

According to Maki (1936) the "common root of
32 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the antennal nerves" gives rise to three nerves, two

(Ad and Al) to the extrinsic, and one (Af) to the

intrinsic muscles of the antenna. He also stated that

the common root divided at the scape into two main

branches (Ai and Aii). Chaudonneret (1950-1951)

described the topography of the Nervus Antennalis

in great detail. His drawings, however, do not show

innervation or relation to other tissues found in the

head. He used a combination of letters and numbers

to designate "nerves" (t42, t47, Naa, etc.). Buckup

(1959) in his study of the mallophagan Myrsidea

showed that the antennal nerve gives rise to three

"nerves" before entering the scape. Two of these

"nerves" (NAntl and NAnt2) innervate what he

called the "Muse, scape anterior" and the "Muse,

scape posterior." The third one (NAnt3) innervates

the "Muse, pedicelli anterior" and the "Muse, pedicelli posterior."

From the above review, it appears that no one has

attempted to name the branches or subbranches of

the main nerves. Maki, Chaudonneret, and Buckup,

however, used letters and combinations of letters and

numbers for most of the nervules innervating the

muscles.

In the honey bee the Nervus Antennalis appears

to be an extension of a small lobe, the Lobus Antennalis (Lob. Anten.), located anteriorly on the

lower part of the Ganglion Hyperoesophagale and

surrounds the top part of the pharynx (Figure 2).

This lobe was called the olfactory lobe by Viallanes

(1887a), whose lead was followed by others. Actually, the roots of the Nervus Antennalis come in part

from the Ganglion Deuto-Hyperoesophagale (Gang.

Deut-Hyperoesoph.), and in part from the Lobus

Antennalis (Jonescu 1909 and Jawlowski 1958).

The Nervus Antennalis extends forward and passes

through the neural mass of the Lobus Antennalis.

In the worker and queen, after leaving the lobe, this

nerve angles anteriorly and cephalad until it enters

the antennal scape; however, in the drone it runs

anteriorly only to the base of the scape. This extrinsic part of the Nervus Antennalis is longest in the

worker; in the queen it is about two thirds as long,

and in the drone about one fifth as long as in the

worker. The extrinsic part of the Nervus Antennalis

in all castes of Vespula maculata is similar to that

found in the drone honey bee, but in Lasius

(workers) it is similar to that in the worker honey

bee.

In the worker and queen a short motor branch,

the Nervus Antennalis Lateralis I (N. Anten. Lat. I),

emerges from the cephalad side of the Lobus Antennalis and runs downward toward the extrinsic

muscles of the antennae. It subdivides into four

small branches, each of which innervates one of the

extrinsic muscles of the antenna. These branches,

designated as nervules, are named the Nervulus

musculi Tentorio-scapualis I (Nl. m. Tent-scap. I),

Nervulus musculi Tentorio-scapualis II (Nl. m.

Tent-scap. II), the Nervulus musculus Tentorioscapualis III (Nl. m. Tent-scap. Ill), and the Nervulus musculi Tentorio-scapualis IV (Nl. m. Tentscap. IV). In the drone, the Nervus Antennalis Lateralis I appears to emerge from the base instead of

the distal tip of the Lobus Antennalis. Also, the degree of bundling of the nervules of the extrinsic

antennal muscles differs among individual drones.

In some cases, each of two sublateral nerves divides

into two nervules, and in other cases there are four

nervules, each serving one extrinsic antennal muscle

and leaving the Lobus Antennalis without bundling

into sublateral nerves. This last situation is similar

to that found in Vespula maculata.

The Nervus Antennalis Lateralis I in the honey

bee appears to be the "accessory nerve of the antenna" described for Caloptenus and Oedaleus

(Acrididae) by Viallanes (1887b). In Lasius it

resembles that in the worker honey bee, but in

Vespula maculata it resembles that in the drone

since it has separate nervules for each muscle.

In drone honey bees that have two sublateral

nerves for the extrinsic antennal muscles, it was

found that one nerve divides into two nervules that

go to the m. tentorio-scapualis I and the m. tentorioscapualis II (dorsal muscles acting as levators). The

other nerve divides into two nervules that innervate

the m. tentorio-scapualis III and the m. tentorioscapualis IV (ventral muscles acting as depressors).

This situation is found also in Chauliodes which,

however, has only one "levator" muscle.

After leaving the Lobus Antennalis, the Nervus

Antennalis gives off a sensory branch that extends

dorsally and anteriorly until it reaches the integument above the area of articulation of the antenna.

There it gives rise to several small branches innervating the integument of the frontal area. In the

area of branching, it is attached to a sense organ

located at the outer end of the upper area of the
NUMBER 99 33

articulating membrane between the scape and the

frons. This nerve is named Nervus Antennalis Tegumentualis. It may be the same as a nerve in Corydalus described by Crauss (p. 180) as a "small

branch which divides in small branches and innervates the area near the eye." This "chordotonal

nerve" described in Lasius by Janet (1905) is probably another homolog even though Jonescu (1909)

was not able to see it in the honey bee.

A short distance from the divergence of the Nervus

Antennalis Tegumentualis, the Nervus Antennalis

gives off from its dorsal side another branch, the

Nervus Antennalis Lateralis II (N. Ant. Lat. II).

This branch extends dorsally, lying against the

Nervus Antennalis until it enters the scape, and

starts diverging to the outer side of the antenna

where it divides into two branches. The first branch,

the Nervulus Scapo-tegumentualis (Nl. Scap-tegum.), is small and sensory, directed dorsally and

laterally and attached to a sense organ located on

the outer dorsolateral corner of the scapal base.

Janet named the homolog of this sense organ in

Lasius the "sensitif tactile ganglia." The second

branch, the Nervulus musculi Scapo-pedicularis I

(Nl. m. Scap-pedic. I), is a motor nervulus, and

extends dorsally and medially in the scape until it

meets with and innervates the m. scapo-pedicularis I.

From the ventral side of the Nervus Antennalis,

a short distance anterior to the point of divergence

of N. Ant. Lat. II, the Nervus Antennalis Lateralis

III (N. Ant. Lat. HI) separates. It extends ventrally

and parallels the main nerve until it reaches the

scape, where it bends toward the inner lateral side

of the scape. It divides into two branches, the first

being sensory and connecting with a sense organ

located on the lateral ventral corner of the scapal

base, and the second, the Nervulus musculi Scapopedicularis II (Nl. m. Scap-pedic. II), extending

ventrally and laterally until it innervates the m.

scapo-pedicularis II. In Lasius, however, the homologs of the intrinsic antennal muscles are innervated

by two subbranches of a nerve that arises ventrally

from the Nervus Antennalis. Maki (1936) and

Buckup (1959) found the same situation to occur

in Chauliodes and Myrsidea cornicis, respectively.

In a few drones the intrinsic muscles of the antenna

are innervated by subbranches of a nerve arising

ventrally. Such drones had only one, relatively large,

sense organ in the dorsolateral corner of the scapal

base, as in Lasius.

Prior to entering the scape, the Nervus Antennalis

divides into two main sensory nerves extending to the

tip of the antenna. These nerves are the Nervus Antennalis Lateralis IV (N. Ant. Lat. IV) and the

Nervus Antennalis Lateralis V (N. Ant. Lat. V).

Each of these sensory nerves, just before entering

the pedicel, gives rise to a short sensory branch

terminating in the so-called Johnson organ.

The topography of the Nervus Antennalis in the

honey bee, especially the drone, is similar to that

in Vespula maculata. It has the same number of

branches and nervules arising from homologous locations and innervating homologous muscles.

Ganglion Trito-hyperoesophagale

Nervus Ganglii Pharyngealis (N. Gang. Phar.) (Figures 1, 3, 10)

Janet (1905) proposed the name "connective of the

frontal ganglion" for this nerve. Hammar (1908)

named it the "arched nerve." Jonescu, one year

later, named it the "frontal ganglionic nerve." This

name has been universally accepted and applies to

the inner nerve of the Nervus Pharyngeo-labrualis

(N. Phar-labr.) which is connected to the "frontal

ganglion."

In the honey bee this nerve leaves the Ganglion

Hyperoesophagale in the area behind the Lobus

Antennalis, adjacent to the pharynx. However, its

center is in the Ganglion Trito-hyperoesophagale.

In other insects this nerve and the Nervus Labrualis

are bundled together for a short distance forming the

so-called "fronto-labral" nerve. This situation is demonstrated clearly in Vespula maculata. The Nervus

Ganglii Pharyngealis runs cephalad against the walls

of the pharynx and curves anteriorly, until it meets

the Ganglion Pharyngeale (Gang. Phar.), which is

located medially between the clypeus and frons.

This ganglion has been known as the "frontal ganglion" in the works of Leydig (1864), Janet (1905),

and others. The term is misleading, although some

authors think it is useful in designating the structure

as a landmark separating the preoral clypeus from

the oral frons. This is questionable, as suggested by

the work of Pesson (1944) on coccids and Dupor:e

(1956) on adult monarch butterflies, since both
34 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

these investigations found this ganglion to be much

more posterior than in more generalized insects. Actually, its nerves innervate muscles belonging to the

pharynx and the anterior cibarial wall rather than

the frons. Snodgrass (1947) stated that the "frontal

ganglion" always lies near the distal end of the

pharynx behind the mouth. For the above reasons,

the term Ganglion Pharyngeale appears to be a

logical designation.

The Nervus Ganglii Pharyngealis gives rise dorsally to a small motor branch immediately after it

curves toward the anterior wall of the pharynx. This

branch, designated as the Nervule musculi Frontisuspensorialis (Nl. m. Fron-susp.), innervates the

m. fronti-suspensorialis. In the same area, but from

its ventral side, the Nervus Ganglii Pharyngealis

gives off two small nervules. One angles anterolaterally until it reaches and innervates the m. tentoriosuspensorialis. This nervule is named the Nervulus

musculi Tentorio-suspensorialis (Nl. m. Tent-susp.).

The other nervule extends posteriorly and innervates

the m. fronti-labrualis and is consequently named the

Nervulus musculi Fronti-labrualis (Nl. m. Fronlabr.). N. Gang. Phar. also gives off another motor

branch just before entering the Ganglion Pharyngeale. This branch, named the Nervus musculorum

Fronti-pharyngealium (N. m. Fron-phar.), extends

dorsally and subdivides into two nervules innervating the m. fronti-pharyngealis I and the m. frontipharyngealis II. Consequently, they are named the

Nervulus musculi Fronti-pharyngealis (Nl. m. Fronphar. I) and the Nervulus musculi Fronti-pharyngealis II (Nl. m. Fron-phar. II), respectively. Although the drone has three muscles belonging to

the musculi fronti-pharyngeales group, no third

nervule has been found for the third muscle. This

may explain why this muscle appears to be degenerating in the drone.

From the Ganglion Pharyngeale, two main nerves

leave in opposite directions. One extends anteriorly

and medially over the cibarium and the other extends posteriorly and medially over the pharynx.

The first one is named the Nervus Ganglii Pharyngealis Anterior (N. Gang. Phar. Ant.). It gives rise

to a variable number of small lateral branches innervating the different bundles of the m. clypeocibarioparietalis. Each nervule is named according

to the bundle it innervates. For convenience, they

are given a collective term, Nervuli musculorum

clypeo-cibarioparietalium (Nli. m. Clyp-cibar.). The

most anterior part of the Nervus Ganglii Pharyngealis Anterior (the part that follows the nervule

going to the most ventral bundle of the m. clypeoepipharyngealis) innervates the m. clypeo-epipharyngealis and is named, accordingly, the Nervulus

musculi Clypeo-epipharyngealis (Nl. m. Clyp-epiphar.). Since the Nervus Ganglii Pharyngealis Anterior has not been studied in detail in pterygote

insects, a sound homology for it cannot be reached.

In Vespula maculata, however, I found that it

divides into a pair of nerves, each innervating the

muscles lateral to it. Since in Vespula each member

of the pair innervates the series of muscles on its

own side of the head, it appears that in the honey

bee the main nerve is bundled. Surprisingly, it is

not involved in the innervation of the m. intrasuspensorialis dorsualis.

The second nerve is named the Nervus Ganglii

Pharyngealis Posterior (N. Gang. Phar. Post.). It

extends mediodorsally and posteriorly over the pharynx. Before passing under the Ganglion Hyperoesophagale, it gives rise to a lateral branch extending

ventrally, paralleling the hypopharyngeal suspensorium and innervating the m. oriscuto-suspensorialis.

Accordingly, this branch is named the Nervulus

musculi Oriscuto-suspensorialis (Nl. m. Orisc-susp.).

It passes under the Ganglion Hyperoesophagale and

the most anterior part of the so-called aorta. Before

passing between the points of movable attachment

of the m. cranio-pharyngealis, it gives off laterally

two small nervules, both innervating the m. craniopharyngealis. Consequently, they are given the name

Nervuli musculi Cranio-pharyngealis (Nl. m. Cranphar.). The Nervus Ganglii Pharyngealis Posterior

continues posteriorly until it reaches the level of the

"dorsal paracardial commissure" where it divides

into two branches. Each member of the pair curves

around ventrally and posteriorly until it is on the

lateral side of the oesophagus, where it continues

without subbranching until it reaches the crop. At

that point each branch divides and subdivides into

many nervules that innervate the walls of the crop.

It was noted that before dividing into a pair, the

Nervus Ganglii Pharyngealis Posterior gives off laterally numerous nervules, the Nervuli musculi Circulopharyngealis (Nl. m. Circulphar.) which innervate the musculus circulopharyngealis. This nerve

has not yet been described in detail in other insects.
NUMBER 9 9 35

In Vespula the homologous nerve follows the same

topographic pattern.

Nervus Labrualis (N. Labr.) (Figures 1, 3)

The name "clypeo-labral" was proposed for this

nerve by Crauss (1884). He wrote that it arises from

each "crus" and gives rise to three small branches

innervating the clypeus, while the main nerve extends cephalad into the labrum. Hammar (1908)

disagreed with Crauss about its origin and indicated

that it arises from the tritocerebrum. Janet (1905)

was the first to associate it with muscles and sense

organs found on the margins (les cotes) of the

pharynx. He also stated that it innervates the various structures belonging to the "post cerebral segment" such as the labrum and the muscles of the

upper parts of the pharynx. Consequently, he designated it as the "proto-cerebral nerve."

Jonescu (1909) considered it to be situated behind

the "deuto-cerebrum," but did not indicate from

which segment it arises. Instead, he stated that it

should be included within the "suboesophageal

ganglion," especially since it shows a close connection

with the latter.

Holste (1910) found that the labral nerve gives

rise to a small branch passing transversely over the

"oesophagus" to join with the "prefrontal plexus" of

the sympathetic nervous system. He found the main

nerve splitting into two branches, the "upper" innervating the clypeus and the "lower" innervating

the labrum ("musculus dilator pharyngis primus"

and "musculus compressor pharyngis"), respectively.

Peterson's (1912) and Swaine's (1920) studies on

Protoparce and Sthenopus (Lepidoptera), respectively, indicate that the topography of the "labral

nerve" is similar to that described by Holste for

Dytiscus. Maki (1936) found almost the same pattern to exist in the neuropteroid, Chauliodes.

Chaudonneret (1950-1951) illustrated and described

in great detail the topography of the "clypeo-labral"

nerve in Thermobia. He found the plan to be very

complicated and quite different from those described

for Pterygota. As might be expected, his findings on

the topography of this nerve are similar to those of

Denis (1928) for Anurida (Collembola).

In the honey bee this nerve is separate from and

directly behind the Nervus Ganglii Pharyngealis. In

other insects, however, such as Corydalus, Chauliodes,

Lasius, and Vespula, both nerves are joined for a

short distance.

The Nervus Labrualis extends anteriorly and ventrally, parallel to the m. tentorio-oriscutarius. About

midway and before crossing over the hypopharyngeal suspensorium, it gives rise to a sensory branch

directed backward and connecting with a sense

organ on the oral plate. This branch is called the

Nervulus Tegumenti Labrualis I (Nl. Tegum. Labr.

I). Mclndoo (1914a) considered this sense organ

to be for taste. Unfortunately, no complete histological or physiological study has been made to determine

its function. The Nervus Labrualis then passes over

the hypopharyngeal suspensorium at the level of the

fixed attachment of the m. tentorio-suspensorialis. In

the above area, it gives rise to a sensory branch that

extends anteriorly until it reaches and innervates the

cranial wall of the clypeus. This branch is named

the Nervulus Tegumenti Labrualis II (Nl. Tegum.

Labr. II). A short distance ventral to the last

branching, the Nervus Labrualis gives rise to a

nervule that is directed medially toward the midline

of the anterior cibarial wall. Since this nervule innervates the m. intrasuspensorialis dorsualis, it is

named the Nervulus musculi Intrasuspensorialis

Dorsualis (Nl. m. Intrasusp. Dors.).

The Nervus Labrualis then parallels the suspensorium and at the level of the basal part of the

oral plate it gives rise to a branch directed horizontally and posteriorly. This branch, designated as the

Nervulus Tegumenti Labrualis III (Nl. Tegum.

Labr. Ill), enters the epipharynx and connects with

the sense organ located laterally on the inner wall of

the epipharynx. The remaining portion of the Nervus

Labrualis extends ventrally and enters the labrum,

innervating its anterior and posterior walls with several subbranches. This terminal portion of the main

nerve is called the Nervulus Tegumenti Labrualis II

(Nl. Tegum. Labr. II) indicating that it innervates

the labrum proper.

In Vespula maculata the topography of the

Nervus Labrualis is similar to that in the honey

bee, thus indicating that criteria of homology can

be established between distantly related genera. Unfortunately, no complete studies of this nerve have

been made. Fragmentary works on Dytiscus (Coleoptera), Protoparce, Sthenopis (Lepidoptera), and

Chauliodes (Neuroptera), however, indicate that the

Nervus Labrualis has quite a different topographic
36 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

pattern in these insects, largely because they have

two additional pairs of labral muscles. In these insects the Nervus Labrualis is connected to the

Nervus Ganglii Pharyngealis Anterior.

Nervus Corpoallatialis (N. Corpoallat.) (Figures 3,

8)

In the honey bee this nerve leaves from the lower

posterior end of the Ganglion Hyperoesophagale,

just above the level of the oesophagus. It extends

backward for a short distance and is attached medially to the anterior side of the corpus allatum.

Hanan (1955), in a detailed study of the relations

between the corpora cardiaca and the corpora

allata in the honey bee, discovered the ring of

"neural and aortal tissue" surrounding the oesophagus and connecting each corpus cardiacum with its

homolog on the other side by what he called the

"dorsal paracardial commissure" and the "ventral

paracardial commissure." He also indicated that

each corpus allatum connected to the corpus cardiacum by a very short, almost indistinguishable, connective. My findings disagree with those of Hanan

in the following particulars: (1) A distinct and

complete ring, probably of neural tissue, surrounds

the oesophagus and connects to the corpora cardiaca

with a membranous tissue. (2) A separate connective

of neural tissue connects the two corpora allata ventrally. (3) Another connective of neural tissue

ventrally connects the ventral parts of the corpora

cardiaca (Figure 8). According to Hanan, the connectives he discovered had not been described in

other insects. The same holds true for the connectives I found between the corpora cardiaca and

between the corpora allata. These connectives are

named the Commissura Corporum Cardiacorum

(Com. Corp. Card.) and Commissura Corporum

Allatorum (Com. Corp. Allot.), respectively.

Commissura Gangliorum Trito-Hyperoesophagalium

Table 5 shows the different names that have been

applied to this commissure. It is distinguishable in

Corydalus, Melanoplus, Dytiscus, Protoparce, and

others, but it is indistinguishable in Lasius and Apis.

According to Snodgrass (1956), it is embedded in

the "suboesophagial" ganglion in the adult honey

bee, although free in the larva (Nelson 1924).

Nervulus musculi Tentorio-oriscutarius (Nl. m.

Tent.-orisc.) (Figure 3)

The nerve arises from the median line on the dorsal

side of the Ganglion Hypoesophagale of the honey

bee, but, according to the histological studies of

Jonescu (1909), its group of motor cells is located

on the side of the labral ganglion. Consequently, it

is described under the Ganglion Hyperoesophagale

rather than under the Ganglion Hypoesophagale.

Jonescu also stated that this "nerve" has a pair of

roots, thus indicating a type of bundling resulting

from the fusion of the two innervated muscles.

The Nervulus musculi Tentorio-oriscutarius extends ventrally and anteriorly adjacent to the musculus tentorio-oriscutarius which it innervates. A

corresponding nervule is in Lasius and two in Vespula maculata.

LOCATION AND TOPOGRAPHY OF THE Ganglion Hypoesophagale

Contradictory opinions exist concerning the placement of this neural mass and whether it is a part

of the so-called brain. However, it is now believed to

be a part of the ventral nerve cord. Even from the

histological aspects, only limited investigat'ons have

been carried out on this ganglionic mass or its main

nerves. The more important works dealing entirely

or in part with this nerve mass are those of Crauss

(1884), Bauer (1904), Hammar (1908), Holste*

(1910), Swaine (1920), Denis* (1928), Maki*

(1936), Marquardt (1939), and Chaudonneret*

(1950-1951). (Asterisk indicates a detailed study of

the "suboesophagial ganglion.")

In the honey bee the main nerves arising from

the Ganglion Hypoesophagale are the Nervus Mandibularis, the Nervus Maxillaris, the Nervus Labialis,

the Nervus Postoccipitalis, and the Nervus Posterior.

In the honey bee this ganglion appears to be

connected directly to Ganglion Trito-hyperoesophagale because of the shortness of the Connectivi Gangliorum Hyper-hypoesophagalium. It is located directly beneath the stomodaeum and above the level

of the point of fixed attachment of the extrinsic

muscles of the antenna. The Ganglion Hypoesophagale has almost the same location in the three castes.

The connectives are also short in Vespula maculata

and Lasius niger.
NUMBER 99 37

Nervus Mandibularis (N. Mand.) (Figures 2, 4)

Crauss probably was the first morphologist to study

the "mandibular nerve" and its branches in Corydalus. His study was fragmentary, however, and

did not deal with innervation. Hammar found the

mandibular nerve in Corydalus to have three

branches: branch 1 bending caudad and innervating

the "large mandibular muscle" (probably the homolog of the musculus cranio-intramandibularis),

branch 2 connecting to "ganglion g" (a part of what

he called the sympathetic nervous system), and

branch 3 entering the mandible and aiso innervating

some muscles (not identified). Holste likewise found

that the "mandibular nerve" in Dytiscus divides into

three branches: branch "nfmd" innervating the

"musculus flexor mandibularis" (cranio-intramandibularis), the second branch innervating both integument and the "extensor muscle of the mandible"

(cranio-extramandibularis), and the third branch

entering the mandible. His investigation showed that

the "mandibular nerve" does not give rise to any

branches connecting to the "sympathetic nervous

system," thus differing from the situation in Corydalus. According to Swaine, the general topography

of the mandibular nerve in Sthenopis is almost the

same as it is in Dytiscus, except that the "mandibular nerve" gives rise to a small branch that fuses

with its homolog from the opposite side and continues

cephalad as a double nerve serving the hypopharynx.

Owing to a "tentorial adductor of the mandible" in

Chauliodes, Maki found the mandibular nerve to

have four branches that "enter the lateral portion

of the clypeus." Chaudonneret found that the topography of the "mandibular nerve" in Thermobia

differed between specimens. He stated also that such

a difference could exist even between the two mandibles of the same specimen. In general, however,

he found that the mandibular segment is innervated

by four "main nerves" and their branches. The

topography of these nerves (thysanuroid-type mandible) differs greatly from those of other groups

studied (orthopteroid-type mandible). Consequently,

there is no need to review it in detail here. It is

notable, however, that Chaudonneret was probably

the first to study the innervation of the mandibular

gland.

The N. Mand. was described by Rehm (1939) for

the worker honey bee. Unfortunately, his description

contains many errors as evidenced in his Figure 1

on page 92.

In the worker honey bee the Nervus Mandibularis

is the most anterior nerve attached to the Ganglion

Hypoesophagale. It passes anteriorly and ventrally

under the pharynx and laterally to the fixed point

of attachment of the intrinsic antennal muscles, the

pretentorium, the m. gena-cardinalis, and the m.

tentorio-stipitalis I. It then angles laterally and anteriorly toward the points of fixed attachment of

the m. tentorio-cardinalis and the m. tentorio-stipitalis II, curves under them, and divides into three

branches.

The first, the Nervus Mandibularis Lateralis I,

extends laterally over the m. tentorio-matidibularis

and posteriorly under the mandibular gland. After

passing under half of this gland, it gives rise to a

small branch, the Nervulus Glanduli Mandibularis,

(Nl. Gland-Mand.) which innervates it. After passing

under the mandibular gland, the Nervus Mandibularis Lateralis I forks into two subbranches. The

branches of this fork extend laterally and upward

until they reach and innervate the m. cranio-extramandibularis. This part of the Nervus Mandibularis

Lateralis I is named the Nervulus musculi Cranioextramandibularis (Nl. m. Cran-extramand.).

The second branch, the Nervus Mandibularis Lateralis II (N. Mand. Lat. II), is very short and almost indistinguishable. It connects directly to the

lateral corner of a diamond-shaped neural mass lying

against the m. tentorio-mandibularis. The ventral

corner is extended as a long threadlike branch connecting with the Nervus Mandibularis before the

latter enters the mandible. The other lateral corner

of the neural mass gives rise to a very thin branch,

the Nervulus musculi Cranio-intramandibularis II

(Nl. m. Cran-intramand. II), which curves upward and passes posteriorly between the two nodes

of the cranial articulation of the cardo. It passes

posteriorly and dorsally over the m. gena-cardinalis,

where it parallels the inner side of the long tendonlike apodemal growth on which the m. cranio-intramandibularis II has its point of movable attachment.

Eventually it reaches this muscle and innervates it.

The third and last branch extends dorsally and

passes between the two nodes of the cranial articulation of the cardo on the outer side of the Nervus

musculi Cranio-intramandibularis II. It continues

dorsally, passing across the m. gena-cardinalis until
38 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

it reaches and innervates branch I of the m. craniointramandibularis. Accordingly, it is named the

Nervulus musculi Cranio-intramandibularis I (Nl.

m. Cran-intramand. I).

After giving off the aforementioned three lateral

nerves, the Nervus Mandibularis curves downward

and passes under the m. tentorio-mandibularis. In

this area it gives rise to a sensory nervule that reaches

the inner articulating membrane of the mandible,

and then extends cephalad, parallel to the inner side

of the m. tentorio-mandibularis. After passing under

the anterior portion of the mandibular gland, the

nervule enters the mandible and innervates its integumental walls. Accordingly, this nervule is named

Nervulus Tegumenti Mandibularis (Nl. Tegum.

Mand.).

Establishing homology for the Nervus Mandibularis among insects is rather difficult because of the

fragmentary work that has been done. For example,

only Chaudonneret (1950-1951) has even mentioned

the innervation of the mandibular gland (in Thermobia). However, by comparing the topography of

the Nervus Mandibularis of the honey bee with

other groups studied, a general plan may be reached.

All authors agree that it divides into several

branches, each of which is responsible for innervating a single mandibular muscle, or the mandible

proper. Accordingly, the branches may be considered

as homologs whenever they innervate homologous

muscles.

In the drone honey bee the topography of the

Nervus Mandibularis is similar to that of the worker

and queen (described above), with minor differences

resulting from a reduction of the mandibular muscles. For instance, since branch II of the m. craniointramandibularis is absent, there is no homolog of

the nervule innervating it. Accordingly, the "diamond-shaped nerve mass" (found in the worker) is

rather triangular in the drone. Also, the male appears to have no Nervulus Glanduli Mandibularis,

because its mandibular gland is greatly reduced in

Nervus Maxillaris (N. Max.) (Figures 3, 4, 5)

According to Crauss, the "maxillary nerve" divides

into four branches: branch "a" entering the maxillary palpus, branch "b" innervating the integument,

and branches "c" and "d" innervating the extrinsic

and intrinsic muscles of the maxilla, respectively.

Hammar (1908) and Swaine (1920) made only

incomplete statements concerning the topography

of this nerve. According to Holste (1910), all the

branches innervating the maxillary muscles arise

from the maxillary nerve directly after it emerges

from the "suboesophageal ganglion." He also stated

that this nerve gives rise to two lateral branches

other than the main branch which enters the maxilla. Holste did not describe the movable and fixed

attachments of the muscles. Instead he described the

muscles according to their function, thus making it

impossible to homologize them with those of other

groups of insects. For this reason I am not reviewing his study in detail. However, he found that one

of the maxillary branches attached to the nerve of

what he called "dorsal-blood-vessel ganglion." Holste

also noted that the "flexor maxillae anterior" has

double innervation.

Maki (1936), however, studied the topography

of the maxillary nerve in great detail. He found

that it divides into three main branches. One branch

(Mai) divides and subdivides into four nerves, three

of which innervate the "adductors of the cardo" (m.

pretentorio-stipitalis I) and the "levator of the

maxillary palpus" (m. stipiti-maxillopalpualis I),

while the fourth nerve subdivides and innervates

the "flexor of the stipes" (m. pretentorio-stipitalis

II). The second main branch (Maii) divides and

subdivides to innervate the "stipital flexor of the

lacinia" (m. stipiti-laciniaris), the "stipital flexor

of the galea" (m. stipiti-galearis), and the "levator

of the maxillary palpus" (m. stipiti-maxillopalpualis

II). The third main branch (Maiii) gives rise to

three subbranches; (Maiiil) serving the lacinial wall,

(Maiiig) the galial wall, and (Maiiip) the maxillary

palpus. He further states that the "levator of the

maxillary palpus" (m. stipiti-maxillopalpualis I) is

the only maxillary muscle to receive double innervation from "the maxillary nerve," in Thermobia. This

muscle (m. stipiti-galearis) he referred to as the

"muscle flexor de la galea maxillaire." He also

found that a mandibular nerve and four maxillary

nerves enter what he called the "corps jugul."8

In the honey bee Nervus Maxillaris is located be8

 This gland was first described by Chaudonneret (1946

and 1950-1951) in Thermobia. According to him it is a

neuroendocrine gland, which is simply a corpus allatum still

preserving the embryological condition. It results from the

fusion and the functional modification of the maxillary and

mandibular ganglia of the sympathetic nervous system.
NUMBER 9 9 39

hind the Nervus Mandibularis. It extends ventrally

and medially under the stomodaeum and laterally

over the points of fixed attachment of the extrinsic

muscles of the antenna and the pretenorium. Just

behind this point it gives rise to a branch designated

as the Nervulus musculi Gena-cardinalis (Nl. m.

Gen-Card.). This nervule angles away from the

main nerve in an anterior and ventral direction and

passes adjacently by the inner side of the m. tentorioprementualis, the m. tentorio-stipitalis I, tn. tentoriocardinalis, and the m. tentorio-stipitalis II. After

passing over the last-named muscle, it curves, turns

under the muscle, twists, and passes dorsally over

its outer side. The nervule then extends between

the nodes of the cranial articulation of the cardo

where it turns posteriorly over the m. gena-cardinalis

and innervates it medially. This nervule connects

with a loose aggregation of neurons before it contacts

the m. gena-cardinalis.

After giving off the aforementioned nervule, the

Nervus Maxillaris passes medially and laterally over

the m. tentorio-prementualis and gives off a branch

termed the Nervus Maxillaris Lateralis I (N. Max.

Lat. I). This branch extends anteriorly and laterally

over the m. tentorio-stipitalis, where it divides into

three nervules: the Nervulus musculi Tentorio-stipitalis I (Nl. m. Tent-stip. I), the Nervulus musculi

Tentorio-cardinalis (Nl. m. Tent-card.), and the

Nervulus musculi Tentorio-stipitalis II (Nl. m. Tentstip. II). The first-mentioned nervule twists dorsally

and anteriorly to contact and innervate the m. tentorio-stipitalis I. The second one extends anteriorly

and innervates the m. tentorio-cardinalis. The third

runs cephalad, parallel to the main nerve, until it

reaches and innervates the m. tentorio-stipitalis II.

The Nervus Maxillaris continues to extend cephalad and mediad, passing laterally over the m. tentorio-stipitalis I and the m. tentorio-stipitalis II,

where it gives rise to the Nervus Maxillaris Lateralis

II (N. Max. Lat. II) and to a sensory branch, the

Nervulus Tegumenti Galearis (Nl. Tegum. Gal.).

The first of these two lateral nerves is directed posteriorly with respect to the second one. After separating from the main nerve, it gives rise to two

small "ganglia" connected directly to it. The Nervus

Maxillaris Lateralis II then passes medially over the

m. stipiti-laciniaris and divides into three branches.

The first, the Nervus Maxillaris Sublateralis I (N.

Max. Sublat. I), diverges upward toward the m.

stipiti-laciniaris, where it forks into two nervules.

One of these enters the m. stipiti-laciniaris and is

consequently named the Nervulus musculi Stipitilaciniaris (Nl. m. Stip-lacin.). The second is sensory,

passing horizontally and posteriorly under the m.

stipiti-laciniaris and over the m. stipiti-maxillopalpualis until it reaches the corner of the articulation

between the cardo and the stipes. It turns under

the m. stipiti-maxillopalpualis and innervates the

basal part of the stipital integument. Accordingly,

it is named the Nervulus Tegumenti Stipitalis I

(Nl. Tegum. Stipiti I). The second branch, the

Nervus Maxillaris Sublateralis II (N. Max. Sublat.

II), turns dorsally toward the m. stipiti-galearis,

where it divides into two nervules. The first, the

Nervulus musculi Stipiti-galearis (Nl. m. Stip-gal.)

enters the m. stipiti-galearis and the lacinial sclerite,

where it diverges toward the distal portion of the

stipes and innervates it.

The third branch of the main nerve, the Nervus

Maxillaris Sublateralis III (N. Max. Sublat. Ill),

extends ventrally, parallel to the main nerve for a

short distance and then divides into two nervules.

The first one passes horizontally over the m. stipitigalearis and then turns under it, passing over the

m. stipiti-maxillopalpualis and innervating it. Consequently, this nervule is named the Nervulus musculi Stipiti-maxillopalpualis (Nl. m. Stip-maxpalp.).

The other nervule extends ventrally and passes over

the tendonlike apodeme on which the m. stipitigalearis is attached and enters the maxillary palpus.

This nervule is named the Nervulus Maxillopalpualis

(Nl. Max palp.).

The Nervulus Tegumenti galearis extends submedially and ventrally between the lacinia and stipes.

It enters the galea, passes between its walls, and

gives rise to several nervules innervating it.

The nervules innervating the extrinsic muscles in

Corydalus (Crauss 1884), and Chauliodes (Maki

1936) are bundled together as in the honey bee.

However, the honey bee differs in having the Nervulus Maxillopalpualis bundled with the nerve innervating m. stipiti-galearis and m. stipiti-maxillopalpualis, rather than with the Nl. Tegum. Gal.

(which innervates the galea) as in Corydalus or

Chauliodes. In Thermobia, the Nervus Mandibularis

connects with the Nervus Maxillaris through a

"jugal body," whereas Apis, Vespula, Chauliodes,

and Corydalus have no such connection.
40 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Nervus Labialis (N. Lab.) (Figures 3, 6, 7)

The investigations of Crauss (1884) and Hammar

(1908) on the "labial nerve" of Corydalus were

incomplete. Holste (1910) also failed to study the

topography of this nerve in detail; he merely mentioned that the "labial nerve" gives rise to two

nerves, one innervating the gula, mentum, and various labial muscles and the other passing by means

of two branches into the "palparium" and the labial

palpus. According to Maki (1936), the labial nerve

in Chauliodes is divided into two main branches,

the first (Lba) of which divides into two subbranches (Lbal) and (Lba2) that innervate the

"median retractor of the mentum" (m. postoccipitiprementualis) and the "median retractor of the

prementum" (m. tentorio-prementualis), respectively. The second main branch gives off four

branches: the first three innervating, respectively,

the "lateral retractor of the mentum" (m. tentorioparaglossaris), the "dorsal dilator of the common

salivary duct" (m. dorsopremento-salivarius), and

the labial palpus muscles, while the fourth innervates the walls of the ligula.

Chaudonneret (1950-1951) found great variability in the topography of the labial nerve of Thermobia between individuals and even between the right

and left half of a labium of one individual. Consequently, he described a "median" type and then

discussed the great variation in the specimens

studied. He found the following muscles to receive

double innervation: "cranial-fulcral," "levator of external labial lobe," "cranial flexors of the internal

labial lobe," and "cranial flexors of the external

labial lobe." By contrast, he found that the "anterior depressor of the labium," the "ventral dilator of

the labial salivary orifice," and the "fulcro-postmental muscle" receive no innervation as a consequence

of their degenerate condition.

In the honey bee the labial nerve arises directly

behind the Nervus Maxillaris. It is directed ventrally

toward the labium. While passing over the extrinsic

muscles of the antenna, it gives rise to a small

"threadlike" branch that turns backward and upward, lying parallel and lateral to the common duct

of the thoracic glands. Where the common duct forks

beneath the ventral nerve cord and extends parallel

to it in the thorax, the nerve branch also forks into

two subbranches, each extending laterally adjacent

to a fork of the thoracic gland. In the area of the

reservoir, each subbranch divides and subdivides to

innervate the gland. Accordingly, this branch is

named the Nervulus Glanduli Thoracicalis.

The Nervus Labialis then passes laterally over the

pretentorium toward the musculus tentorio-prementualis, which is provided with a nervule, the Nervulus

musculi Tentorio-prementualis (Nl. m. Tent-prement.). A short distance more distally the N. Lab.

gives rise to another nervule, which is directed laterally and posteriorly and innervates the musculus

postoccipiti-prementualis in several points by means

of several subbranches. This nervule is designated

as the Nervulus musculi Postoccipiti-prementualis I

(Nl. m. Postoccip-prement. I). The Nervus Labialis

then extends posteriorly and ventrally and passes

medially between the closely approximated pair of

musculi postoccipiti-prementualis. Each nerve of the

pair then diverges underneath the corresponding

member of the muscle pair. Before the area of

divergence, it gives rise to a second nervule that leads

to the m. postoccipiti-prementualis and innervates it

ventrally. This nervule is named the Nervulus musculi Postoccipiti-prementualis II (Nl. m. Postoccipprement. II).

The Nervus Labialis continues distally, passing

submedially between the m. postoccipiti-prementualis

and m. basipremento-salivarius. Before it starts paralleling the salivary duct, it gives rise laterally, on

the outer side, to a branch designated as the Nervus

Labialis Lateralis I (N. Lab. Lot. I). This lateral

nerve is divided into two nervules, Nervulus musculi

Basipremento-salivarius (Nl. m. Basiprement-saliv. I)

and the Nervulus Tegumenti Prementualis I (Nl.

Tegum. Prement. I). The first nervule extends posteriorly and innervates the m. basipremento-salivarius. The second one extends laterally over the m.

basipremento-salivarius, then penetrates posteriorly

between the latter muscle and the m. premento-paraglossaris, until it reaches and innervates the integument. In the same area, but from the inner lateral

side, the Nervus Labialis gives rise to a nervule that

passes forward over the salivary duct until it reaches

and innervates the m. dorsopremento-salivarius. It

is named the Nervulus musculi Dorsopremento-salivarius (Nl. m. Dorsoprement-saliv.).

The N. Lab. continues to extend distally and while

passing over the m. basipremento-salivarius, it gives

rise to the Nervus Labialis II. This lateral nerve
NUMBER 99 41

divides into three nervules: the Nervulus musculi

Premento-glossarius (Nl. m. Prement-Gloss.), the

Nervulus Tegumenti Prementualis II (Nl. Tegum.

Prement. II), and the Nervulus musculi Prementolabiopalpualis (Nl. m. Prement-labiopalp.). The first

nervule passes under the m. basipremento-salivarius

then twists around it and innervates the musculus

premento-glossaris. The second nervule penetrates

between the m. tentorio-glossaris and the m. tentorioparaglossaris, then passes laterally under the latter

muscle until it reaches the lateral wall of the prementum, where it subbranches and innervates the

integument. It was also noted that this nervule is

connected to a chordotonal sense organ that extends

from the base of the labial palpus. The third nervule

extends laterally over the m. premento-paraglossaris

and innervates the m. premento-labiopalpualis. Before diverging toward the labial palpus, the Nervus

Labialis gives rise to the Nervulus musculi Prementoparaglossaris (Nl. m. Prement-paragloss.), which extends laterally to innervate the m. premento-paraglossaris.

In the course of its divergence, the main labial

nerve passes under the m. postoccipiti-prementualis

and the m. premento-paraglossaris, above the m.

basipremento-salivarius and parallel laterally to the

m. premento-labiopalpualis. In the area of the "palpiger," this main nerve gives off three branches.

The first branch, the Nervulus Tegumenti Paraglossaris (Nl. Tegum. Paragloss.), extends toward

the paraglossa, enters it, and innervates its integumental walls. The second branch, the Nervulus

Tegumenti Glossaris (Nl. Tegum. Gloss.), extends

laterally and ventrally. It then passes over the tendonlike apodemal growth to which the m. prementoparaglossaris is attached, reaches the lateral side of

the glossal rod, and stays adjacent to the rod until

it terminates. This nervule probably innervates the

labellum, but only detailed histological studies could

prove this point. The third branch, the Nervus Labialis Sublateralis HI (N. Lab. Sublat.), extends

medially through the labial palpus to its termination. While running through the first segment of the

maxillary palp, this lateral nerve passes under the

m. labiopalpomere I—II, to which it gives off a

nervule designated as the Nervulus musculi Labiopalpomere I-II (Nl. m. Labiopalp. I—II). The part

of the Nervus Labialis Sublateralis III that passes

through the labial palpus gives rise to several

branches innervating the integument. Accordingly,

this portion is named Nervulus Tegumenti Labiopalpualis (Nl. Tegum. Labiopalp.).

Nervus Tegumentualis (N. Tegum.) (Figures 1-10)

In the honey bee, this nerve is a separate structure

on the posterior face of the Ganglion Hyperoesophagale. According to Jonescu (1909), however, this

nerve has its center in the Ganglion Hypoesophagale.

Jonescu also states that "according to Kenyon, the

'salivary gland' nerve arises on the side of tritocerebrum." Yet examination of Kenyon's original publication revealed that Jonescu misinterpreted Kenyon's statement with regard to this nerve. Actually,

Kenyon indicated that it arises from the side of

"ventrocerebron." According to Chaudonneret (1950-

1951), nerves innervating the cephalic integument

are of "protocerebral" origin. Consequently, he

named these nerves as the anterior and posterior

tegumentary nerves of the protocerebrum. Jonescu

(1909) agreed with Kenyon's findings and regarded

the "nerf tegumentaire" of Viallanes as a "motor

salivary gland nerve." Hanstrom (1928) stated that

it arises from the "tritocerebrum" but is entirely

tegumentary. Snodgrass (1935) found the same

situation in Dissosteira Carolina Linnaeus. Accordingly, in the present study, this nerve is described

under the Ganglion Hypoesophagale rather than the

Ganglion Hyperoesophagale.

In the honey bee the Nervus Tegumentualis extends dorsally adjacent to the Ganglion Hyperoesophagale. When it reaches approximately the level

of the movable attachment of branch II of the m.

cranio-intermandibularis, it divides into three main

branches. Two of these branches form a fork and

extend dorsally until they reach and innervate the

integument on each side of branch II of m. craniointermandibularis. In their course, they extend over

parts of the salivary gland. The third branch angles

laterally toward the compound eye, then turns ventrally, passing over parts of the hypopharyngeal

gland until it reaches the level of the lower part

of the compound eye. At this point it angles laterally

and innervates the adjacent integument. This nerve

is more conspicuous and has more branches in the

drone than in the worker or queen.

A homolog of the Nervus Tegumentualis was

found in the acridid Oedipoda coerulescence by
42 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Viallanes (1887b). Kenyon (1896) was the first to

find this nerve in the honey bee, but he disputed

Viallanes' idea that it is a sensory nerve and innervates the integument. He stated that in the honey

bee it is a "nerve to the salivary gland." Jonescu

(1909) agreed wih Kenyon with regard to its nature. My findings agree with those of Viallanes and

contradict those of Kenyon and Jonescu. Usually

this nerve passes over the salivary gland but does

not innervate it. Also, its termination (which both

Kenyon and Jonescu were unable to locate) was

found on the integument in several places. Superficially, the salivary gland seems to be innervated by

the N. Tegumentualis, but examination under the

compound microscope indicated that what appears

to be a structure of neural origin is in fact a small

trachea. Probable homologs of this nerve are found

in Vespula, (Hymenoptera), Dytiscus (Coleoptera),

Dissosteira (Orthoptera), Thermobia (Thysanura),

and others. Workers are, however, in disagreement

as to the origin of this nerve and the major ganglion

to which it belongs.

Nervus Postoccipitalis (N. Postoccipit.) (Figure 9)

Viallanes (1887a) and Kenyon (1896) were the

first authors to observe this nerve in the wasp and

the honey bee, respectively. Since they were unable

to follow it to its termination, however, they did

not name it. Jonescu (1909) termed it nerve "X"

but did not investigate its origin or topography.

In the honey bee it arises from the posterior side

of the Ganglion Hypoesophagale, close to the lateral

side of the ventral nerve cord. It angles posteriorly

and ventrally toward the postoccipital sulcus, where

it attaches to a very small ganglion located under a

previously undescribed bridgelike structure which is

formed by an arm extending transversely from the

base of the tentorium, parallels the tentorial bridge

and attaches medially to the ventral lobe of the

postocciput. The two ganglia (one on each side of

the occipital foramen) are connected to each other

by a nerve embedded in a furrow found on the posterior part of the postocciput. A very thin nerve

connects this small ganglion with the Nervus Prothoracicalis Anterior (N. Prothorac. Ant.) which

enters the thorax, passes under the occipital process

of the episternum, over the cervical apodeme of the

episternum and over the m. episterno-endosternalis,

where it meets with the Nervus Prothoracicalis

Anterior.

Nervus Posterior (N. Post.) (Figure 9)

Holste (1910) designated this nerve as "nervus jugularis primus." He found that in Dytiscus it leaves the

"suboesophageal ganglion" and enters the prothorax,

shortly after which it gives rise to two small branches

that innervate the foramen integument and then

extend farther into the thorax to innervate the "rotator capitis superior."

Rehm (1939) described the Nervus Posterior in

the honey bee as a lateral dorsal nerve leaving the

connective union between the suboesophageal and

prothoracic ganglia. He named it the "dorsal connective nerve" but did not name its two branches.

In this study, these branches are named as follows:

the Nervulus musculi Episterno-endosternalis (Nl.

m. Epister.-endoster.), which innervates the m. episterno-endosternalis, and the Nervulus musculi Endosterno-postoccipitalis (Nl. m. Endoster n-postoccip.), which innervates the m. endosterno-postoccipitalis. A sound homology for this nerve is impossible

for the time being, since the only complete study

was made by Holste (1910), using Dytiscus. Unfortunately, he named the muscles according to their

function and did not describe their points of

attachment.

Acknowledgments

My sincerest appreciation goes to Dr. George E.

Bohart of the Federal Wild Bee Pollination Investigations Laboratory for his guidance and criticism

throughout the study.

Dr. Marian Robertson of the language department, Utah State University, deserves my thanks for

helping me devise the Latin and Greek terminology

used in the text.

Thanks are due to the Scholarly Publication Committee, Utah State University, for its financial support in several aspects of the manuscript preparation.

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1952. The Necessity of Motor Innervation for the Development of Insect Muscles. Anatomical Record,

113:560-564.

Wolff, O. J. B.

1875. Das Riechorgan der Biene. Nova Acta Leopoldina.

Deutsche Akademie der Naturforscher, 38:1—251.

Youssef, N. N.

1964. Topography of the Abdominal Nervous System

and a Review of the Abdominal Musculature of

the Honey Bee, Apis mellifera Linneaus. Master's

Thesis. Utah State University Library, Logan,

Utah.
46 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

m. cran-intramand. II

Nl. m. Cran-intramand. II

m. cran-intramand. I

Gang. Hyperoesophag.

Nl. m. postoccip-prement.

N. Gang. Phar. Post.

m. fron-susp.

m. fron-labr.

Nl. m. Fron-phar. II

m. fron-phar. II

N. Pharlabr.

Nl. m. Fron-phar. I

m. fron-phar. I

Nl. m. Fron-labr.

Nl. m. Fron-susp.

Gang. Phar.

m. clyp-susp.

Nl. m. Clyp-susp.

Nl. m. Cran-intramand. I

Nl. m. Gen. Card.

mi. clyp-cibpariet.

Nl. Gland, mand.

N. Gang. Phar. Ant

gland.mand.

Nl. Tegum. Labr. I

N. Labr.

Nl. m. Clyp-epiphar.

m. clyp-epiphar.

Nl. Tegum. Labr. II

FIGURE 1.—Dissection of head of the worker (frontal view).
NUMBER 99 47

m. cran-intramand. //

Nl. m. Cran-intramand. II

FIGURE 2.—First stage of dissection of the head of the worker (sagittal aspect).
48

Com. Corp. Allat.

Com. Corp. Card,

m. oriscut-susp.

Nl. m. Circulophar.

m. circulophar.

m. tent-oriscut.

Nl. m. Tent-orics.

m. postoccip-prement.

Nl. m. Postoccip-prement. I

m. tent-prement.

Nl. m. Tent-prement.

Nl. m. Tent-stip. II

labrum

Nl. m. Clyp-epiphar.

m. clyp-epiphar.

mandFIGURE 3.—Second stage of dissection of the head of the worker (sagittal aspect).
NUMBER 9 9

N. Postoccipit.

N. Anten. Lat. I

N. Gang. Phar.

N. Ant. Tegum.

Nl. m. Tentscap. I

m. tent-xap. I

Nl. m. Tentscap. II

m. tent-xap. II

N. Ant. Lat. II

m. tent-xap. Ill

Nl. m. Tentscap. Ill

m. tent-xap. IV

Nl. m. Tentscap. IV

N. Labr.

m. gena-card.

m. tent-card.

Nl. Tegum. Labr. I

Nl. Tegum. Labr. II

Nl. m. Intra. Susp. Dors,

m. fron-labr.

Nl. Labr.

m. clyp-epiph.

Nl. Tegum. Labr. Ill

m. stip-maxpalp. I

m. stip-maxpalp. II

FIGURE 4.—Third stage of dissection of the head of the worker (sagittal aspect).
50 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

m. gena-card.

cardo

m. tent-card.

Nl. Tegum. Stipiti I

m. stip-lac.

N. Max.

N. Max Lat. II

N. Max Lat. Ill

Nl. m. Stip-lacin.

N. Max. sub/at. I

N. Max. sublat. II

Nl. m. Stip-maxpalp. //

Nl. m. Stipgal.

N. Max. sublat. II

Nl. m. Stipgal.

lacinia

m. stip-maxpalp. II

Nl. Tegum. Stipit. II

m. stip-gal.

stipes

m. stip-maxpalp. I

Nl. Maxpalp.

Nl. Maxpalp.

N. Max. Lat. Ill

93 lea

FIGURE 5.—Dissection of the maxilla of the worker (lateral aspect).
NUMBER 99 51

prement.

m. prement-gloss.

N. Lab.

Nl. Tegum. Prement I

Nl. m. Postoccip-prement. II

Nl. m. Prementsalv.

N. Lab. Lat. I

m. postoccip-prement.

m. basiprement-sal.

N. Lab. Lat II

Nl. m. Prement-labiopalp.

m. prement-paragloss.

Nl. m. Prement-paragloss.

Nl. m. Dorsoprement-salv.

m. dorsoprement-sal.

m. prement-labiopalp.

m. postoccip-prement

Nl. Tegum. Prement. II

paraglossa

palpus

m. labiopalp. Ill

Nl. m. Labiopalp. Ill

FIGURE 6.—First stage of dissection of the labium of the worker (frontal aspect).
52 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 7.—Second stage of dissection of the labium of the worker (frontal aspect).

m. prement-gloss.

N. Labr.

Nl. Tegum. Prement. I

Nl. m. Prement-Gloss.

Nl. m. Prementlabiopalp.

Nl. Tegum. Prement II

m. prementparagloss.

Nl. Tegum. Paragloss.

Nl. Tegum. Gloss

N. Lab. Lat. Ill

paraglossa

Corp. Card,

dorsal vessel

Nl. Gland. Thorac.

N. Corp oa Hat.

N. Gang. Phar. Post

Nl. m. Cran-phar.

m. cran-phar.

Corp. Allat.

Com. Corp. Card.

pharynx

Com. Corp. Allat.

FIGURE 8.—The retrocerebral complex in the honey bee.
NUMBER 99 53

N. Postoccipit

N. Prothorac. Ant.

Nl. m. Endostern-postoccip.

m. endostern-postoccip.

Nl. m. Epister-endoster.

m. epister-endoster.

FIGURE 9.—Dissection of the cervical area of the worker showing the topography

of Nervus Posterior.
54 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 10.—Dissection of the head and cervical area of the worker (dorsal aspect).

' U.S. GOVERNMENT PRINTING OFFICE: 1971 137-336/8


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