The Mouth Parts and Digestive Tract of Adult Dung Beetles (Coleoptera: Scarabaeidae), with Reference to the Ingestion of Helminth Eggs

The Mouth Parts and Digestive Tract of Adult Dung Beetles (Coleoptera: Scarabaeidae),
with Reference to the Ingestion of Helminth Eggs
Author(s): Albert Miller
Source: The Journal of Parasitology , Oct., 1961, Vol. 47, No. 5 (Oct., 1961), pp. 735-744
Published by: Allen Press on behalf of The American Society of Parasitologists
Stable URL: https://www.jstor.org/stable/3275463
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THE MOUTH PARTS AND DIGESTIVE TRACT
OF ADULT DUNG BEETLES (COLEOPTERA: SCARABAEIDAE),
WITH REFERENCE TO THE INGESTION OF HELMINTH EGGS":
ALBERT 'MILLER
Department of Tropical Medicine and Public Health, School of Medicine,
Tulane University of Louisiana, New Orleans
bium (fig. 1). The hypopharynx, attached to
When the eggs of human Ascaris and hook-
worm are ingested by adult dung beetles they the inner surface of the labiumi, lies in the oral
are usually destroyed or damaged. The experi- cavity or cilariuml surrounded by the other
lmental results reported separately (Miller et al,mouth parts. Excepting the maxillary palpi and
1961) indicate that helminth eggs in fecal foodthe ternlinal segment of the labial palpi, the
are destroyed by the action of the mouth parts exposed parts of the imaxillae and labium are
of Canthon and Phanaeus, since they rarely ap- densely clothed with hairs which conceivably
peared at any level of the digestive tract unless counteract their tendencv to become caked with
they were artificially introduced past the mlouth Iloist feces and soil and facilitate their cleans-
parts by injection. Pinoti,s, oni the other hand, ing. The oral aperture is surrounded and comswallowed many eggs which survived, althoughpletely concealed by the bases of the appendages.
a high percentage were daiiaged.
The mouth parts and digestive tract of COaWVhile these mouth parts are fundamentally
thon lCaeis (1)rury), Phianaes igne1s MacL.,
sililar to those of leaf-eating scarabaeid beetles
and Pinoturs carolinlls (Linn.) were studied
(e.g., Junle beetles) they are markedly modified
conlparatively to determine the mechanism ofto adapt them for manipulating the soft moist
these effects. The three species are essentially feces which constitute the usual diet of dung
alike in the form and function of these organs.
beetles. This adaptation is most conspicuous in
the hairy and flexible spatulate blades borne by
OBSERVATIONS
the nlandibles (figs. 2 and 3, inc) and maxillae
The NMootlt Parts
(fig. 2, Ga, Le) which gather portions of food.
The labruml (fig. 2, Lb) and labium (Lmi) are
The mouth parts of dung beetles are of the
relatively less iio(lified, but their inner surfaces
mandibulate insect type for gathering, mastibear nnumerouis spines and hairs that probably
cating, and ingesting solid food. They consist
serve tractile as well as tactile and gustatory
of a labrum, a pair of miandibles, a pair of
functions. The hypopharynx (Hphy) is a soft,
maxillae, a hypopharynx, and a labium (fig. 2).
bulky, mobile organ for pushing the food back
These parts extend in a horizontal plane on the
between the grinding lobes (mool) of the llmandiventral surface of the head, which is of the
bles which lie directly in front of the oral aperprognathous type, and are comlpletely concealed
turle. A median ridge (x) on the hypopharynx,
from above by the expanded shovel-like frontocurved to conformll with the space between the
clypeus. The labruni is hinged to the deeply inopposed molar areas, closes the masticating
flected border of the clypeus, mnandibles and
cleft anteriorly when hel( against the imandibles.
mnaxillae are articulated to the ventral margin
(As in miost Coleoptera, no salivary glands are
of the head capsule between the eyes, and the
evident.)
base of the labiuml formis part of the miedian
The mandibles are of special interest since
ventral wall of the head. The entire labrum and
their form and function support the experimenall but the outer basal area of the mandibles are
tal evidence that they are the organs responsible
concealed by the underlying maxillae and lafor the destruction of ingested helminth eggs.
They are mechanically complex to adapt them
Received for publication February 2, 1961. for their dual function of gathering and masti* This investigation was supported in part by
eating fecal material.
Each mandible (figs. 2 and 3) consists of a
National Institute of Health Research Granit No.
G-4102.
735
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736
'THE JOURNAL OF PARASITOLOGY
The mlolar
basal supporting articular portion, a distal
in-areas constitute the precise site
cisor lobe (ine) and an inner basalwhere
molar
food
lobe
particles and inclusions like helminth is
eggs
are comlllinuted. The efficiency of
(mol). The supporting portion, which
nartitration
depends upon the structural characrowly triangular in side view, bears
a dorsal
teristics
of the
socket (fig. 2, da) and a ventral coidyle
(figs.
1 mlandibles in general and of
these areas in particular.
and 3, va) which articulate with corresponding
Aside
structures on the head capsule mresad of
thefrom
eye.the shape and direction of curvature fulcral
of the surface, the left and right molar
These articular points form a vertical
areas adductor
are structurally similar (figs. 4 and 5).
axis between the insertions of the large
The
grinding surface is vertically elongate, 4
muscle (fig. 3, ad) and the smaller
abductor
to 5 tinmes as
muscle (ab) which are attached, respectively,
tohigh as wide. It bears a series of
parallel,
the inner and outer edges of the base.
The closely
man- set, transverse cuticular ridges
(r), ofto
uniforlml
thickness except for gradual
dible, hinged along its laterobasal edge
the
enlargement
at the upper end of the molar area.
head, thus pivots in a horizontal plane.
The in-
The ridges
appear superficially as striatiolns
cisor lobe (ine) is a thinl leaflike blade
which
projects forward horizontally beneath
la- posteriorly to form a stiff fringe
whichthe
project
suggest a file-like surface. Since the
brum. It bears a proximal collib of (mnfr)
hairs and
(cllb)
ridges
extend
and distal fimbriated processes (ifr)
along
its parallel to the direction in whilch
thethe
mlolar
area moves, it is evideint that they
inner edge, and many small setae on
dorsal
and ventral surfaces of the blade. The molar
cannot function directly as grinding ridges.
Closer inspection reveals that the true surface
lobe (mol) is massive, projects mnesad in a vertiin fact, not ridged, but siiiooth, leathery, and
cal plane, and bears a smooth molar area onis,
the
resilient (fig. 6, s).
medial surface which opposes that of the other
When the molar area is isolated, cleared, and
mandible. Varying degrees of sclerotization in
mounted, with or without pretreatrment with
the walls of the mandible produce thick, rigid
supporting areas and thinner flexible regions.
potassium hydroxide, high magnification discloses that the ridges are microscopically coiiVentrally a distinctive oval flexible area (fx),
plexisin structure (figs. 6, 7, 8). Viewed froml
consisting of a series of corrugated folds,
present between the incisor and mlolar lobes.
above, they appear cross-striated or barbed, b)ut
analytical study of detached fragments of ridges
The two muandibles are syllmmetrical except
for the miedial molar area. This is convex on
in lateral or transverse aspects reveals that the
the right mandible (fig. 2, Md') and concave on upper edge of each ridge bears a double series
the left (Md"), the two miolded perfectly to fit of rectangular lobes. These are contiguous with
closely together. They form an efficient grinding those of the neighboring ridges and collectively
apparatus that functions like a pair of opposed formn a smlooth microscopic pavemen t which
millstones that part to adniit grist, coiie to- constitutes the true surface of the molar area
(figs. 6, s, and 7). The ridges which carry and
particles between them. These Ilovemenits, cush- underlie these structures have a greater optical
ioned by the flexible areas of the molar lobes, density and are thus visible beneath the surface.
The architecture of the ridges is extraordiare ilmparted by alternate contractions of the
mandibular muscles, the abductors swinging the narily precise and regular. The distal ol upper
mandibles outward and the adductors inward.
half of the ridge widens and is incised at uniThe simlultaneous miotion of the two miiandiblesform intervals alternately on each side (figs. 7
gether, and oscillate through a short are to crush
thus alternately spreads apart and approxi-and 8, b, c) to produce two parallel rows of
mates the incisor lobes to push food medially prismatic lobes. A ridge fragment viewed froim
the side thus appears comb-like, with a srries
and at the same time produces the grinding
of columnar, truncate, and continguous "teeth"
action of the molar lobes upon mnaterial that is
introduced between thelm by the anteroposterioralong its upper edge. Viewed from above, tlhese
movements of the hypopharynx. The special are seen to be the edges of the narrowly recflexible areas (fx) of the iman-dibles may also en-tangular lobes which extend transversely froiml
able independent mioveiments of the molar lobes the midline of the ridge. The lobes on one side
by the adductor iiuscles while the mlandiles areof the ridge lie opposite the incisions which
demarcate the lobes oii the other side. In a verin the closed position.
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MILLER-ALIMEN TARY SYSTEM OF DUNG BEETLES
737
In the
species of the subfamily Coprinae, the
tical cross-section of the ridge the paired
lobes
sizes of
molar areas and of the tritors are
form a laimellate scraper-like structure
at the
the
correlated with the average size of the
sumnlit (fig. 6, t, and 8). Each lobe is directly
vertically
beetle,
all three dimensions decreasing in the
striate due to minute parallel grooves
on the
series Pinotus
side which is directed toward the anterior
edge - Phanaeus - Canthlon - Ateuchus
(= Choeridium) - Onthophlagis. The large Pinoof the molar area (fig. 7, c). At the posterior
tlis has
fewer
edge of the molar area, only the upper
edge
ofand larger tritors than Ph(naeus
and Canthon,
the ridge projects to form a ray of the
molar and its molar area is thus inconfringe (figs. 4, 5, ifr). It widens and spicuously
forms a coarser in strucure. The small mandibles oftip.
Ateuchus and Onthophag,ls, with fewer
flat blade with a blunt or raggedly toothed
On the fringe ray the ridge lobes are replaced
by pointed spines which project outward
on
C;
each side and become sparse distally.
Each of the ridge lobes is a microscopic
grinding, rubbiig, or triturating instrulment,
here termled a "tritor" (figs. 7, 8, tri). The
tritors are specialized cuticular structures which
extend at right angles to the direction in which
the molar area moves. Their position and structural characteristics are perfectly fitted to their
function. They combine strength and firmlness
with a degree of flexibility, collectively constitute the entire molar surface, and act as a multitude of stiff scrapers. Food squeezed into a thin
film and rubbed between the two closely apposed
molar areas is thoroughly triturated by thousands of these milute scrapers acting in unison
against those of the opposite mandible. The
efficiency of the grinding action is attested to by
the destruction of particles as small as hellnith
eggs and perhaps even protozoan cysts. In this
regard, the size of the tritors relative to such
eggs and cysts is significant.
Table I compares seven species of dung
beetles in regard to body length, dimensions of
the molar areas, and size of typical tritors,
o00
dCC3
CZ
C) c, 'T'
u,
HePi
O
c
) CM
odoa
co
I'l
a
E?
s
3 3
3 ,?a re a
;U
c.
y
k
"
E1Q! a
E?
1 k
c
r1
I
e
?,3'" a
'c,
3
fcE oU t
'I.
i/-Y IR E
E.
-q
x xx x x x
X
x
_: ,X.,
0 ,
.-4 -X
t-
h
;1 C"
sr
5
C
3 S 3 k.i O
trori=k
31 0 %3 0
Eoa- 33
h
x
E*
Ct,
N
Ie t
3
O
c
26C)=
h
u
3kQ,53j rc'ij
rr
h
xx
0 -4 (M co
v
fC
C
X X I I
O
Q,
C13
00
1-
CC 0 0
-
k~-
019.
C11cl -tr
Q1V
3
cfi
0d
-
Da
3kE:
X
>t- C
1_
r..
_
MC
a c,.,
ol;
G
F9P'
5
CL : 1k. 0 0 0
i^ - 5+ co d
+e
C'li-ii-l
r-l
X
3r S 5
;lli *4 1
N
along with the total nunlber of ridges and tritors
on the Inandibles. The size of the molar area in
each species varies within narrow linlits with
the size and sex of individual beetles and differs
r3
We
N
03~r
0?
ii;
'C_ 0 0 !
slightly between right and left mlandibles. It is
here represented by the average lengths of its
ridges and fewer but
much finer structure than those of Canthon and
long and short axes. The tritors show a slight
Phanaeus.
gradation in size according to their position;
the dimensions given are averages based on The mandibles of Aphodius (Aphodiinae)
measurements of series on ridge fragments from
are simlilar to the coprine type, except for a
the central part of the molar area. The number
shorter and more triangular incisor lobe. The
of ridges is, for each species, an approximate
molar area is wider relative to its length and
has a smaller area and fewer and thicker tritors
average of several pairs of mandibles, and the
estimated number of tritors (two rows on each
than that of Onthophagus pennsylvanicus Har.,
ridge) for both mandibles is derived from the
a coprine of similar size. In Geotrupes blacklength and number of ridges and the thickness
barnii (Fabr.) (Geotrupinae) which is comof the tritors.
parable in size to Canthon laevis and Phalaeus
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sm
THE JOURNAL OF PARASITOLOGY
738
igneus, the mandibles differ markedly
are in
structurally
appear- capable of grinding material
into particles smaller than Ascaris eggs, but
ance from the Canthon type. They are relatively longer, have a massive, rigid, and toothed they allow many eggs to pass into the digestive
incisor lobe, a less specialized hirsute comb area, tract in a viable condition when they are ingested
and a less strongly developed molar lobe. There with feces.
are fewer tritors, and these are slightly larger
The Digestive Tract
than those of Ph. igneus.
The digestive tract (figs. 9, 10) consists of
The comparative average sizes of the eggs
of Ascaris lnmbricoides (70 by 47 microns), a short pharynx (Phy) and esophagus (Oe)
Necator americamus (70 by 38 microns), and which constitute the fore-gut; a long, coiled
Trichuris trichiutra (52 by 24 microns), the cysts ventriculus (Vent) which is the mid-gut; and a
hind-gut which includes an anterior intestine
Giardia lamblia (11 by 7 microns), and the (AInt) and a posterior intestine or rectum
(Rect). In Canthon laelis the lengths of these
tritors of Canthon and Pinotus are shown by the
diagram in figure 6. In figure 7 outlines of thedivisions in millimeters are: pharynx, 0.5;
ascaris egg and amebic cyst are superimposed esophagus, 1.5; ventriculus, 164; anterior inon the surface view of the molar structures, the testine, 9; rectum, 1. The mid-gut thus constisolid outlines indicating scale relative to the
tutes most of the total length of 176 mm and
tritors of Canthon and the broken outlines the
is about 10 times as long as the body. The proscale relative to Pinotlus. The surface area of a
portions are similar in the larger tract of
of Entamoeba histolytica (12 microns) and
Pinotus.
tritor in Pinottus is about twice that in Canthon,
so that the longitudinal section of the ascarisThere is no differentiated crop or proventriculus in the fore-gut, and the esophageal
egg covers an area equivalent to about 166
tritors in Canthon and about 76 in Pinotus and
valve consists of a simple fold of epithelium
into
the cross section of the amebic cyst an area
of the ventriculus at its junction with the
about 7 tritors in Canthon and 3 in Pinotus.
esophagus, as described and illustrated for
These differences in the relative size of the
Phanaeus by Becton (1930).
The ventriculus extends from the prothorax
tritors may account, at least in part, for the
to the base of the abdomen as a straight tube
greater destruction of helminth eggs observed
(ThVent),
then narrows slightly and becomes
in Canthon (and in Phanaeus) compared
to
that observed in Pinotts.
a closely coiled mass (AbVent) that occupies
The efficiency of the grinding action of most
the of the abdominal cavity. This compact
mass consists of four counterclockwise spiral
mandibles is also reflected by the size of parcoils succeeded by five clockwise coils, the smaller
ticles in the paste-like gut contents. These apcentral coils lying within the larger anterior and
pear coarser in Pinotbus. In field-collected beetles
posterior coils, and all held closely together by
preserved in alcohol, samples of the midgut
contents from four to six specimens of each
an abundance of tracheae ensheathed in adipose
species showed the following ranges in the size, tissue. Throughout its length the ventriculus
respectively, of the largest particle and of most bears numerous small papillar crypts (Cpt)
of the larger particles (in microns): Pinotus that confer a villous appearance to this portion
carolinus, 6 to 16 and 6 to 12; Canthon laevis, of the digestive tract. These crypts are cylin7 to 9 and 5 to 8; Phanaeus vindex, 7 to 10 and drical masses of epithelial replacement cells
5 to 7; Onthophagus pennsylvanicuts, 3 to 5 andprojecting through the lattice-like layer of
2 to 4. These particle sizes show positive correla-weakly developed circular and longitudinal
muscles which surrounds the epithelial tube.
Although the efficiency of the grinding ac- At the junction of the ventriculus and hindtion must depend upon a combination of me-gut is a short muscular pyloric valve (fig. 11,
Py) which lies behind the insertions of the four
chanical factors, including the precision of ocMalpighian tubules. The anterior intestine declusion and the amount, nature, and rate of flow
of material between the mandibles, it is evi- scribes one small clockwise coil which is succeeded by a single large counterclockwise loop
dently significantly influenced and limited by
the size of the individual tritors that constitute
that lies dorsal to the ventricular mass and joins
tion with the sizes of the tritors listed in Table I.
the rectum. The anterior intestine and rectum
the grinding surface. The mandibles of Pinotus
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MILLER-ALIMENTARY SYSTEM OF' DUNG BEETLES
739
slender,
coiled ventriculus (stomach) and
are provided with colspicuous spiral
and and
circular muscles which surround a layer
longi-nutrients are digested directly by
theof
contained
tudinal muscles. The rectum opensthe
to beetle.
the exThe residue is partly dehydrated in
terior through the anus which is located at the
the hind-gut and is excreted as a soft strand
apex of the abdomen between the pygidium and
surrounded by the peritrophic membrane.
The beetles are voracious feeders and evihypopygiuni.
The mid-gut and hind-gut are lined by a
dently Imust ingest large amounts of feces to
thin peritrophic lmembrane (Pmb) which sur- obtain sufficietnt nourishment. The fecal mlatter
rounds the intestinal contents ald encloses the
contains undigested food residues, endogenous
continuous strand of excrement which the beetle
secretory and excretory products, and bacteria,
extrudes as it feeds.
yeasts, and molds. The cheiiiical composition of
The four Malpigllian tubules (Mal) lie humlan
in
feces, cited by Everett (1946), is apa tightly coiled miass within the loop of the proximlltely
an75 percent water, 4 percent fats,
terior intestine anld between the adjoining ve(n3.5 pelrcent inorganic salts, 2 percent sterols,
tricular loops.
and 1 percent total nitrogen. Less than 5 perThere are no grindlg structures in the dicent of the digestible dietary constituents are
excreted, and 10 to 25 percent of the fecal mass
gestive tract. The food material which is finely
consists of bacteria. The microbic content of
conmminuted by the ilandibles is swallowed and
passes through the ventriiculus as a uniformn
the dung of herbivorous animals is probably
paste which is subjected to the action of dieven greater. Like coprophagous fly larvae, dung
gestive fluids secreted by the epitheliulm. Ab- beetles undoubtedly subsist to a considerable
sorption of nutrients presumably occurs silmul- degree upon the substance and products of
taneously in the -ventriculus. Charcoal-laden
microorgaMllisms that they ingest.
feces ingested by PI'ha,aes vindex extend
Comtparative Morphology
throughout the ventriculus within 2 hours. When
The spatulate maxillary and mandibular lobes
undisturbed, beetles mlay continue to feed at the
and the type of miolar areas described are charsamie spot for several hours and extrude coiled
acteristic of the dung-feeding Coprinae and
strands of excremenl t which somettimies exceed
Aplhodiinae. They d(iffer markedly from the
five centimeters in length.
correspondilng stlructures in plant-feeding scaraThe digestive tract is adapted by its length
baeids of other subfamnilies which have stout
and capacty to extract lnutrilment rapidly from
maxillary and Imandibular lobes with rigid teeth
relatively large ammiounts of the fecal food.
for grasping and cutting, and coarse mlolar
DISCUSSION
Alimentation alnd Nultrition
ridges for bruising and chopping vegetable tis-
sues (as in the Japanese beetle, illustrated by
Swingle, 1930, and Snodgrass, 1950). Examina-
The functional modifications apparent in tlletion of the luolar areas of several phytophagous
morphology of the alimentary system of adult
species reveals that, in place of the fine horizondung beetles are readily correlated with thle tal, tritor-bearing ridges found in dung beetles,
physical and chemical nature of their food. This
there are coarse vertical ridges, mnassive in strucis typically soft, moist vertebrate fecal niaterial,
ture and devoid of tritors. In a pollen-feeder
but solme species also eat decaying aniltmal and(Euphoria sp.) and a sap-feeder (Ligyyrus gibvegetable matter or fungi (Ritcher, 1958). Thebosus) neither ridges nor tritors are present on
beetles are hence fundamllentally mlicropliagousthe molar areas which are sliall non-protuber(Brues, 1946). The food is swept iito the oral
ant plates near the bases of the mIandibles.
cavity by the blade-like distal lobes of the miaxil-Geotrilpes blackbfurnii, which feeds on dung,
lae and mandibles, pushed back by the large mo-carrion, and fungi (Howdeln, 1955), has tritors
bile hypopharynx, and thoroughly coiminiiiutedalnd spatulate mIaxillary lobes, but the incisor
by the specialized molar areas of the mandibles.lobe of the mllandible is rigid and bears teeth.
Since there are no storage chamlbers and no in-(Cf. Hardenberg, 1907.)
dication of microbial smiiibioiits in the alimien- The scarabaeid type of coprophagous mouth
tary canal, the finely divided food material, en-parts is not found in coprophilic beetles of other
closed in the peritrophic lmembrane, presumlablyfamilies. The mnandibles of Trox (Trogidae) are
moves in a continuous streaml through the long,
hard, short, and massive and have neither molar
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740
FTHE JOURNAL OF PARASITOLOGY
tailed comparison
of the larval and adult mouth
lobe nor molar area of the coprine type,
while
parts
of individual species of dung beetles would
the Histeridae and Staphylinidae have
cutting
of particular interest in the following coninandibles primarily adapted for abepredatory
text.indicated
habit. (Coprophagy, however, may be
by secondary modifications: in the Ingestion
staphylinid
of Parasites
Baryodma the cutting edge of the mandible
is structural details of the lmanThe described
extended into a thin hairy flange and the maxildibles and digestive tract elucidate experimental
lary lobes are hairy flaps.)
observations, previously reported, that Canthon
The digestive tract of dung beetles
rela- destroy ascaris and hookworm
andisPhanaens
tively much longer than in phytophagous
scaraeggs and
protozoan cysts present in ingested
baeids: 8 to 10 times as long as the
body
inbearing on the oral infection of
feces.
Their
dung beetles by other parasites must also be
times in Phyllophaga, Diplota.is, and Popilliaconsidered.
(Becton, 1.930; Fletcher, 1930; Jones, 1940;
The observed destruction of helminth eggs
Swingle, 1930). The ventriculus also constitutesis directly attributable to the grinding action of
a greater portion of the tract in dung beetles the mandibles. The nature of the molar areas
(about 88 percent) than in the plant-eaters (50 explains the ability to destroy microscopic obto 66 percent). The hind gut of dung beetlesjects in the food, and the absence of other grindlacks the specialized area or dilatation of the ingl structures in the digestive tract enables eggs
Phanaels and Canthon, compared to 1.5 to 3
anterior intestine which is preslumably a fermeni-
to escape mechanical injury when inoculated
tation chamber in phytophagous species. Fecal into the pharynx behind the mlandibles.
food apparently does not require further miSimilarities in the mandibular mnechanism
crobial processing within the beetle for its utilisuggest that all species of dlung beetles are capazation.
ble of destroying ingested eggs of ascaris and
The larvae of Coprinae feed upon buried
hookwortl. The degree of destruction evidently
dung which the adults provide when the eggs are
dep-nlds upon the relative efficiency of the manlaid. The illustrations of the mouth parts of
dibles in a given species of beetle, and this seems
the larvae of Pinotus given by Ritcher (1945) to be influenced by their size. Although the large
show that they differ miarkedly from the adultmlolar areas of Pinotus have only slightly larger
organs. The mandibles and maxillae bear teeth tritors, they allow the passage of lany viable
instead of spatulate lobes and are in this way eggs, while those of (anthon, and Phanaeus
perhaps adapted to cut fecal material that has destroy practically all ingested eggs. No experibecome consolidated and partly dehydrated. Themental observations have been made on small
fine structure of the molar area has not been
species like Onthophagls, but the small size of
described, and the efficiency of its grindingthe tritors and of particles in the gut would lead
action is unknown. The larval mlandible of Geoone to expect that they, too, could destroy eggs
trotpes (Ritcher, 1947) also differs from the
anld cysts of the kinds that proved vulnerable in
adult mIandible. In contrast to the adult, the
the larger species. The demonstrated efficiency
larva of Canthon has a digestive tract only twice
of the medium-sized species indicates that they,
as long as the body (Rapp, 1947), although
at least, do not transport the eggs of human
longer than the tract in phytophagous scara- ascaris and hookworml internally.
baeid larvae (1.3 to 1.8 times body length:
Dung beetles serve as the intermediate hosts
Areekul, 1957). However, like the adult, the
of a lnumber of spirurid inemlatode and tape-
larvae has a relatively longer ventriculus than
worlm parasites of insectivorous and carnivorous
phytophagous larvae and lacks the gastric caecavertebrates (Hall, 1929; Morgan and Hawkins,
and (in Rapp's figure) the dilatation of the1949). Spirurid larvae have been reported in
anterior intestine which are variously developed
species of Scarbaeofs, , Coitheo1, Pha7ae,s, Piin phytophagous larvae. In described phytonotfrs, Copris, Onthophiagtfs, Aplhodiois, Ataephagous species the larval ventriculus has caeca
nilts, and Geotrupes, and the larvae of avian
but no crypts while the adult ventriculus hastapeworms in Cbhoeridfinm, Onthophi)ag.is, Apho-
crypts but no caeca. The physiological and phydilsR Ataeni,fs, and Geotr)pes (Seurat, 1916;
logenetic relations reflected by these variations
Ransomi and Hall, 1915; Cram, 1931; Aiic(ita,
of structure invite further investigation. De- 1935). Spirurid larvane were frequently folnd
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MILLER-ALIMENTARY SYSTEM OF D)UNG BEETLES
741
microns,
the shells are "thick" (3 microns), and
in the body cavity of adult Canthon,
Phaiaaeus,
and Pinotus in the course of the present
each contains
invesa larva when passed in the vertebrate host's feces
tigation, but ascaris larvae in elmbryonated
eggswhich does not hatch until
did not survive ingestion by Canthon. How,
ingested by the arthropod host. The eggs of
then, do dung beetles become infected with
cestodes known to undergo larval development
spirurid and cestode larvae despite the ability in the beetles range from 60 by 45 to 88 microns
of the mouth parts to destroy other hellninth in diameter, have thick enlvelopes surrounding
eggs?
the smaller onchosphere, and Imay be enclosed
Most of the published records indicate sim- in the adult proglottid when passed by the verply that spirurid larvae were found in the body tebrate host (Sprehn, 1932). It seems doubtful
cavity of beetles collected in the field. Seurat that the size of these eggs would make them
(1916) states that they were usually encapsu- immune to the grinding action of dung beetle
mandibles that destroys ascaris and hookworm
lated third-stage larvae, in one instance 68
Spirocerca sanguinolenta and 4,880 Physocephaeggs which are of similar or only slightly larger
lbs sexalatus in an individual Scarabaens sacer.
dimensions. They or the contained larvae must
be adapted in solie way to withstand lmechanical
-lowever, he also reports finding first-stage
larvae of these worms, approaching the first
destruction when ingested, perhaps by a resilmolt, free in the body cavity of adult S. iency
sacer.of the walls different from that of the
Sotme of the larvae that we found in other beetles
hunllan parasite egg,s, or by additional protecwere not encapsulated. Since spirurid eggs con-tive coverings arou(lnd the egg mass. Probably
many are, ill fact, destroyed during ingestion,
tain larvae when deposited in host feces and
hatch only in an insect host, these records indi- while others may be assisted to hatch by the
cate that dung beetles miay ingest them in large griinding action of the manldibles. Since spirurid
numhbers and mav become infected in the adult
eggs may be very abundant in the dung that is
stage.
eaten in large aimtoumits by beetles, their destruc-
Experimental infection by feeding eggs to
adult dung beetles seems to have been reported
only for the following: The spururids, (ongy-
of infection in the insects. The coltentts of the
lonema pulchrim in Aphodias spp. (Ransom
and Hall, 1915), Ascarops strongylina in Aphodits granarius and Physocephala.s sex.alat.l in
Ataenitts cognates (Alicata, 1935) ; and the cestodes, Raillietina cesticiflls1 and Hiymnenolepis
carioea, in Choeriditum histeroides (Cram and
Joiies, 1929) and in Aphodias granariais (Jones,
1930), Hymenolepis cantaniana in A taeni.s
cognatsn (Jones and Alieata, 1935), and Cho-
anotaenia infundibi(llfm in Geotr'ipe.s sy7l vati-
cis, Ataenius cognatrs and Aphodias spp.
tionl may preventt excessive and harmful degrees
destroyed eggs would presumably be utilized as
food, so that il the encoumlter between worm
and beetle, the beetle would emerge the victor
rather than the victim.
The observed difference in Canthon and Pinotals with respect to the destruction of ingested
ascaris and hookwoirm eggs suggests that species
of dung beetles, in the adult stage, may also
differ in susceptibility to spirurid and cestode
infection in a(ccodance with the grinding efficiency of the nmandibles. In the species that have
been, experimentally infected, mastication may
(Horsfall and Jones, 1937, citing Joyeux, 1920, be weaker than in Canthon because the man-
for Geotrupes). Except for Geotr.pes, the dibles are simall (ApJhodis, A tnaelsl , Choeridbeetles infected experimentally a re all small
ilm) or less specialized (Geotrapes). The occurrence of spirurids in the large d1ung beetles
could also l)e the result of iiigestioni of eggs by
Seurat (1916) records Ph!/isaloptera al)brethese species during their larval stage. Mandibu-
species (Aphodiinae an1d Choeriild,m of tih
Coprinae).
rinata third-stage larvae in a larva of A tench .s
Ilar a ctiom nmay be less efficient in the larva than
(= Sanrabae(s), and Ransom and Hall (1915)
in the (adulllt.
found newly hatched larvae of (ong/ylo1em1 n
scIfOtItama, (= palch rm ) in larval A phiodis spp., Fuirther( detaliled imorlphological and experimental investigation is needed to resolve the
but no published record of experimental infe.-
tioii of larval dung beetles has }been encountered.factors underlying the apparent contrast in the
fate of different kinds of helminth eggs when
The eggs of spirurids for which dlng beetles
serve as hosts range fronl 30 by 11 to 59 by 34they are in'ested by dung beetles.
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THE JOURNAL OF PARASITOLOGY
742
SUMMARY
the trophi of the Scarabaeidae. Tr. Wis. Acad.
Sci., Arts, Lett. 15: 548-602.
M. W. AND JONES, M. F. 1937 The
1. The chewing mouth parts of adultHORSFALL,
dung
history of Choanotaenia infndibluim, a
beetles are specialized for efficient ingestionlife
and
cestode parasitic in chickens. J. Parasit. 23:
mastication of soft feces. The terminal lobes
435-450.
of the maxillae are spatulate anld hairy,HOWDEN,
the
H. F. 1955 Biology and taxonomy of
hypopharynx large and mlobile. The complex
North American beetles of the subfamily
Imandible has a flexible, fringed, blade-like in-Geotrupinae, with revisions of the genera
Bolbocerosoma, Eucanthus, Geotrupes, and
cisor lobe and a large molar lobe which bears
Peltotrupes (Scarabaeidae). Proc. U. S. Natl.
a smooth, resilient grinding area. This consists
Mus. 104 (3342): 151-319.
of a multitude of precisely arranged triturating
JONES, C. R. 1940 The alimentary canal of Dipstructures of a miinute size that is directly correlotaxis liberta Germ. (Scarabaeidae: Colcoptera). Ohio J. Sci. 40: 94-103.
lated with the size of the beetle. The asyiinetriJONES, M. F. 1930 (Notes on the life cycle of
cal miolar lobes are closely apposed.
Raillietina cesticillus, in Proc. Helm. Soc.
2. The tubular digestive tract colnsists of a
short pharynx and esophagus, a very long,
coiled ventriculus lined with a peritrophic melm-
brane, four Malpighian tubules, and a short
Wash.) J. Parasit. 16: 158-159.
AND ALICATA, J. E. 1935 Developmentc
and morphology of the cestode, Hymenolepis
calntaniana, in coleopteran and avian hosts.
J. Wash. Acad. Sci. 25: 237-247.
hind gut. Proventriculus, dilated storage chamJOYEAUX, C. 1920 Cycle evolutif de quelques
bers, and salivary glands are absent.
todes. Recherches experimentales. Bull. Biol.
3. Alimlentation, nutrition, comparative morFrance et de Belg., Paris, Supp. 2: 1-219.
phology, and the relation of dung beetles to
(Cited by Horsfall and Jones, 1937; not seen.)
parasitic helninths are reviewed and appraised. MILLER, A., CHI-RODRIGUEZ, E. AND NICHOLS R.
1961 The fate of helminth eggs aind proto-
The grinding efficiency of the mllandibles, varyzoan cysts in human feces ingested bly d(ung
ing with species, may be a significant factor in
beetles (Coleoptera: Scarabaeidae). Am1. J.
the susceptibility of beetles to infection by inTrop. Med. Hyg. In press.
MORGAN, B. B. AND HAWKINS, P. A. 1949
gested parasites.
Veterinary Helminthology. Burgess Publishing Co., Minneapolis.
REFERENCES CITED
RANSOM, B. H. AND HALL, M. C. 1915 The life
ALICATA, J. E. 1935 Early developmental
history
stages
of Gongylonelma scutatuzt. J. Parasit.
80-86.
of nematodes occurring in swine. U.2: S.
Dept.
Agr. Tech. Bull. 489, pp. 1-96. RAPP, W. T. 1947 The number of gastric ca-ca
AREEKUL, S. 1957 The comparative internal
in some larval Scarabaeoidea. Can. Eat. 79:
larval anatomy of several genera of Scara145-147.
baeidae (Coleoptera). Ann. Ent. Soc. Am.
R.ITCHER, P. 0. 1945 Coprinae of eastern Northl
50: 562-577.
America with descriptions of the larvae and
BECTON, E. M., JR. 1930 The alimentary tract of
keys to genera and species (Coleoptera:
Phanaeus vindex MacL. (Scarablaeidae). Ohio
Scarabaeidae). Ky. Agr. Exp. Sta. Bull. 477,
J. Sci. 30: 315-323.
1-23.
BRUES, C. T. 1946 Insect Dietary. Harvard pp.
Univ.
Press, Camlbridge, Mass.
CRAM, E. B. 1931 Developmental stages of some
lemlatodes of the Spiruroidea parasitic in
poultry alnd game birds. U. S. Dept. Agr.
Tech. Bull. 227, pp. 1-27.
CRAM, E. B. AND JONES, M. F. 1929 Observa-
1947 Larvae of Geotrupinae with
keys to tribes and genera (Coleoptera: Scarabaeidae). Ky. Agr. Exp. Sta. Bull. 506, pp.
1-27.
1958 Biology of Scalrlabaleidae. Ann.
Rev. Ent. 3: 311-334.
tions on the life histories of Raillietina cesti-
SEURAT, L. G. 1915 Contributions a l'etude des
cillus and of Hynmenolepis carioca, tapeworms formes larvaires des nematodes parasites
of poultry and game birds. N. Am. Vet. 10: heteroxenes. Bull. Soc. Sci. France et Belg.
49-51.
EVERETT, M. R. 1946 Medical Biochemistry. 2d
ed. Paul B. Hoeber, Inc., New York.
FLETCHER, F. W. 1930 The alimentary canal of
Phyllophaga gracilis Burm. Ohio J. Sci. 30:
Ser. 7 49: 297-377.
SNODGRASS, R. E. 1950 Comparative studies oil
the jaws of mandibulate arthropods. Smith-
son. Misc. Coll. 116 (1): 1-85.
SPREHN, C. E. W. 1932 Lehrbuch der Helmintllologie. Gebriider Borntraeger, Berlin.
HALL, M. C. 1929 Arthropods as intermediate
SWINGLE, M. C. 1930 Anatomy and physiology of
hosts of helminths. Smithson. Misc. Coll. 81:
1-77.
the digestive tract of the Japanese beetle. T.
HARDENBERG, C. B. 1907 Comparative studies in Agr. Res. 41: 181-196.
109-119.
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MIILLER-A LIMEA'TARY SYSTEM OF DUNG BEETLES
743
EXPLANA\TION OF PLATE
Alimentary Organs of Adult Dung Beetles
Abbreviations used in figures: Ab, abdolmenl; ab, abductor muscle; AbVent, abdomiiinl
ventriculus; ad, adductor nmuscle; AInt, anterior intestine; An, anus; Ant, antenna; Asc,
Ascaris egg (Ascaris luImbricoides) ; Clp, clypeus; cnlb, comb of incisor lobe; Cpt, crypt; Ct,
cuticular wall of mandible; da, dorsal articular socket of mandible; E, colnlpouiid eye; Eh,
cyst of Enta)ioeba htistolytica; fx, flexible area of mandible; Ga, galea (outer terminal lobe
of maxilla); G1, cyst of Giardia lamiblia; Gu, gula; H, head; Hphy, hypopharynx; ifr, fringe
of incisor lobe; ine, incisor lobe; Lb, labrumn; Lc, lacinia (inner terminal lobe of maxilla);
Lf, molar area of left mandible; Lm, labiuml; LmPlp, labial palpus; Mal, Malpighian tubules;
Md', right nanldible; Md", left nmandible; nmfr, posterior mlolar fringe; tmol, molar lobe (position of samle in figs. 9 and 10); Mx, maxilla; MxPlp, maxillary palpus; Nee, hookworm egg
(Necator avmericannes); Oes, esophagus; Pgl, paraglossa (outer terminal lobe of labium);
Phy, pharynx; PMb, )peritirotllic membranee; Py, pylorus; r, molar ridges; Rect, rectum (posterior intestine); Rt, molar area of right lmandlible; s, molar surface; t, cross section of
molar area; Th, thorax; ThVent, thoracic ventriculus; Tr, nwiiplworm egg (Trichiuris trichiura) ; tri, tritor; va, vaMd, ventrall articular condyle of mandiile; Vent, velntriculus; x, median
ridge of hypopharynx.
FIGURE 1. Head of Cuathion laceis, ventral aspect. 5 x
FIGURE 2. Mouth parts of Canthon showing relative positions and cibarial surfaces:
veiitral or epipharyngeal aspect of labruni (Lb), anterodorsal aspects of right (Md') and left
(Md") mandibles, and dorsal aspects of nmaxillae (Mx), hypopharynx (Hply), and labium
(Lm). 16 x
FIGURE 3. Right mandible of Canttllio, ventral aspect. 16 x. Arrow imllicates direction of
movement.
FIGURES 4 a1nd 5. Molar areas of right (Rt) and left (Lf) malndibles of Canthol laeyis
(fig. 4) and Pilotlts carolina (fig. 5), drawn to the scale indicated. 21 x
FIGURE 6. Diagramis showing relative sizes of molar structures of Calthlon laevis (A)
and Pinotuts carolinus (B) and of helminthl eggs and prlotozoan cysts: r, molar ridges; s, molar
surface composed of tritors; t, cross sectioii of ridges and tritors. 90 x
FIGURE 7. Diagram of a portion of the molar surface with superiilposed outlines of
Ascaris egg (Asc) and Entavmocba histolytica cyst (Ell) with size relative to Calthon laevis
indicated by solid outlines and scale liic (397 x) and size relative to Pintotus carolinus indicated by broken lines (257 x) : a, 1b, e, successively higher frontal sections of tritor-bearing
ridges, with c enlarged to show details of structure. Anterior direction toward right.
FIGURE 8. Stereodiagram of thle structure of the molar surface, with portions of ridges
reimoved at successively higher levels (a, b, c). (Calthon, 397 x; Pinotius, 257 x) Anterior
direction toward lower right.
FIGURE 9. Digestive systemi of Caltlo71 lacvis, in situ within body outliiie. 2.25 x
FIGURE 10. Alimentary tract of Can thon laceis, with ventri-icular coils and Malpighian
tubules spread apart. 2.25 x
FIGURE 11. Pyloric regioni of the alimentary tiact of Canttion latcyis, showing bases of
Malpighian tubules anld a portion of the peritrophiic memblrane which lilnes the tract. 10 x
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'THE JOURNAL OF PARASITOLOGY
744
PLATE I
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An
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a - IS`
oh- ;-c
ob
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-Lb
-mo/
3
Im
R4 t Lf
r,
4^r
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i
Lf
Mo/
I
5
A
I
k
rs
6
t
6O Nec
O
O
'111
I
,
-Asr
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-A-
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In8
0
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&a
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