<oological Journal of the Linnean Society (1988), 94: 319-338. With 4 figures
The relationship between diet and the size
of the midgut caeca in grasshoppers
(Insecta: Orthoptera: Acridoidea)
R. F. CHAPMAN
Department o f Entomological Sciences, University of California, Berkeley,
Calzfornia 94720, U.S.A.
Receixd June 1987, accepted,for publication November I987
A survey of the size and form of the midgut caeca in relation to diet has bern carried out on 173
species from 2 I families and subfamilies of Acridoidea (grasshoppers). Although differences exist in
the size of the anterior caecal arms relative to body length, these differences are not related to the
type of food eaten. Assuming that the anterior arms have a key role in digestive and absorptive
processes, this suggests that different foods make similar demands on these processes. T h e posterior
caecal arms are smaller in graminivorous species than in species eating other types of plants as a
whole or part of their diet. This is true across all the taxa, including those families and subfamilies
that are predominantly forb-feeding. I t is suggested that the posterior caecal arms have a special
role in the detoxification of plant secondary compounds and that the requirement for this is reduced
in graminivorous species because of the lower levels of toxic secondary compounds in grasses. A
specialized pocket region is present in the posterior caecal arms of some forb-feeding species. Its
occurrence across the taxa is spasmodic. It may be concerned with the removal of phenolic
compounds.
KEY WORDS:-Grasshoppers
-
midgut caeca
-
host
plant
relationships - plant
secondary
compounds.
CONTENTS
Introduction . . . . . .
Material and methods . . . .
Results and discussion . . . .
Food of the major taxa
.
.
Size of the anterior caecal arms
Size of the posterior caecal arms
Role of the posterior caecal arms
. . .
The pocket region.
Conclusions . . . . . .
Acknowledgements
. . . .
References.
. . . . . .
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319
320
321
321
326
328
334
335
335
336
336
INTRODUCTION
In all grasshoppers (Acridoidea) the midgut forms six caeca at its junction
with the foregut. Typically each caecum comprises an anterior arm, projecting
forwards alongside the foregut and a posterior arm which projects back from the
0024-4082/88/120319+ 20 $03.00/0
319
0 1988 T h e Linnedn Society of London
320
R F.CHAPMAN
point of origin (Uvarov, 1966). T h e epithelium of the anterior arms is thrown
into a number of longitudinal folds in nearly all the species investigated (Hafez
& Ibrahim, 1960; Hodge, 1936, 1940) and it contributes by far the greater
surface area of midgut epithelium available for the production of digestive
tnzymes and for absorption (Chapman & Brandenburger, unpublished). In
contrast, the epithelium of the posterior arms is not folded and its contribution
to the total midgut epithelium is small. This suggests some functional
differentiation of the two parts and this suggestion is reinforced by obvious
variation in the size of the posterior caecal arms in different species (Uvarov,
1966) and by the presence of a specialized region, called the pocket region, at
the base of the posterior arms in some species (Bernays, 1981). Physiological
studies have already demonstrated the importance of the anterior arms in
absorption ( DOW,1986).
This study examines the size and form of the caeca in relation to feeding
habits for a range of species in different taxa. I n particular, it emphasizes the
differences in the posterior caecal arms between insects feeding on grasses and
those feeding on dicotyledonous plants. The results are discussed in relation to
the necessity of detoxifying plant secondary compounds.
M A I E R I A L AND METHODS
Grasshoppers used in this study were obtained from a number of countries to
cover a wide range of taxa and to ensure that differences observed within tasa
were not local phenomena. Insects were obtained from Australia. Brazil, Costa
Rica, India, Kenya and the United States. Where possible insects were
examined fresh (many specimens from Australia, Costa Rica and United
States); others were examined after fixation. While this adds variability to the
results, no consistent differences were observed as a result of such differences in
the state of the material where comparisons were possible. Consequentl) no
distinctions are made in the following account.
The size of caeca varies with the age of an insect, within an instar (Chapman,
1988), and the degree of food deprivation (Baines, 1979). I t was impossible to
control these variables in collections made by colleagues, but most observations
were made on adults; final instar nymphs were used only if no adults were
available. Whenever possible, a minimum of five adults of each species mas
examined, two of one sex and three of the other. In total, 764 specimens were
examined from 173 species and 21 families or subfamilies of Acridoidea. A
collection of voucher specimens of U.S. material is held in the Entomology
Department at the University of California, Berkeley.
The classification followed is that given by Uvarov (1966) but with
Romaleidae raised to family status and the American Catantopinae treated as in
Amedegnato (1976). Oedipodinae and Acridinae are considered as separate
subfamilies. The species examined are listed in Table 1.
In the examination of each specimen body length from mouth to anu$ was
recorded. This measure was taken, rather than overall body length, because it iq
probably a better measure of gut length than measurements which include
elongate head capsules or subgenital plates. Variability is introduced into any
measure of body length by differences in the degree of distension of the abdomen
due, primarily, to age within the instar and state of sexual maturity in the
DIET AND THE MIDGUT CAECA OF GRASSHOPPERS
32 I
females. I n none of the major taxa, however, was length based entirely on
insects of one sex or age so that this variability will not have introduced a
significant bias into the results. Subsequently the insect was opened from the
ventral surface and the ventral caeca measured in situ. This was done to avoid
the possibility of confusion between dorsal and ventral surfaces. After removal of
the gut from the body the lengths of the dorsal caeca were measured. All caecal
measurements were made under a stereomicroscope to an accuracy of 0.1 mm.
The food plants of the species studied were determined primarily from the
literature.
The following terminology is used: forbivorous-feeding on dicotyledonous
plants; graminivorous-feeding
only on Poaceae; ambivorous-this
term was
coined by Uvarov ( 1 977) for species feeding equally readily on grasses and forbs.
I n the literature such species are commonly called mixed feeders. Mixed feeding
is used here to refer to a family in which some species are graminivorous while
others are not.
Where possible, classification was based on analyses of gut or faecal contents
using the grass/forb index of Mulkern, Toczek & Brusven (1964) and taking a
mean value of the index for all the information available. Since the literature is
extensive only key references are cited. For purposes of this study insects are
classified as forbivorous if the grass/forb index is greater than 50, graminivorous
if it is less than -50 and ambivorous if it is between 50 and -50. Data on
mandibular structure is derived from Isely (1944) for North America species
and from Chapman (1964) for African species. Where information is available
for a genus, but not the species used in this study, it is indicated in italics in
Table 1.
I n the absence of information in the literature, classification of food type is
based on a study of the gut contents and mandibles of the specimens used for
measurements of caeca. Gut contents were classified as grass or forb by
microscopic examination. Mandible structure was determined by comparison
with the illustrations in Chapman (1964) and Isely (1944) and mandibular form
is considered a more reliable measure of the feeding behaviour of a species than
gut contents because only small numbers of insects were examined. The two
features were generally in agreement and never differed to any important
extent. Data derived from current observations are shown bold in Table 1.
Except in the case of North American and some Central American species,
information on the range of foods eaten, within the general categories of
forbivorous and graminivorus, is sparse and widely scattered. Where evidence is
available, species known to feed on one or a restricted range of plants are
indicated; otherwise they are assumed to be polyphagous, feeding on plants from
several families.
RESULTS AND DISCUSSION
Food o f the major taxa
All the Pyrgomorphidae studied, except Colemania sphenarioides, have
forbivorous mandibles. I n C. sphenarioides they approach the ambivorous type.
I n most cases forbs comprise the principal or only food plants, although
Chrotogonus brachypterus also feeds extensively on grasses (Kevan, 1954). The
family is categorized as forbivorous.
322
R . F. CHAPMAN
< .
I A B L E 1. 'l'he species examined and food eaten. F = forbivorous, G = graminivorous.
A = ambivorous, FA= intermediate forbivorous/ambivorous. Italicized letter indicates literature
record for the genus, but not the species. Bold lctter indicates data from current study
I ype of food
-~
Gut,
faecal
analyuis
Mandibular
structure
-~
-
~
t.'
E
Number
rxamincd
FF
FF
A
F
7
I
F
F
F
3
7
G
F
1
F
G
G
F pockrts
G
G
F pockets
F
F t pockets!
A pockrts
3
G
G
G
7
G
1
c;
cG
1
F
F
F:
G
7
2
1
I
6
4
3
2
1
G
c;
G
G
6
F
F
2
F
3
G
.-1
G
F
A
AA
A
A
A pockets
I.
A A pocketa
AF
A porkets
F
FF
E
F
F
FF
F
F
F
.f
~+
F
-
G
F pockets
F pockets
F
F
I.F
FF
F
F pockets'
F
Ff pockcts'
FS pockcts
F
A
G'
4
1
1
4
3
3
4
22
13
9
1
3
1
5
5
3
3
3
5
6
7
2
D I E T AND 1 H E MIDGUT CAECA O F GRASSHOPPERS
323
TABLE
1. Continued
rype of food
Gut/
Macrotona ANIC sp 7 *
Pearatantops impotens (Johnston)
Phaeocalantops neumanni (Ramme)
Phaulacridium vittatum (Sj6stedt)
Melanoplinae
deoloplides minor (Bruner)
tenuipenuis (Scudder)
Daclvlotum pirtum
Dichroplus punctulatus (Thunberg)
Hesperotettix pacifica Scudder
viridb (Thomas)
Lonalcea henachincona
Melanoplus aridus (Scudder)
cinereus Scudder
complanatipes Scudder
devastaior Scudder
d i f k i t i a l i s (Uhler)
insignis
1igneolu.r Scudder
marginatus (Scudder)
sanguinipes (Fab.)
yarrowii (Thomas)
Oedaleonotus borckii (Stilj
Oedomerus corallipes Bruner
Phoetalioles nebrascensis (Thomas)
Poecilotetlix sanguineus Scudder
Proctolabinae
Balarhowsbacris olivacea (Bruner)
Dlymophilacris bimaculata (Rehnj
Leioscapheus sp.
?ela neeavora Deschamps and Rowell
Zosperamerus sp.
Copiocerinae
Copiocera austera (Gerstaecker)
speculnris Gerstaecker
Le p t ysminae
Guetaresia lankesteri Rehn
Stenacris Jissicauda Hebard
Ornmatolampinae
Abracris dilecla Walker
jaziolineata (De Geer)
Leptomerinthoprora breuipennis Rehn
;Clirro@lopteryx fusijormis Rehn
hebardi Rehn
Omalotettix obliquum (Thunbergj
Pseudannzcerus nigrinervzs (Stihl)
Kachirreagra nothra Rehn
Acridinac
Acrida exallata (Walker)
conica Fab.
sp. 1
sp. 2
Colyphosima amplijcata (Johnston)
SP.
(iymnobothroides sp.
faecal
analysis
Mandibular
structure
F
F
F
G
F
F
F
7
2
FF
F F pockets?
F pockets?
F
FF
F
A pockets?
F
F
F
F
AA
F
F
A
4
5
5
1
5
5
~
F
F
I.’
FF
F
F
~
F
F
F
F
F
F
F
F
A
F
-
Number
examined
3
9
5
I
3
5
5
5
5
5
5
10
-~
F pockets?
F
F
G
A
F:
-
F:
F:
F
1
6
F:
(FA)*
(FA)
(FA)
F
1
-
(FA)
2
palm?
palm?
G
G pockets
1
4
Araceae:
G
F
1
5
FF
F
fcrns,
Urticaceae
A
understorey
monocots
F
F
F
G
GG
GG
GG
GG
GG
G
G
F pockets?
A pockets
A pockets
5
5
2
5
1
5
3
10
5
(FA)
Gt
5
F pockets
F pockets
A pockets
4
5
5
GG
GG
GG
GG
GG
GG
G
1
5
7
2
1
1
10
5
324
R. F. CHAPAIAN
I'ARLE
1. Continued
Typc of food
Gut /
faecal
a11a I y si s
-
Mandilxdar
structure
____~
~-
Nunihcr
rxaruincd
~
-.
GG
GG
G
G
GG
G
G
(
;
G
G
F
'1
F
AG
3
1
G
3
A
5
10
E'
A?
A?
A?
F
F
A
4A
G
G
GG
A
G
GG
G
A
A
G
G
G
G
GG
G
G
G
G
F
A
A
A
A
A
G
F
F
G
1A
G
G
F
G
G
G
FF
G
G
G
Ft
F
F
F
F
A
'4
G
G
(
;
A
A
.i G
c;
G
A
1;
F
I.'
I.'
F
I.'
F$
5
5
5
1
1
3
1
1
5
3
5
3
2
7
2
ti
)
4
3
9
5
2
2
3
2
3
9
3
5
2
2
5
4
2
5
2
5
6
2
10
5
3
13
D I E T AND T H E MIDGUT CAECA OF GRASSHOPPERS
325
TABLE
1. Continued
Type of food
Gut/
faecal
analysis
Rrachychrotaphus tl-yxalicerus (Fischer)
Charthippus curtipennis (Harris).
Cibolacris paruiceps (Walker)
Cordillacris crenulata (Bruner)
occipitalis (Thomas)
Eritettix simplex (Scudder)
Eupzgnodes sierranus (Rehn and Hebard)
Heliaula ruja (Scudder)
Horesidotes cinereus Scudder
Lzgurotettix coquilletti McNeill
plnnum (Bruner)
Mermiria bivittata (Serville)
Opeia obscura (Thomas)
Orphulella punciata (De Geer)
Paropomala pallida (Bruner)
wyomzngensis (Thomas)
Phlibostroma quadrimaculatum (Thomas)
Pnorisa squalus Stil
Psoloessa texana Scudder
Siluitettix sp.
Syrbula montezuma (Saussure)
Xeracris snowi (Caudell)
Truxalin ae
Ajrohippus sp.
Phorenula sp.
77uxalii sp.
Mandibular
structure
G
G
F
G
G
G
G
G
A
~-
G
Number
examined
____
2
5
5
A?
5
4
3
5
G
G
4
G
G
F:
F
F
GG
G
GG
G
G
G
G
G
G
G
G
G
G
GG
F
5
9
5
8
4
5
5
2
5
4
5
3
5
5
G
1
GG
1
G
1
F:
G
G
G
G
G
G
~~
G
-
GG
G
G
*code number in the Australian National Insect Collection, Canberra.
tmandibles highly specialized.
$recorded as having a restricted diet breadth.
+ ( ) indicate right and left mandibles of different types on basis of literature.
The two specimens of Usambilla sp. (Lentulidae) examined had forbivorous
mandibles, but one contained finely chewed grass in the gut. Uvarov (1977)
classifies the family as herbivorous ( = forbivorous) and that classification is
retained here.
Amongst the Romaleidae, Epiprora hilaris and Phaeoparia lineaalba had
graminivorous mandibles and grass in the gut. Romalea guttata and Taeniopoda
eques are known to be highly polyphagous (Whitman & Orsak, 1985) while
Tytthole maculata feeds only on Larrea (Otte & Joern, 1977). The family is
classified as of mixed feeding habits.
All the information available on the species of Hemiacridinae,
Tropidopolinae and Oxyinae studied indicates that they are graminivorous,
while the present studies show the single species of Coptacridinae, Calliptaminae
and Euryphiminae to be forbivorous. Uvarov (1977) classifies these last three
families as herbivorous ( = forbivorous).
The Eyprepocnemidinae are ambivorous as species, but the subfamily is
classified here as forb-feeding because none of the species examined is
graminivorous. The Cyrtacanthacridinae are classified as forbivorous although
some species readily eat grasses.
Most of the Catantopinae have forbivorous mandibles and had fragments of
326
R. F. CHAPMAN
forbs in the gut. Data on species other than those used here suggest that they are
generally polyphagous (Joyce, 1952), but the two species of Goniaea have highly
specialized mandibles and probably feed on Eucalyptus (R. Lewis, personal
communication). Both species of Macrotona have graminivorous mandibles and
grass was found in the gut of M . australis. The subfamily is classified as mixed
feeding .
The assessments of food eaten by Melanoplinae are based on extensive
analyses of crop on faecal contents. Important references are Joern, 1985;
Mulkern et al., 1969; Sheldon & Rogers, 1978. Most of the species are
forbivorous and polyphagous with forbivorous mandibles, but some species have
ambivorous mandibles and Phoetaliotes nebrascensis is essentially graminivorous
and refuses most forbs (Pruess, 1969); it has ambivorous mandibles. Because ofthis species the subfamily is classified as mixed feeding. Poecilotettix spp. are
recorded as feeding only on Baccharis (Otte & Joern, 1977).
Three of the Proctolabinae are recorded as specializing on single plant families
by Rowell (1978) with mandibles intermediate in form between forbivorous and
ambivorous. The subfamily is classed as forbivorous. Copiocera spp. (Copiocerinae)
feed on palms (Rowell. 1978) and have mandibles with grinding molar cusps,
similar to those of grass-feeders. Most Leptysminae that have been studied are
graminivorous (Gangwere & Ronderos, 1975) and this appears to be true also o f
Stenacris jissicauda. The single specimen of Guetaresia lankesteri was collected on an
'
epiphytic aroid, on which it is probably a specialist (Rowell, unpublished). C11ve11
this variability the subfamily is classified as mixed feeding.
Most of the Ommatolampinae are forbivorous (Rowell, 1978), but
,%i'icro~ylopley~x
fusformis is ambivorous and M . herbardi feeds on understorey palms,
bronieliads and helioconias. T h e mandibles are either forbivorous or ambivorous
in form except in hi'. herbardi where the molar surfaces form grinding ridges as in
graminivorous species. The subfamily is classed as forb-feeding even though
.\I. herbnrdi feeds on broad-leaved monocotyledons.
The Acridinae studied are exclusively graminivorous. Feeding habits in the
Oedipodinae are very variable. Some, such as Aiolopus thalassinus and
Trachyrhachnys kiowa are exclusively graminivorous with graminivorous
mandibles, others such as Anconia integra and Tropidolophus formosu.~ are
forhivorous, while some species are ambivorous. Major references to feeding
habits are Chapman, 1964; Mulkern p t al., 1962, 1969; Pfadt & Lavigne, 1982.
T h e subfamily is classified as mixed feeding. dnconia inlegra is possibly restricted to
feeding on Atriplex (Otte & Joern, 1977).
Most of the Gomphocerinae feed only on grasses (Mulkern et al., 1962, 1964,
I969), but Cibolacris paruiceps is polyphagous on a range of forbs, the Ligurotettix
species have limited host-plant ranges and Bootettix argentatus feeds only on Larrea
(Otte & Joern, 1977). The subfamily is classified as mixed to accommodate
these species despite the fact that these are exceptions to the general rule of
graminivory. The Truxalinae are exclusively graminivorous.
Size of the anterior caecal arms
The length of the median ventral anterior caecal arm is proportional to the
length of the body, but it is relatively shorter in longer insects (y=O.54+2Ox,
wlierey=length of the caecal arm, x=body length; r=0.84; n=735; P <0.001).
DIET AND T H E MIDGUT CAECA OF GRASSHOPPERS
45
327
I;O
FORBIVOROUS
Pyrgomorphidae
Lentulidae
+-6
+1
i
Coptacridinae
Calliptaminae
+1
1
+
Euryphiminae
4
-+-
Eyprepocnemidinae
Cyrtacanthacridinae
Proctolabinae
Ommatolampinae
-+-5
-+-a
5
8
-+-a
FORBIVOROUS and GRAMINIVOROUS
Romaleidae
r7-ab
Catantopinae
-+-a
Melanoplinae
Leptysminae
-+----a
16
-21+42
Oedipodinae
Gomphocerinae
28
-+-
GRAMlNIVOROUS
Hemiacridinae $Tropidopolinae
Oxyinae
Acridinae
Truxalinae
+-
+1
-+-+-
3
14
3
7
PALM FEEDERS
Copiocerinae
2
-+'
I
05
'
I
,lo
Length of dorsal ardventral arm
Figure 1. Ratio of length of anterior median dorsal caecal arm to anterior median ventral arm.
Mean ( ~ s . D . )for each family and subfamily based on mean values per species. Number above each
mean shows the number of species on which it is based; a; significantly shortrr than Oedipodinae; b,
significantly shorter than Gomphocerinae and Melanoplinae. P < 0.05 Bonkrroni tcst following
ANOVA.
For example, an insect with a body length (mouth to anus) of 10 mm has, on
average, an anterior caecal arm 2.5 mm long; for insects with a body length of
30 mm, the average length of the caecum is 6.5 mm.
Regression equations relating the lengths of the caecum and the body for each
family or subfamily are given in Table 2. These are based on all the individuals
for each taxon, not on mean values for each species, but taxa with less than six
individuals are excluded. Significant differences do occur between taxa, and
Romaleidae, hfelanoplinae and Proctolabinae have, on average, caeca which
are about 1 mm longer than most other taxa over a range of body lengths from
10 to 30 mm. In this table the families and subfamilies are grouped according to
the feeding habits determined in the previous section. Although variation does
occur, particularly in the position of the intercept on the y-axis, there are no
consistent differences between the groups. The possibility that the differences are
related to specific differences in food type cannot be excluded, but seems
unlikely given the wide range of plants eaten by many of the species (see Joern,
1983).
R . k'. CHAPMAN
328
'I'ABLE2. Rrgression equations of the length of the median ventral anterior caecal arm on body
length for each family or subfamily. Based on values for individual insects
Frrding class
_
_
Intercept
Stope
I
23
14
53
15
44
-0.423
1.022
0.344
0.407
0.0 I6
0.22 I
0. I48
0.204
0.256
0.241
0.9588
0.7508
0.7449
0.7899
0.8384
Romaleidae
Catantopinae
Melaiiopliiiac
Leptvsmiriae
Oedipodinae
Comphorerinae
21
65
90
6
I79
I29
0.304
-0.173
I .306
-3.116
0.506
I .494
0.258
0.238
0.201
0.395
0.187
0.166
0.9299
0.8740
0.5680
0.9334
0.8337
0.6663
Hemiacridinae
Oxyinae
Acridinae
6
11
58
-0.596
-0.438
0.058
0.270
0.236
0.202
0.9561
0.9 I24
0.8801
6
-4.408
0.387
0.9208
Fdmily/subfamily
~
~ ____
n
b'm b i l o r u i i \
Pyrgomorphidae
Eyprepocnemidinac
Cyrtacaiithacridin;ir
Proctolabinac
Ommatolampinae
Fiirbii:orous nird ,qroniznii:oro~i.r
Gruminiu~rou.\
l'nlm feeders
Copiorerinae
The six anterior caecal arms of an individual are not all of equal length.
Usually the lengths decrease progressively from ventral to dorsal (Table 3 ,
Fig. 2A). Chapman & Brandenburger (unpublished) observed this pattern in last
instar nymphs of Schistocerca americana. T h e median dorsal arm is nearly always
shorter than all the others, ranging from an average of 0.85 the length of the
median ventral arm in Oedipodinae to about 0.50 of the ventral arm in the
isolated species of Leptysminae and Tropidopolinae which were studied (Fig. 1 .
The average length of the median dorsal arm relative to the median ventral arm is
significantly greater in Oedipodinae than in some other taxa, and in Romaleidae
is significantly shorter than in Melanoplinae and Gomphocerinae (ANOVA,
P = 5.147, d.f. = 20, P<O.OOl, and see Fig. I ) . However, there is no indication
that these differences are related to the type of food eaten by the insects. In seven
species the anterior dorsal arm was slightly less than half the length of the ventral
aims, but this feature is not related to taxonomy or food.
If the anterior caecal arms are the principal site of nutrient absorption, as the
evidence suggests (Chapman & Brandenburger, unpublished; Dow, l986), the
lack of obvious differences in the sizes of the arms in relation to diet may
indicate that different foods do not impose different constraints on the system
with regard to the supply of nutrients. This, despite the fact that the protein
content of grasses tends to be lower than that of herbaceous dicotyledons
(Bernays, 1985).
Size of the posterior caecal arms
'The dorsal posterior caecal arms are often slightly longer than the ventral
ones, the reverse of the position with the anterior arms. This is true in 1 12 of 170
species examined. Mean values for families and subfamilies, based on means for
each species, varied from 0.7 in Hemiacridinae (only two species examined) to
1.4 in Ommatolampinae (eight species), but these differences are not significant
Schistocerca nitens
Abracris jlauolineata
Amphitornus coloradus
Coryphosima sp.
Species
Left
dorsal
0.744k0.067
0.740+_0.098
0.879k0.1 15
0.722+_0.105
No.
of
insects
13
10
10
11
I
0.981 k0.066
1.034k0.055
0.963k0.053
0.992k0.051
1
I
I
Median
ventral
Left
ventral
0.995 0.053
1.013 k 0.092
0.980 f0.102
0.988k0.077
Right
ventral
Length of caecal arm
Median
dorsal
0.667+0.076
0.675 k0.113
0.851 +0.100
0.7 12 k0.088
Right
dorsal
0.749 k0.050
0.655 k0.202
0.882 k0.085
0.728k0.077
TABLE
3. Lengths ( x ~ s . D . of
) the anterior caecal arms relative to the median ventral arm in four representative species
W
N
W
R. I-'. CHAPMAN
330
A
posterior
anterior
-
lmm
ventral
arms
B
/
pocket
region
-
lmm
Imm
Figure 2. Diagrams of the cacca. A, Copiorera spemlaris, showing t h r different Imgths of dorsal a r i d
\ r n t d anterior arms. B, Schisloccrra americana showing thr pockrt region. C, Chorlhzppu, rurlipznnr.5. n
graniinivorous s p r c i r s with short posterior arms.
(ANOVA, F= 1.389, d.f. = 20, P= 0.135). Taken over all 170 species, the
posterior dorsal arm was 1.1 times as long as the posterior ventral arni, and i n
only 10 did the ratio of the lengths of dorsa1:ventral arms exceed 1.5. The
extreme cases were the two species of Micro&lopter_y.x (Ommatolampinae), i n
which the median dorsal arm was about twice as long as the ventral arni
(2.076_+0.612 ( x + s . D . ) in M . Juszformis; 1.795k0.837 in M . hebardi), and
Kinangopajeanneli (Catantopinae) in which the ratio of dorsal : ventral lengths was
3.4.
'The relative lengths of anterior and posterior caecal arms were assessed by
taking a mean value of the ratio posterior: anterior for all six caeca of each
individual and calculating a mean for each species from the individual values.
T h e posterior arms were nearly always shorter than the anterior arms, but the
relative length varied from group to group (Figs 2, 3). In the predominantly
grass-feeding taxa average values for the ratio posterior : anterior arms were less
than 0.4 and in Acridinae, Gomphocerinae and Truxalinae the ratios were
significantly less than in most taxa containing predominantly forb-feeding
species (ANOVA, F=9.889; d.f.=20, P<0.001; see Fig. 3 ) . T h e means for
Oxyinae, Tropidopolinae and Hemiacridinae were similar to those for the othcr
grass-feeders, but did not differ significantly from most forb-feeders, probably
because the number of species examined was low in each case. In taxa
containing some species which are graminivorous and others which are
D I E T AND T H E MIDGUT CAECA OF GRASSHOPPERS
FORBIVOROUS
?
to
0;s
+6
Pyrgomorphidae
+1
Lentulidae
Coptacridinae
b
A
Calliptaminae
Euryphiminae
Eyprepocnemidinae
b
-$-
-+-5
Cyrtacanthacridinae
Proctolabinae
Ommatolampinae
-*-5
+8-
FORBIVOROUS and GRAMINIVOROUS
Romaleidae
Catantopinae
Melanoplinae
7
+-----a
16
+-a
-21+-a
+2
Leptysminae
Oedipodinae
42
-+-a
*-
28
___
Gomphocerinae
GRAMINIVOROUS
Herniacridinae
Tropidopolinae
Oxyinae
Acridinae
Truxalinae
33 1
obcd
--8-ob
1
+a
-$-ab
-+- 14 abd
d-aabde
PALM FEEDERS
Copiocerinae
-+-2
I
0
'
I
05
'
I
I0
Length of posterior arms/anterior arms
Figure 3. Ratio of lengths of posterior caecal arms to anterior caecal arms. Mean ( +s.D.) for each
family and subfamily based on mean values per species. Number above each mean shows the
number of species on which it is based; a, significantly shorter than Ommatolampinae; b,
significantly shorter than Lentulidae; c, significantly shorter than Romaleidae; d, significantly
shorter than Cyrtacanthacridinae, Catantopinae, Melanoplinae, Oedipodinae and Proctolabinae;
e, significantly shorter than Calliptaminae and Euryphiminae. P < 0.05 Ronferroni test following
ANOVA.
forbivorous or ambivorous, the posterior caeca were always small in the
grassfeeders (Fig. 4) and in the Leptysminae the ratio length of
posterior : anterior arms is 1.03 in Guetaresia lankesteri which feeds on epiphytic
Aracea (but note, only one specimen examined) compared with 0.35 in Stenacris
jissicauda, a grass-feeding species (five examined). Conversely in the Gomphocerinae most species with ratios greater than 0.5 are forb feeders (Fig. 4). The
only grass-feeding species in this subfamily with relatively large posterior caeca
(ratio 0.56) is Aulocara elliotti. In Cordillacris crenulala, Opeia obscura and Paropornala spp. no posterior caecal arms are present, while in some other species they
are visible only in some specimens or some caeca. I n these cases they are very
small and sometimes are apparently so contracted that they are not
distinguishable. Posterior caecal arms are also absent from Afrohippus sp.
(Truxalinae).
Amongst the wholly forb-feeding groups the Ommatolampinae have
significantly longer posterior caecal arms than the Pyrgomorphidae. In this
R. F. C HAPMA N
332
,,,Catantopinae
,Melanoplinae
6
0
c
fF
I
'
pomaleidae
," ,o Gomphocerinae
I
0.5
lo
09
1- .t_+
os
-
-
-
-
O
0
'
0
-
.
.
- - -11.22-
-
**
-
-
-
-
- - -
.
'
f
c
I
c
*-•
*
c
I
c -*-*-c
c
-
*
~
Figure 4. Scattergrams of the ratio length of posterior caecal arm: anterior arm for taxa containing
both forbivorous and graminivorous spccies. Species are equally spaced along thc x-axis; their
forb-feeding; 0 ,forb-feeding on one or a limited range of species;
sequence is of no significance. 0,
I&, graminivorous. Numbers refer to anomalous species. They are: 1, Goniaea australa3iae; 2 , Goniaea
cotam; 3, A2i'acrotona australis; 4, Marrotona ANIC sp. 7 ; 5, Hesperotettix paciJira; 6, Hesperotet1i.i rwidis.; 7 .
fhoetaliotes npbrasrensis; 8 , Acrolophitus neaadensis; 9, Cibolacris pariiceps; 10, Eupignodes tierranui; 1 1,
I.iguroletti2 coquilletti: 1 2, Ligurotettix planurn; 13, Bootettzx argentatus: 14, Tytthole maculata; 1 5. Ep@orn
hilarzs; 16, t'hueoparia lineaalba.
subfamily Abracris dilecta and both species of Microtylopteryx have longer posterior
than anterior caecal arms (ratio > 1 .0). The only other species of which this is
true is Usambzlla sp. (Lentulidae), Phymeurus granulatus (Euryphiminae),
Guetaresia lankesteri (Leptysminae) and Hadrotettix trzfasciatus (Oedipodinae).
Conversely only four species have very short posterior arms (ratio < 0.4). These
are Goniaea australasiae, which has highly specialized mandibles and probably
feeds on Eucalyptus, Bootettix argentatus (Gomphocerinae) and TTtthole maculata
(Romaleidae), which are both specialists on Larrea tridentata, and Melanopliu
aridus, which Otte & Joern (1977) record as having a limited host range.
A limited amount of data on the relative lengths of the anterior and posterior
caecal arms can also be obtained from the literature. This is summarized in
Table 4. T h e data is derived almost entirely from drawings in the papers cited.
These suffer the drawbacks that usually only one complete caecum is depicted,
the position (dorsal or ventral) is not specified, and proportions in the drawings
do not always agree with information in the text. Nevertheless, the results are
clearly in agreement with the more extensive body of data in the present
account. I n nearly all the grass-feeding species the posterior caecal arms are less
than half the length of the anterior arms, while they exceed 50°, in most of the
forb-feeders. The only exceptions among the latter are amongst the
Oedipodinae, which commonly include grass in the diet. The exceptional grass-
DIET AND THE MIDGUT CAECA OF GRASSHOPPERS
*
333
334
R. F. CHAPMAN
feeder with relatively long posterior caecal arms is Nomadacris septemfasciata, but
this probably reflects a bias in the data on which the species is classified as
graminivorous. These studies (Chapman, 1957, 1959) were carried out in an
area where grasses dominated; other reports emphasize the polyphagous habit of
the species (Johnston & Buxton, 1949), but because these do not quantify the
amounts of different plants eaten it is not possible to use them in assigning the
insect to a food-plant category.
Role of the posterior caecal arms
These results raise the question why the posterior arms are so poorly
developed or even absent in grass-feeding species. There is no evidence that
feeding on grass involves any difference in terms of digestive enzymes and
absorption. In any case, i t is likely that the posterior arms contribute relatively
little to these functions because of their small surface area (Chapman &
Brandenburger, unpublished). T h e implication is that the processing of forbs in
the gut involves some characteristic which is not required, or is required to a
much lesser extent, in the digestion of grasses.
Graminivorous grasshoppers are very sensitive to a wide array of plant
secondary compounds and host-plant selection by these species is based to a very
large extent on the avoidance of secondary compounds (Bernays & Chapman,
1978). The diversity of secondary compounds is much lower in grasses than
amongst forbs (Bernays & Barbehenn, 1987) with few having any known
toxicity. Phenolics, cyanogenic glycosides and alkaloids may be present in
seedling grasses, but the concentrations of these substances decline as the grass
matures and this is directly linked to an increase in the palatability of the grass
(Bernays & Chapman, 1976; Woodhead & Bernays, 1978). Normally, then,
graminivorous grasshoppers will not eat plants containing high levels of
secondary compounds. Silica, which is sometimes regarded as a secondary
compound, is in a different category because there is no evidence that it has any
chemical effect on grasshoppers, though it may have a mechanical one. In
addition, two experimental studies show that at least some graminivorous
acridids are more sensitive than forb-feeding species to secondary compounds
dnd other toxins given orally. McDonald (1967) tested 23 insecticides against
Melanoplus bivittatus, M . sanguinipes and the grass-feeding Camnula pellucida. The
insecticides were fed to the insects on discs of lettuce. The LD,, was lower for C.
pellucida (i.e. it was more sensitive to the insecticide) in almost every case. There
was no instance in which a compound was much less toxic to C. pellucida than to
the other species. Cottee ( 1984) cannulated various plant secondary compounds
into the midgut of fifth instar nymphs of Locusta migratoria (graminivorous) and
Schzstocerca gregaria (polyphagous). Some of the compounds had no effect on
either species, but nicotine hydrogen tartrate and ally1 isothiocyanate both
caused mortality of L. migratoria, but had no effect on S. gregaria over the same
concentration range. When daily doses of encapsulated sinigrin were given, fifth
instar L. mzgratoria lost weight and died; S. gregaria grew normally.
Thus graminivorous species seem to be poorly equipped to detoxify secondary
compounds and this correlates with poorly developed posterior caecal arms. It is
suggested that the posterior caecal arms have a major role in detoxification and
their weak development or absence in graminivorous species is a consequence of
DIET AND THE MIDGUT CAECA OF GRASSHOPPERS
335
the behavioural avoidance of toxic compounds exhibited by these species.
Several of the food specialists also have relatively short posterior caecal arms.
For example, Goniaea species, which are probably specialists on Eucalyptus have
posterior : anterior caecal arm ratios which are well below average for
Catantopinae (Fig. 4).Amongst the Melanoplinae, Hesperotettix species feed on a
relatively limited range of plants compared with most species (Joern, 1983) and
they have relatively short posterior caeca (Fig. 4). Bootettix argentatus
(Gomphocerinae) and Tytthole maculata (Romaleidae) feed exclusively on Larrea
and both have very short posterior caecal arms (Fig. 4). O n the other hand all
the Proctolabinae, including several species with restricted ranges of food plants,
have relatively long posterior caeca.
T h e pocket region
Bernays (1981) described a region of epithelial pockets in the posterior caecal
arms of Schistocerca gregaria. These pockets are often visible from the outside of the
caeca (Fig. 2B) and their presence was recorded whenever possible. However, a
failure to record them may sometimes have been due to the state of feeding of
the insect or to its state of preservation, so the records obtained may be
conservative.
Pockets were present in most Romaleidae, but not in the grass-feeding species
(Table 1). All Cyrtacanthacridinae examined in this study have a pocket region.
Bernays (1981) recorded that pockets are not present in Anacridium melanorhodon,
but she has kindly re-examined her material and found that they are present.
Pockets were only noted in Tylotropidius gracilipes amongst the
Eyprepocnemidinae. They are not present in most Catantopinae, but do occur
in Goniaea spp. and possibly in Coryphistes ruricola. Finally, they are present in
most, probably all, of the Ommatolampinae examined and in the Copiocera spp.
Many of the species in which caecal pockets are present feed on woody plants
with a high phenolic content, and Bernays (1981) showed that quebracho and
tannic acid accumulate in the caecal pockets. T h e peritrophic membrane lines
the pockets and this lining, together with the contents of the pockets, is passed
out with the faeces a t frequent intervals. I n addition, Bernays (1978) has shown
that the peritrophic membrane is intimately connected with the protection of
the midgut epithelium from tannins and with their removal from the gut. It is
tempting to suggest that the pocket region of the caeca has a special role in the
removal of phenolics from the gut.
The pocket region is included in the length of the posterior caecal arm and in
Ommatolampinae this probably accounts for the unusual length of the arms. I n
other taxa with pockets there is no evidence of a compensatory increase in the
length of the posterior arms and the pockets are developed at the expense of the
unmodified region.
CONCLUSIONS
This survey provides strong circumstantial evidence for a functional
relationship between the size of the posterior caecal arms and food quality. All
species that feed on forbs have long posterior caecal arms, and these are
commonly larger in polyphagous species; in grass feeders the posterior arms are
336
R. F. CHAPMAN
small or absent. It is suggested that detoxification mechanisms are associated
with the posterior arms and these mechanisms allow the insects to feed on plants
that normally contain chemically active secondary compounds, in many cases
permitting the insects to be polyphagous.
There is also evidence that the form of the caeca is highly adaptive.
Primitively, grasshoppers certainly fed on broad-leaved plants since the group is
known to pre-date the evolution of the grasses (Bernays & Chapman, 1978) and
it seems certain that graminivory has arisen independently on a number of
occasions. T h e Hemiacridinae, Tropidopolinae and Oxyinae probably represent
a graminivorous line which is quite separate from the grouping of Oedipodinae,
Acridinae, Gomphocerinae and Truxalinae. T h e graminivorous Romaleidae
certainly represent a third independent line, while in other taxa such as the
Catantopinae and Melanoplinae the occasional grass-feeding species must also
have arisen separately. Yet all of these are characterized by short posterior
caecal arms. Conversely amongst the Gomphocerinae, most species which have
become forbivorous now have longer posterior arms although presumably
derived from forms with short posterior caecal arms. These changes are coupled
with changes in the form of the mandibles, as is evident from Table 1 , and it
appears that these features of the alimentary system will only represent
temporary barriers (in evolutionary time) to host-plant switching.
ACKNOWLEDGEMENTS
Many friends and colleagues helped by collecting and identifying insects for
this study. Without their help it would have been impossible. They are: E. A.
Bernays, H. E. Braker, J. Capinera, C. S. Carbonell, R . J. Cooter, R . Farrow,
N . D. Jago, R . Lewis, K. Milton, D. Rentz, J. M . Ritchie, I. A. D. Robertson,
D. W. Whitman and members of the Department of Entomology, University of
Queensland. Studies in Costa Rica were made possible by the Organization for
Tropical Studies and La Selva Biological Station. Travel within the United
States was assisted by a grant, to Dr E. A. Bernays, from the American
Philosophical Society.
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