Research Article

Journal of Orthoptera Research 2019, 28(2): 145-154

Morphology, developmen, and reproduction of Eyprepocnemis plorans
ibandana (Orthoptera: Acrididae) in South Cameroon rainforests

ALFIERY LAUREL DJOMNANG NKWALA!, FRANKLIN SIMO TALLA2, CHARLY OUMAROU NGouTE2, SEVILOR KEKEUNOU2,
ALAIN CuHrisTeL WAND, MARCELLE MBADJOUN Nzike2, ALAIN SIMEU NouTcHoM2, MPOAME MBIDA!

1 Laboratory of Biology and Applied Ecology, Department of Animal Biology, Faculty of Science, University of Dschang, Cameroon.
2 Laboratory of Zoology, Department of Animal Biology and physiology, Faculty of Science, University of Yaoundé 1, Cameroon.

Corresponding author: Charly Oumarou Ngoute (coumaroungoute@yahoo.fr)

Academic editor: Ludivina Barrientos-Lozano | Received 25 January 2019 | Accepted 26 April 2019 | Published 3 September 2019

http://zoobank.org/E2C87654-0958-402F-8E07-C9BC6735A966

Citation: Nkwala ALD, Talla FS, Ngoute CO, Kekeunou S, Wandji AC, Nzike MM, Noutchom AS, Mbida M (2019) Morphology, development, and
reproduction of Eyprepocnemis plorans ibandana (Orthoptera: Acrididae) in South Cameroon rainforests. Journal of Orthoptera Research 28(2): 145-154.

https://doi.org/10.3897/jor.28.33370

Abstract

Eyprepocnemis plorans ibandana is a very common grasshopper spe-
cies in open environments and agricultural systems of tropical Africa. It
is a pest that significantly benefits from forest degradation in southern
Cameroon, hence the need to study the bioecology of this subspecies. We
studied the reproduction as well as the morphological characteristics and
development times of the post-embryonic instars of E. p. ibandana. Sixty-
one adult pairs were obtained from sixth instar nymphs caught in grassy
vegetation in the Nkolbisson area (Yaoundé) and bred in the laboratory.
After hatching, the first instar nymphs were individually placed in cages
and fed every two days using fresh leaves of Manihot esculenta. The postem-
bryonic development of E. p. ibandana took six instars in the male and six
to seven instars in the female. Mean nymphal development took 79.16
+ 0.51 days in males, 89.93 + 0.58 days in 6 instar females and 94.96 +
1.22 days in 7 instar females. The survival rate of the first instar was low
(53%). However, from the second instar on the survival rate was very high
(> 87%). Sexual dimorphism is distinct in adults, fifth and sixth nymphal
instars. Adults of E. p. ibandana took on average 32.57 + 3.88 days to start
mating, and mating lasted 2.12 h on average (1-3 h). Oviposition took
place on average 52.03 + 5 days after first mating; each female deposited
one to eleven oothecae with an average of 34.93 + 2.37 eggs per ootheca.
Our study provides important information for the control of this subspe-
cies in southern Cameroon.

Keywords

Cameroon, ecology, grasshopper pests, nymphal development

Introduction

Knowledge of an organism’s life cycle is a prerequisite for
any management, control, or conservation action (see Peveling
2001, Zeug et al. 2012). This is particularly the case for locusts and
grasshoppers, some of which are endangered species (Samways et
al. 1995, Samways 1997, Samways and Lockwood 1998), while
other species are important pests (FAO 2010, 2018, Zhang et al.
2019). For the most important pest species, their life cycle is well

known (see Lecoq 1978, Duranton et al. 1982, Gangwere et al.
1997), but some remain largely unstudied despite their economic
importance. This is the case for Eyprepocnemis plorans (Charpen-
tier, 1825), which has been the subject of only rare studies (Jago
1963, Lecog 1980, Hernandez and Presa 1984, Olmo-Vidal 1990,
Schmidt et al. 1996).

Eyprepocnemis plorans — also called Clover or Berseem grass-
hopper — is widely distributed in Africa, southern Europe, and
southwestern Asia, and consists of four geographic subspecies
Jago 1963, Dirsh 1965, Hernandez and Presa 1984, Olmo-Vidal
1990, Schmidt et al. 1996, Cigliano et al. 2018). These include E.
p. plorans (Charpentier, 1825), which occurs in the Mediterranean
and western Asia, E. p. ornatipes (Walker, 1870), which is found in
the Sahelian zone to northern Kenya and southern Arabia, E. p.
meridionalis (Uvarov, 1921), which is distributed in east and south-
eastern Africa and E. p. ibandana Giglio-Tos, 1907, which occurs
in west and central Africa (Dirsh 1965). The latter subspecies is
found in forest and pre-forest areas and has been reported from
Benin, Céte d'Ivoire, Ghana, Guinea, Liberia, Mali, Nigeria, Togo,
South Sudan, Congo, Angola, Uganda, and Cameroon (Mestre
and Chiffaud 2006). E. plorans is usually regarded as a minor pest,
but damage can occasionally be significant, and this species is
regarded as an important polyphagous agricultural pest in some
countries. This is the case in Egypt, especially in oases and along
the Nile (Nakhla 1957, 1976, COPR 1982). In eastern Algeria,
this species consumes potatoes, beans, beets, radishes, and spin-
ach (Harrat and Moussi 2007). It is also present on farmland of
southern Cameroon (Mestre and Chiffaud 2006), where it dam-
ages crops such as cassava, potato, and beans.

Descamps (1953) studied some aspects of the biology of the
species in the Sahelian zone of Cameroon, where the subspecies
E. p. ornatipes is present (Dirsh 1958). Lecog (1980) studied the
life cycle of E. p. ornatipes in the Sudanese zone of West Africa and
identified two generations per year and a period of quiescence at
the imaginal stage during the dry season. In forest regions where
E. p. ibandana occurs, the life cycle of the species has not yet been

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

146 A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJI, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

investigated. This is unfortunate not only because of the species’
increasing ravaging activities facilitated by forest degradation in
southern Cameroon, but also because of data on the life cycles of
different subspecies across various eco-geographical regions in the
world (Jago 1963, Lecog 1980, Hernandez and Presa 1984, Olmo-
Vidal 1990, Schmidt et al. 1996).

In the Sahelian zone, this species is found throughout the year
as both nymphs and adults (Lecog 1988). In Spain, there is only
one generation per year, from July to March (Hernandez and Presa
1984). Schmidt et al. (1996) bred up to four generations per year
in the laboratory of E. p. plorans from Sardinia. They observed six
post-embryonic nymphal instars in the male and seven instars in
the female (mean development time 25 + 9 days) without any
diapause. In E. p. meridionalis from Tanzania, Jago (1963) found
seven instars in the male and seven to eight in the female. How-
ever, data on the life cycle, reproductive biology, and nymphal de-
velopment of E. p. ibandana are lacking. This study aimed to col-
lect these data; specifically, we aimed (1) to determine the number
and duration of nymphal instars of E. p. ibandana, (2) to mor-
phologically describe each instar, (3) to study the survival rates of
these different instars, and (4) to study the reproductive behavior
of E. p. ibandana in southern Cameroon.

Methods

Study area.—The individuals raised in the laboratory were caught
between August 2014 and March 2017 at Nkolbisson, Yaoundé.
Yaoundé is located in a semi-deciduous forest area, but the natural
vegetation is highly degraded because of anthropic activity. The
region is characterized by alternating hills and swamps (Bachelier
1959). The climate is of Guinean equatorial type with four sea-
sons: a short rainy season (mid-March to June), a short dry season
July and August), a long rainy season (September to mid-Novem-
ber), and a short dry season (from mid-November to mid-March).
The rainfall is about 1,600 mm per year and temperature varies
from 19° to 33°C (Suchel 1987).

Sampling.—Adults of E. p. ibandana (n = 61 adult pairs) used in
this study were obtained from sixth instar nymphs collected on
grass vegetation at Nkolbisson using a sweep net. Nymphs were
transported to the laboratory in cylindrical polypropylene plastic
boxes (type 1 cages: 9 cm high and 13 cm in diameter) closed
with a wire mesh lid. In the laboratory, these nymphs were reared
individually in the same type 1 cages on a shelf.

Meteorological data collection in the laboratory.—Temperature and
relative humidity (RH) in the laboratory were recorded daily dur-
ing the experiment (morning, afternoon, and evening) with a Got-
tingen Thermohygrograph. The temperature and RH during the
breeding period are provided in Fig. 1.

Reproduction.—After the final molt of the specimens collected in
the field, the adults were paired in 15 wire cages (type 2 cages: 11
cm high and 10 cm in diameter) closed by a mesh cover. Each cage
was one third filled with heat-sterilized wet sand, serving as an
oviposition medium. Observations were conducted every two days
to record pre-mating, mating, oviposition, and hatching dates.

Post-embryonic development.—First instar nymphs obtained from
each adult pair were counted and placed individually in type 1
cages, then kept on shelves for development monitoring. A dry
stem of Chromolaena odorata (14 cm long) was placed in each cage

Humidity (%) m=Temperature (°C)

g [s)
& 100 50 &
90 45
80 40
70 35
-_ 60 30 oO
= ry
= 950 25 5
so 2
E (oD)
5 40 20 2
x= o

IE
30 15
20 10
10 5
0) 0
NY @ x SS
SS Sc < “S » eS
\y \ oO S)
Y @ + ye @
« ee

Fig. 1. Variation in temperature and relative humidity from Janu-
ary to September 2017. Laboratory of Zoology Faculty of Science
University of Yaoundé 1.

to support molting of the nymphs. Each cage was labeled with
hatching date, number, stage, and sex. Each nymph was fed every
two days with a cassava leaf (Manihot esculenta). The presence of
exuviae was recorded daily and the state (dead or alive) of the
nymphs was noted. The cages were also cleaned and the leaves
used as food were renewed.

Morphology and morphometrics.—The morphology and morphom-
etry of E. p. ibandana were recorded from freshly dead individuals
during rearing. The morphological characteristics were observed
using a Heerbrugg binocular lens. For each developmental instar,
measurements were made and, for paired structures, the right
structure was measured and their shape and color were described.
The following parameters were measured as described by De Gré-
gorio (1987) and Default (2012): Total body length (Lt): from the
tip of the fastigium to the tip of the abdomen, measured in lateral
view; length of cephalic capsule (Lcc): length of head from the tip
of the fastigium to the most posterior part of the head, measured
in dorsal view; width of cephalic capsule (Icc): head width includ-
ing compound eyes, measured in dorsal view; length of thorax
(Lth): from the anterior to posterior margin of pronotum; length
of abdomen (Labd): from posterior margin of pronotum to tip
of abdomen, measured in lateral view; length of pronotum (Lpr):
along midline, measured in dorsal view; length of antenna (La):
from the scape to the apex of the last segment of flagellum; num-
ber of antennal articles (Na) in the flagellum; length of tegmina
(Lel): from the insertion point to the apex of tegmen, measured
in dorsal view; length of hind wing (Lai): from the insertion point
to the apex of wing, measured in dorsal view; length of hind fe-
mur (Lcul): maximum length of hind femur; length of median
femur (Lcu2): maximum length of median femur; length of an-
terior femur (Lcu3): maximum length of anterior femur; length
of hind tibia (Ltil): maximum length of hind tibia; length of mid
tibia (Lti2): maximum length of mid tibia; length of anterior tib-
ia (Lti3): maximum length of anterior tibia; number of external
spines on hind tibia (Nse).

Drawings were made with the same magnifying glass in a light
chamber and at 25-50X magnification.

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJL, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

Data analysis.—Data were analyzed using Excel (version 2016) and
PAST (version 2.5) softwares. Excel was used to draw the different
curves; PAST was used to calculate averages of development times
and morphometric parameters. The averages were compared with the
Kruskal-Wallis and Mann Whitney tests at the 5% significance level.

Results

Number of instars and duration of postembryonic development.—In the
laboratory, nymphal development of E. p. ibandana went through
six instars in males and six (75% of females) to seven (25% of fe-
males) instars in females (Table 1). The average total development
time differed significantly (p < 0.0001) between the sexes: 79.16 +
0.51 (54 to 124 days) in the males, 89.93 + 0.58 (67 to 131 days)
in six-instar females, and 94.96 + 1.22 (67 to 161 days) in seven-
instar females (Table 1). From the fifth nymphal instar onwards,
average development times differed significantly (p<0.0001) from
one instar to another (Table 1).

Nymphal survival rate. —We obtained 2,603 hatchlings, 793 (30.46%)
of which reached the adult stage. The transition from the first instar
(L1) to the second (L2) was marked by a very high mortality rate
(47%), but from the L2 instar on the survival rate was high, with
values between 87% and 92% (Fig. 2), resulting in a linear decreas-
ing number of individuals from L2 to the adult stage (Fig. 2).

Reproduction: courtship, mating, and oviposition.—Courtship began
32.47 + 3.88 days (8 to 59 days) after the final molt, by contact of
the palps and antennae between both sexes. The male clung to her
pronotum; when the latter was not receptive, the male remained
on her back (this could last more than 2 hours). In some cases, the
female used her hind legs to prevent the male from clinging to her.
When the female was receptive, the male clung to her pronotum
with his prothoracic and mesothoracic legs, the metathoracic legs
being free and folded. In this position, the male bent his abdomen
about 180° to the left or right below that of the female in order
to bring the two genital regions into contact. He then introduced
his phallus between the genital valves of the female to the vaginal
opening. The coupling (n = 61) lasted for 2.12 h on average (be-
tween 1 and 3 hours) if uninterrupted.

After pairing, the first ootheca was deposited 9 to 70 days later
(average 52.03 + 5 days). Females laid between 1 to 11 egg pods
(average 3 + 1.4) and the number of eggs per ootheca ranged from
14 to 50 (34.93 + 2.37 on average). On average, the females took
52.02 + 5.1 days for laying of the first pod, 73.23 + 6.84 days for
the second pod, and 101.3 + 10.31 days for the third pod.

147
Morphology of the different developmental stages. —

Egg: The eggs of E. p. ibandana are 3 to 5.5 mm long (average 4.37
+ 0.44 mm) and 1 to 1.5 mm in diameter (average 1.00 + 0.05
mm). The eggs have a yellowish color, an elongated shape, are
slightly curved and with rounded ends.

Adults: The general body color is of a variable brown, sometimes
light beige, or brown-gray. The eyes are streaked with a small
black band highlighting the sub-ocular suture. The pronotal disc
is flat, with weakly pronounced lateral carina that are blurred in
the metazona; the posterior border is slightly angular. The prono-
tal disc has two light bands running along the lateral carina and
surrounding a dark brown zone; the dark zone narrows towards
the anterior and posterior margins; the prosternal process is cylin-
drical. The elytra and wings are fully developed, slightly shorter,
reaching or extending beyond the posterior apex of the abdomen
and bearing a beige longitudinal stripe in the median field. The
lower outer half of the posterior femora is usually yellow or light
beige, lighter than the upper half. The basal half of the posterior
tibiae is blue, the apical half reddish with whitish spines and black
apices. The posterior tarsi are red.

Males are 21 to 27 mm long (average 24.33 + 1.60 mm). The
head is between 5 and 7 mm (average 6.30 + 0.67 mm) long; the

Survival rates (%)

L1 L6 Adult

Instars
Fig. 2. Survival rate of the nymphal instars of E. p. ibandana in the

laboratory. Solid line: % survival of each instar; broken line: % of
all nymphs still surviving. LI-L6 = nymphal instars 1-6.

Table 1. Eyprepocnemis plorans ibandana, male and female nymphal instars average development time (mean + standard error in days),
under laboratory conditions. Number of specimens: 388 males, 325 six instar females, 143 seven instar females.

Sexes Instars Kruskal Wallis Test Total

L1 Nymph L2 Nymph L3 Nymph L4 Nymph L5 Nymph L6 Nymph L7Nymph HValue P Value duration
Males
Duration 12.22+0.13* 11.324+0.17>48 =11.534+0.17>%8 12.6440.19% 13.5+40.20% 18+0.28% - 517 <0.0001 79.16+40.514
Range (4-28) (4-24) (2-33) (6-38) (6-46) (6-38) (54-124)
Females of six instars
Duration 12.78+0.17% 11.70+0.19>4 12.1040.22% 13.7240.25% 14.92+0.31% 24.72+0.48% - 249.4 <0.0001 89.93+0.583
Range (6-26) (4-28) (4-27) (4-33) (2-48) (9-51) (67-131)
Females of seven instars
Duration 12+0.27248 10.81+0.24>8 11.19+0.30°8 12.74+0.40% 13+0.34% 14.2740.42© 20.52+0.634 260.9 <0.0001 94.9641.22©
Range (6-26) (2-21) (2-27) (4-33) (5-32) (4-37) (5-56) (67-161)

Notes: Values in table indicate: mean + standard error (Min-—Max). Legend
zontally.

: Uppercase letters compare values vertically; lowercase letters compare values hori-

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

148 A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, $. KEKEUNOU, A.C. WANDJI, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

sone
<3 gi eae oe ff

Fig. 4. Eyprepocnemis plorans ibandana, female, from Ongot, Cam-
Fig. 3. Eyprepocnemis plorans ibandana, male from Ongot, Cameroon. eroon.

instar 1

instar 2

instar 3 \ Fike

lmm.
instar 4 = \ SSS =} Female of 7 instars : ae TiLBe See
vA instar 5
1mm
(intermediary instar)
Male and female of 6 instars ee

instar 5

Imm.

I

instar 6

adult adult

Fig. 5. Eyprepocnemis plorans ibandana, postembryonic development of pronotum and wings (lateral view). Pro: pronotum; Wbs: Wing buds.

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJL, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

instar 2

instar |

instar 4 :
instar 6

Fig. 6. Eyprepocnemis plorans ibandana, postembryonic develop-
ment of males’ external genitalia (ventral view). Ceq: cerci, Ep:
epiproct, Pap: paraproct, Psg: subgenital plate, 8 stn: sternite 8, 9
stn: sternite 9.

eyes bear six longitudinal eye stripes; the antenna carries 24 ar-
ticles, measures 9.90 to 10 mm (average 9.99 + 0.03 mm) and
reaches dorsally almost the posterior margin of the pronotum.
The thorax measures 6 to 9 mm (average 7.72 + 0.98 mm); the
pronotal disc measures between 4 and 5 mm (average 4.81 + 0.37
mm). The abdomen is 11 to 14 mm long (average 12.74 + 0.84
mm); the sub-genital plate is conical with acute apex (Figs 3, 5, 6
and Table 2).

Females that passed through six nymphal instars have a body
of 29.80 to 41.70 mm (average 35.86 + 2.94 mm) long. The head
measures 7.10 to 10 mm (average 8.45 + 0.65 mm); the antenna
carries 24 to 25 articles, measures between 9.30 and 12 mm (aver-
age 10.74 + 0.73 mm), and reaches dorsally almost the posterior
margin of the pronotum. The eyes bear six clearly visible longi-
tudinal eye stripes. The thorax measures between 9 and 12 mm
(average 10.44 + 0.77 mm). The pronotal disc is between 5.50 and
7 mm (average 6.35 + 0.49 mm) long. The abdomen measures
between 17 and 27.50 mm (average 21.79 + 2.7 mm). The genital
valves are very robust and slightly curved towards the rear. The
posterior margin of sternite 8 is undulating without a median pro-
cess (Figs 4, 5, 7 and Table 2).

Females that passed through seven nymphal instars are not sig-
nificantly different in size than females that have passed through six
instars (Table 2), but they are distinctive in having an eye with seven
clearly visible longitudinal eye stripes; the pronotal disc has in its
middle part a clearly visible median dark band, surrounded by two
clearly visible pale beige lateral carinae and the posterior margin of
sternite 8 carries a small median process (Figs 5, 7, and Table 2).

149

instar |

instar 2

instar 3
instar 4 F'6

instar 5 F7
intermediary instar

instar 5 F6
instar 4 F7

instar 6 F7 instar 7 F7
adult F6 aay

Fig. 7. Eyprepocnemis plorans ibandana, postembryonic develop-
ment of females’ external genitalia (ventral view). Ceq: cerci, Ep:
epiproct, Pap: paraproct, Vad: dorsal valve, Vav: ventral valve, 9
stn: sternite 9, F6: female of six instars, F7: female of seven instars.

— 40
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L1 L2 L3 L4 L5 L6 L7/A6 A7
—@—Male —O—Female6 ++*@+++Female7

Fig. 8. Eyprepocnemis plorans ibandana, increase in body size under
laboratory conditions. L= nymph; A= adult.

Common characteristics of the nymphal instars. —The body is usually
dark brown in color with spots and light beige bands. The head is
weakly conical, dark brown in color with a beige band behind each
compound eye, extending onto the anterior border of the prono-
tum. The fastigium is trapezoid in shape with a slight mid and
concave longitudinal depression; it is brown, with a midlength
pale beige band extending over the pronotum to the posterior
end of the abdomen. The face is light beige with brown spots; the
frontal ridge is concave with two more or less parallel longitudi-
nal carinae reaching the base of the mouthparts. The pronotum is
cylindrical in shape, weakly roof-like, bearing three brown sutures

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

150 A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S$. KEKEUNOU, A.C. WANDJI, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

Table 2. Eyprepocnemis plorans ibandana, male and female measurements of morphological characters.

Instars Sex/type Lt Lec Icc Lth Labd Lpr La Na
L1 Male 5.0140.63 2.01+0.14 1.264+0.12 1.83+0.26 2.12+40.29 0.98+0.06 1.7040.23 11400 (11-11)
(3.20-6.00) — (1.30-2.20) — (1.00-1.50) —(1.20-2.50) = (1.40-2.60) ——- (0.80-1.10) _—(1.10--2.10) (32) A
(32) A (32) A (32) A (32) A (32) A (32) A (32) A
Female 5.19+0.78 2.10+0.17 1.29+0.16 1.7340.34 2.49+0.60 0.984+0.04 1.7740.16 10.63+40.49
(3.80-6.90) (2.00-2.90) — (1.00-1.50 = (1.00-2.10) —-(1.70-3.90) — (0.90-1.00) _—-(1.40-2.10) (10-11) (30) A
(30) A (30) A (30) A (30) A (30) A (30) A (30) AB
L2 Male 7.3540.83 2.3140.18 1.8340.13 2.29+0.28 3.96+0.56 1.29+0.12 2.1640.13 15+00 (15-15)
(5.90-8.80) (2.10-2.90) —(1.50-2.00) _—(1.90-3.00) — (2.50-5.00) —- (1.10-1.70) _—(1.90-2.50) (30) B
(30) B (30) AB (30) B (30) B (30) B (30) B (30) B
Female 7.7640.73 2.48+0.28 1.94+0.08 2.45+0.25 4.05+0.47 1.394+0.12 2.28+0.18 15+00 (15-15)
(6.50-9.30) (1.30-2.80) (1.80-2.00) —_ (2.00-3.00) —_ (3.00-5.00) —-(1.20-1.60) — (2.00-2.60) (30) B
(30) B (30) B (30) B (30) B (30) B (30) B (30) B
L3 Male 10.58+0.76 3.18+0.15 2.17+40.09 3.29+0.26 5.7640.52 1.94+0.08 3.07+0.09 16.8740.34
(9.00-12.00) (2.90-3.50) — (2.00-2.30) — (2.80-4.00) —_ (5.00-7.00) —_ (1.80-2.00) —_ (2.90-3.30) (16-17) (30) C
(30) C (30) C (30) BC (30) C (30) C (30) C (30) C
Female 10.46+0.72 3.21+0.16 2.19+0.07 3.3440.28 5.69+0.52 1.9740.05 3.0540.12 16.7140.46
(9.00-11.50) (3.00-3.50) —- (2.10-2.30) —- (2.80-3.80) (4.60-6.40) _—_ (1.80-2.00) — (2.80-3.30) (16-17) (28) C
(28) C (28) C (28) C (28) C (28)-G (28) C (28) C
L4 Male 11.7141.76 3.7740.29 2.7940.34 3.60+0.39 6.30+0.88 2.3540.24 3.7840.30 19.06+40.36
(10.1-14.00) (3.30-4.60) — (2.40-3.90) —- (3.00-4.50) — (5.20-8.00) — (2.00-3.10) — (3.20-4.50) + (18-20) (30) D
(30) C (30) D (30) D (30) C (30) C (30) D (30) D
Female 12.10+1.38 3.8540.37 2.7540.28 3.73+0.46 6.47+0.74 2.4140.34 3.8440.47 19.03+40.18
(9.40-15.00) (3.00-4.90) — (2.00-3.20) — (2.80-4.70) —_ (5.00-8.10) —(1.90-3.00) —_(2.90-5.00) (19-20) (30) D
(SIE (31) D (31):.D (31) CD (BIR ES (31) D (31) D
L5 Male 14.40+1.56 4.40+0.27 3.09+0.11 4.09+0.41 8.0441.34 3.16+0.09 4.91+0.27 21.09+0.68
(12.1-18.00) (4.00-5.00) — (3.00-3.30) —- (3.50-5.00) (6.10-11.00) _—_ (3.00-3.30) —- (4.20-5.30) (20-22) (33) E
(33) D (33).E (33) E (33) DE (33) D (33)E (33) E
Female 6 17.340.95 5.50+0.41 3.8740.21 4.93+0.26 9.814+0.60 4.04+0.16 6.09+0.65 21.00+00 (21-
(16.00-18.3) (4.90-6.00) (3.50-4.00) — (4.30-5.10) — (9.20-10.60) — (3.70-4.20) —_ (5.00-7.40) 21) (23) E
(23) E (23) F (23) F (23) F (23)E (23) F (23) F
Female 7 16.05+1.65 4.58+0.45 3.30+0.26 4.264+0.84 9.44+1.07 3.12+0.15 4.64+0.30 21.00+00 (21-
(14.5-18.00) (4.10-5.10) — (3.00-3.60) —— (3.30-5.10) — (8.40-10.70) — (3.00-3.30) — (4.30-5.00) 21) (20) E
(20) E (20) E (20) E (20) E (20) E (20) E (20) E
Lo Male 17.2041.36 5.01+0.16 3.6240.28 5.27+0.39 9.44+1.19 3.9640.23 6.23+0.42 23.00+00
(15.0-19.2) (4.80-5.50) — (3.20-4.00) —- (4.80-6.00) —-(7.50-11.00) — (3.50-4.30) — (5.50-7.00) (23-23) (36) F
(36) E (36)G (36)G (36) F (36) E (36) F (36) F
Female 6 25.17+2.00 7.1840.53 5.04+0.46 7.09+0.57 13.8841.94 5.74+0.40 8.7640.95 23.00+00
(21.0-27.0) (6.50-8.00) — (4.20-5.50) — (6.00-7.70) —- (11.0-16.0) —_(5.10-6.10) —- (7.30-10.00) (23-23) (30) F
(30) F (30) H (30) H (30) G (30) F (30) G (30) GH
Female 7 25.80+0.54 6.93+0.26 5.52+0.52 7.1040.25 15.15+0.39 5.98+0.16 8.44+0.88 23.00+00
(25.2-26.7) (6.50-7.30) — (5.00-6.10) — (6.70-7.50) — (14.8-16.00) (5.70-6.20) — (7.00-10.00) (23-23) (32) F
(32) F (32) H (32) I (32) G (32) G (32) H (32) G
L7 Female 7 25.614+2.13 6.93+0.23 4.94+0.31 7.15+0.49 15.3141.52 5.9740.22 9.02+0.88 24.00+00
(21.0-27.0) (6.50-7.20) — (4.30-5.30) — (6.10-7.50) —-(12.0-16.3) — (5.50-6.20) —_ (7.30-10.00) (24-24) (38) G
(38) F (38) H (38) H (38) G (38) G (38) GH (38) H
Adult Male 24.33+1.60 6.3040.67 3.9940.33 7124098 12.74+0.84 4.8140.37 9.99+0.03 24.00+00
(21.0-27.0) (5.00-7.00) — (3.90-4.00) (6.00-9.00) _—- (11.0-14.0) — (4.00-5.00) —_ (9.90-10.00) (24-24) (25) G
(25) F (25) I (25) F (25) 44 (25) F (25) I (25) 1
Female 6 35.864+2.94 8.45+0.65 5.42+0.36 10.44+0.77 21.7942.79 6.3540.49 10.74+40.73 24.05+0.23
(29.8-41.7) (7.10-10.0) (5.00-6.00) _(9.00-12.00) —_ (17.0-27.5) (5.5-7.0) (36) J (9.30-12.00) (24-25) (36) G
(36) G (36) J (36) I (36) I (36)H (36) J
Female 7 35.78+4.40 8.36+40.42 5.43+0.37 10.69+1.01 23.1743.94 6.3640.47 10.52+0.63 24.23+0.43
(30.0-44.0) (8.0-9.20) —_(5.00-6.00) _—_ (9.00-13.00) —_(17.0-29.00) (5.7-7.0) (26)J (9.0-11.0) (24-25) (26) G
26)G 26) J 26) I 26) B 26) I 26) J

Notes: Each value of the table represents: mean and standard error (min- max) (sample size). Within columns, means with same letters are not sig-
nificantly different. Legend: Lt: length of body. Lec: length of cephalic capsule. Icc: width of cephalic capsule. Lth: length of thorax. Labd: length of ab-
domen. Lpr: length of pronotum. La: length of antenna. Na: Number of antennal articles. Lel: length of elytra. Lai: length of the hind wing. Lcul, Lcu2
and Lcu3: length of femur 1, length of femur 2, length of femur 3. Ltil, Lti2, Lti3: length of tibia 1, length of tibia 2, length of tibia 3. Nse: Number of
external spines on hind tibia. L= nymphal instars.

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJL, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

Table 2. Continued. Eyprepocnemis plorans ibandana, male and female measurements of morphological characters.

151

Instars Sex/type Lel Lail Leul Lcu2 Lcu3 Ltil Lti2 Lti3 Nse
Ll Male - - 0.98+0.04 1.06+0.06 3.05+40.09 0.99+0.03 1.09+0.17 2.96+0.13 1.00+0.00
(0.9-1.00) (0.90-1.10) (2.70-3.20) (0.90-1.00) (1.00-2.00) (2.40-3.10) (1.00-1.00)
(32) A (32) A (32) A (32) A (32) A (32) A (32) A
Female - - 0.99+0.04 1.08+0.06 3.07+0.11 0.98+0.04 1.06+0.06 2.94+0.10 1.00+0.00
(0.90-1.10) (0.90-1.20) (2.90-3.30) (0.90-1.00) (0.90-1.20) (2.70-3.00) (1.00-1.00)
(30) A (30) A (30) A (30) A (30) A (30) A (30) A
L2 Male - - 1.12+0.06 1.26+0.09 4.04+0.18 1.13+0.06 1.30+0.10 3.7540.19 2.00+0.00
(1.00-1.30) (1.10-1.50) (3.60-4.30) (1.00-1.30) (1.10-1.50) (3.10-3.90) — (2.00-2.00)
(30) A (30) AB (30) B (30) AB (30) B (30) B (30) B
Female - - 1.17+0.09 1.36+0.16 4.3140.25 1.1540.08 1.3540.12 3.92+0.22 2.00+0.00
(1.00-1.40) (1.10-1.70) (3.60-4.80) (1.00-1.30) (1.20-1.60) (3.40-4.30) (2.00-2.00)
(30) A (30) B (30) B (30) B (30) B (30) B (30) B
L3 Male - - 1.69+0.08 1.8540.16 5.6440.32 1.63+0.14 1.85+40.13 4.70+0.30 3.00+0.00
(1.60-1.90) (1.20-2.00) (5.10-6.10) (1.40-1.90) (1.50-2.00) (4.10-5.80) (3.00-3.00)
(30) B (30) C (30) C (30) C (30) C (30) C GB0)'E
Female - - 1.70+0.11 1.91+0.09 5.71+0.22 1.61+0.11 1.90+0.10 4.77+0.17 3.00+0.00
(1.50-2.00) (1.70-2.00) (5.40-6.20) (1.40-1.90) (1.70-2.00) (4.30-5.20) (3.00-3.00)
(28) B (28) C (28) C (28) C (28) C (28) C (28) C
L4 Male - - 2.02+0.15 2.17+0.26 7.24+0.66 2.01+0.21 2.274+0.24 5.8740.44 4.00+0.00
(1.80-2.50) (1.90-3.00) (6.20-9.00) (1.80-2.50) (2.00-2.90) (5.10-7.10) (4.00-4.00)
(30) C (30) CD (30) E (30) D (30) D (30) D (30) D
Female - - 2.04+0.19 2.16+0.28 7.33+0.86 1.96+0.18 2.35+40.29 6.0740.57 4.00+0.00
(1.70-2.70) (1.60-3.10) (5.40-9.20) (1.60-2.30) (2.00-3.00) (4.70-7.50) (4.00-4.00)
GIBES (31) D (31) E (31) D (1) (31) D (31) D
L5 Male 2.11+0.13 2.32+0.22 2.5240.36 2.8540.18 9.31+0.75 2.49+0.24 3.13+0.29 7.49+0.40 5.00+0.00
(1.90-2.30) (2.10-2.70) (1.90-3.00) (2.50-3.00) (8.30-11.10) (2.20-2.90) (3.00-4.00) (6.70-8.00) (5.00-5.00)
(33) A (33) A (33) D (33)E (33) F (33)E (33)E (33) E (33) E
Female6 2.82+0.27 3.04+0.22 3.08+0.17 3.5140.32 12.14+0.77 3.03+0.23 3.97+0.23 9.58+0.58 5.00+0.00
(2.30-3.00) (2.50-3.20) (2.80-3.30) (3.00-3.90) (10.90-12.9) (2.70-3.50) (3.40-4.20) (8.80-10.10) (5.00-5.00)
(23) A (23) A (23) E (23) F (23)G (23) F (23)e (23) F (23) E
Female7 1.25+0.19 1.19+0.10 2.61+0.26 2.86+0.24 9.50+0.64 2.51+40.24 3.0540.27 7.614+0.58 5.00+0.00
(1.20-1.30) (1.10-1.30) (2.20-2.90) (2.60-3.10) (8.50-10.20) (2.00-2.70) (2.50-3.30) (7.00-8.30) (5.00-5.00)
(20) A (20) B (20) D (20) E (20) F (20) E (20) E (20) E (20) E
L6 Male 5.55+0.68 4.90+0.48 3.13+0.19 3.67+0.31 11.58+0.76 3.10+0.24 3.88+0.20 8.93+40.59 6.00+0.00
(4.00-7.00) (4.10-6.00) (3.00-3.70) (3.10-4.00) (10.3-13.1) (2.90-4.00) (3.50-4.20) (8.00-10.00) (6.00-6.00)
(36) B (36) C (36) E (36) F (36)G (36) F (36) F (36)G (36) F
Female6 8.014+1.64 9.44+1.07 4.23+0.60 4.69+0.46 16.63+0.99 4.12+0.10 5.15+0.08 13.14+0.88 6.00+0.00
(5.20-9.50) (8.40-10.70) (3.20-4.80) (4.00-5.10) (15.0-18.0) (4.00-4.10) (5.00-5.20) (11.5-14.00) (6.00-6.00)
(30) C (30) D (30) F (30) G (30) H (30) GH (30) GH (30) H (30) F
Female7 8.10+0.18 7.09+0.58 4.57+40.14 5.16+0.19 16.87+0.90 4.18+0.14 5.23+0.20 13.19+0.81 6.00+0.00
(7.90-8.40) (6.10-8.00) (4.30-4.70) (5.00-5.50) (15.2-18.00) (4.00-4.40) (5.00-5.50) (12.0-14.0) (6.00-6.00)
(32)'C (32).) (32) F (32) H (32) H (32)G (32) G (32) I (32) F
L7 Female 7 8.10+0.77 7.15+40.51 4.44+0.34 4.90+0.40 16.83+1.06 4.12+0.08 5.15+0.11 12.36+0.45 7.00+0.00
(7.00-10.80) (6.20-8.00) (4.00-5.00) (4.00-5.20) (15.0-18.0) (4.00-4.20) (5.00-5.30) (11.6-13.20) (7.00-7.00)
(38) C (38) D (38) F (38) GH (38) H (38) GH (38) GH (38) J (38) G
Adult Male 20.2241.57 18.294+1.62 4.92+0.39 5.59+0.39 14.66+0.91 3.98+0.28 4.98+0.22 12.31+0.61 6.00+0.00
(17.0-23.0) (15.3-21.0) (4.00-5.70) (5.00-6.00) (13.0-16.0) (3.00-4.90) (4.50-5.90) (11.0-13.0) (6.00-6.00)
(25) D (25)E (25)G (25) I (25) I (25) H (25) H (25) J (25) F
Female 6 28.35+42.05 26.07+2.23 5.45+40.41 6.34+0.44 20.83+0.39 5.01+0.18 6.75+0.45 16.39+0.89 6.00+0.00
(23.5-32.00) (21.5-30.0) (5.00-6.00) (5.50-7.00) (17.0-26.5) (4.60-5.50) (6.00-7.30) (15.0-18.1) (6.00-6.00)
(36)E (36) F (36) H (36) I (36) J (36) I (36) I (36) K (36) F
Female 7 28.06+2.63 25.61+2.74 5.48+40.37 6.36+0.44 20.88+1.82 5.23+0.33 6.56+0.33 16.7541.11 7.00+7.00
(24.0-32.0) (21.5-30.0) (5.00-6.00) (6.00-7.10) (17.0-23.2) (4.90-6.00) (4.90-6.00) (14.9-18.6) (7.00-7.00)
26)E 26) F 26) H 26 26) J 26) J 26) I 26) K 36)S

Notes: Each value of the table represents: mean and standard error (min- max) (sample size). Within columns, means with same letters are not sig-
nificantly different. Legend: Lt: length of body. Lec: length of cephalic capsule. Icc: width of cephalic capsule. Lth: length of thorax. Labd: length of ab-
domen. Lpr: length of pronotum. La: length of antenna. Na: Number of antennal articles. Lel: length of elytra. Lai: length of the hind wing. Lcul, Lcu2
and Lcu3: length of femur 1, length of femur 2, length of femur 3. Ltil, Lti2, Lti3: length of tibia 1, length of tibia 2, length of tibia 3. Nse: Number of
external spines on hind tibia. L= nymphal instars.

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

152 A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJI, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

dotted with beige spots forming the median carina. The mesoster-
nal space is open, much wider than long, with rounded lobes. The
elytra are absent. The abdomen has ten segments visible dorsally
and nine visible ventrally. The cerci are conical with an acute apex
slightly exceeding the epiproct. The epiproct is triangular, bifur-
cated and with a rounded apex dorsally beyond the paraprocts
(Figs 5-7 and Table 2).

Identification key for post-embryonic instars. —Refer to the key of Jago
(1963) on Eyprepocnemis plorans meridionalis.

Sexual dimorphism.—We observed a clear sexual dimorphism
from 5“ nymphal instar to adults. At these instars, the length of
body, head, thorax, abdomen, pronotum, antennae, elytra, wings,
femora, and metathoracic tibiae are larger in females than in males.

Growth rate.—The growth rate was similar for both sexes from
the first nymphal instar to the fourth. Starting from 5" instar, the
growth of males became slower than that of the two types of fe-
males (six and seven instar females). At the sixth nymphal instar,
six instars females increased faster in size than seven instar fe-
males, but as the latter passed through an additional instar, there
was no significant difference between the sizes of the two types of
adult females (Fig. 8).

Discussion

Postembryonic development of E. p. ibandana.—Our study showed
that the number of instars varies between the two sexes in E. p.
ibandana: six in the male and six or seven in the female, confirming
the results obtained by Jago (1963) for E. p. meridionalis, Hernan-
dez and Presa (1984) in Spain for E. p. plorans, and Schmidt et al.
(1996) in Sardinia. In southern Cameroon, the nymphal develop-
ment of three pyrgromorphid grasshoppers (Zonocerus variegatus,
Pyrgomorpha vignaudii, Taphronota ferruginae) has been studied pre-
viously (Kekeunou 2007, Kekeunou et al. 2015, Kekeunou et al.
2018), all of which had a fixed number of six instars in both sexes.
On the other hand, a variable number of instars is well known for
many Orthoptera species (Uvarov 1966).

The tropical grasshopper Cornops aquaticum may have five to
seven nymphal instars depending on the host plant, humidity,
and its distribution range from Mexico to Argentina (Adis and
Wolfgang 2003, Adis et al. 2004). This could be explained by the
genetic and environmental indices that are known to be factors
affecting growth rates and number of nymphal instars in Orthop-
tera (Hochkirch and Gréning 2008). This means that females
can maximize their fitness by reaching a larger adult body size,
which allows them to produce more eggs, while males can maxi-
mize their lifetime reproductive success through multiple mating
for a relatively short period of time (Sai-Keung 1973, Shine 1989,
Hochkirch and Groéning 2008). This is due to the differences in
activity patterns of the molting glands, corpora allata, and corpora
cardiaca between the sexes. Indeed, molt and metamorphosis in
hexapods depend on the circulating peak of ecdysone and juvenile
hormone in both sexes (Joly 1968).

From our results, the nymphal development of E. p. ibandana
was longer than in Jago’s (1963) study on E. p. meridionalis, which
obtained for the male and the female 55.3 and 59.45 days, respec-
tively. These differences may be explained by the different rear-
ing conditions of both studies. Jago (1963) reared his material in
the laboratory (approximately 25°C) in UK, while our study was
done in Cameroon in semi-outdoor rearing conditions subject to

natural variations in temperature. Differences in temperature are
an important reason for the differences observed: our work better
reflected field conditions and our results may be closer to what
happens in nature than in the laboratory study of Jago (1963). The
duration of development is strongly influenced by temperature in
all insects (Ratte 1984) as well as by the host plants, e.g., Hal-
ouane (1997) and Ould El Hadj et al. (2004) found, respectively,
41 and 43.58 days for nymph development of S. gregaria on cab-
bage, while Ghidaoui (1990) and Ouchene (1995) found, respec-
tively, 61.22 and 29.6 days on lemon and cabbage plus grass. An
additional factor influencing development is the size of the cages.
Kaufmann (1965) has shown that the life cycle of Z. variegatus is
shorter in large cages than in smaller cages.

Nymphal survival rate.—The survival rate of the first nymphal in-
star was quite low in our study compared to the later instars. This
lower survival of first instars in the laboratory and in nature is
common in other grasshoppers and locusts, e.g., desert locust,
Australian plague locust (Dhouib 1994, Seddik 1994, Symmons
and Cressman 2001, Ould El Hadj et al. 2004). This reflects a
high sensitivity of first nymphal instar that is related to varia-
tions in environmental conditions and possibly the monospe-
cific diet they were subjected to in the laboratory. Indeed, E. p.
ibandana is a species of mesophilic environments with a poly-
phagous diet in the field (Blanchet 2009). According to Kekeu-
nou et al. (2018), the high mortality of young nymphs could
be explained by problems such as inadequate watering, molting,
and nutrition. In our study the nymphs were fed with leaves of a
single food plant; the nature of this monospecific diet may have
affected nymphal development.

Reproduction of E. p. ibandana.—The mating of E. p. ibandana is sim-
ilar to that observed in most other short-horned grasshoppers (Du-
ranton and Lecog 1990, Symmons and Cressman 2001, Dushimiri-
mana et al. 2012), including also some species from Cameroon
such as T: ferruginea (Kekeunou et al. 2018), P. vignaudii (Kekeunou
et al. 2015), and Z. variegatus (Kekeunou 2007). Mating started on
average 32.47 days after the final molt. This result differs from those
obtained by Kekeunou et al. (2018) on T. ferruginea and Kekeunou
et al. (2015) on P. vignaudii, who assessed the time between fledging
and first mating at 42.47 days and 12.7 days, respectively. These dif-
ferences could be explained not only by the time required for each
species to reach sexual maturity, but also by the time needed to find
favorable ecological conditions, adequate temperature and humid-
ity, and availability of food (Duranton and Lecoqg 1990).

We found that a female of E. p. ibandana lays between one and
eleven oothecae during her adult life-span. The number of eggs
per egg pod ranged from 14 to 50. In the laboratory, S. gregaria
females produce a mean of 22 pods, each containing 47.6 eggs
(Wang and Sehnal 2002), which suggests that they produce a total
of 1,050 eggs during their entire reproductive life (Dushimirimana
et al. 2012). For the same species, Norris (1952) reports 5-9 pods
(each pod contained 10 to 140 eggs), while Popov (1958) found
no more than 2 or 3 egg-pods for each female. In nature, Chap-
man et al. (1986) observed 17-77 eggs per ootheca in Z. variega-
tus, but only 6.5 eggs on average by Miramella alpina feeding on
Vaccinium myrtillus and V. uliginosum (Asshoff and Hattenschwiler
2005). These differences could be explained by the fact that the
number of eggs per ootheca depends on the environmental condi-
tions in which the insects live (Joly 1968), as well as the number
of ovarioles of each ovary (Chiffaud and Mestre 1990). Whitman
(2008) and Ackman and Whitman (2008) have also shown that a

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S. KEKEUNOU, A.C. WANDJL, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

number of other factors, such as the length of the pre-oviposition
period and the number of females participating in reproduction,
also influence the reproductive capacity of a population.

Sexual dimorphism in E. p. ibandana.—Sexual dimorphism is
marked in adults, as well as in 5" and 6" nymphal instar of E. p.
ibandana. These results corroborate those of Hochkirch and Gron-
ing (2008) who state that in 99% of Caelifera, adult females are
larger than males. The larger size of the females probably reflects
the need for egg production (Duranton and Lecog 1990).

Two major hypotheses have been proposed to explain the ulti-
mate causes of dimensional dimorphism: the intersexual competition
hypothesis and the differential equilibrium hypothesis (Hochkirch
and Gréning 2008). The first suggests that sexual dimorphism is a
mechanism to reduce intra-specific competition, allowing the sexes
to specialize in different foods. The differential equilibrium hypoth-
esis proposes that different body sizes represent fitness optima of spe-
cific sexual shapes, which are caused by their specific life history strat-
egies. Females can maximize their reproductive success by increasing
the number (or size) of eggs (selection of fecundity), while males can
maximize their reproduction by being more mobile and fertilizing
many females in a short time (Hochkirch and Groning 2008).

Conclusion

Under laboratory conditions, nymphal development of E. p.
ibandana fed on cassava went through six instars in males and six
(75%) or seven (25%) instars in females. The average development
time in days was 79.16 in males and 89.93 to 94.96 in females. Fifth
and sixth nymphal instars showed slightly longer development
times. The survival rate of the first nymphal instar was low in our
study compared to the later instars. Data on instar recognition and
development times are useful for treatment programs by providing
information on what stage the grasshoppers are at and how much
time is left for treatment before the more damaging adult stage. It
also gives an idea of how quickly treatments need to be performed
to reduce nymphal populations in the field and reduce damage.

Acknowledgements

The Theodore J. Cohn Research Grant 2016 of the Orthopter-
ists’ Society funded this work. We also thank members of the Plant
Protection Service, Cameroon (2PC) who helped in data collec-
tion in the laboratory.

References

Ackman O, Whitman DW (2008) Analysis of body size and fecundity in
a grasshopper. Journal of Orthoptera Research 17: 249-257. https://
doi.org/10.1665/1082-6467-17.2.249

Adis J, Lhano M, Hill M, Wolfgang JJ, Marques MI, Oberholzer H (2004)
What determines the number of juvenile instars in the tropical grass-
hopper Cornops aquaticum (Leptysminae: Acrididae: Orthoptera)?
Studies on Neotropical Fauna and Environment 39: 127-132. htt-
ps://doi.org/10.1080/01650520412331271729

Adis J, Wolfgang JJ (2003) Feeding impact and bionomics of the grasshop-
per Cornops aquaticum on the water hyacinth Eichhornia crassipes in cen-
tral Amazonian floodplains. Studies on Neopropical Fauna and Envi-
ronment 38: 245-249. https://doi.org/10.1076/snfe.38.3.245.28167

Asshoff R, Hattenschwiler S (2005) Growth and reproduction of the alpine
grasshopper Miramella alpina feeding on CO,-enriched dwarf shrubs
at treeline. Oecologia 142: 191-201. https://doi.org/10.1007/s00442-
004-1714-0

153

Bachelier G (1959) Etude pédologique des sols de Yaoundé. Contribution
a l'étude de la pédogénése des sols ferrallitiques. Agronomie Tropi-
cale 14: 280-305.

Blanchet E (2009) Développement des marqueurs moléculaires chez
les Orthoptéres: application a l'étude du genre Calliptamus. Théses
de Doctorat, Montpellier, France: Université Montpellier HI - Paul
Valéry.

Chapman RF, Page WW, McCaffery AR (1986) Bionomics of the variegated
grasshopper (Zonocerus variegatus) in West & Central Africa. African
Journal of Biotechnology 33: 479-505. https://doi.org/10.1146/an-
nurev.en.31.010186.002403

Chiffaud J, Mestre J (1990) Le Criquet puant Zonocerus variegatus (Linne,
1758). Essai de synthése bibliographique. CIRAD-PRIFAS, 140 pp.

Cigliano MM, Braun H, Eades DC, Otte D (2018) Orthoptera Species File.
Version 5.0/5.0. http://Orthoptera.SpeciesFile.org

COPR (1982) The Locust and Grasshopper Agricultural Manual. Centre
for Overseas Pest Research, London.

De Grégorio R (1987) Zonocerus variegatus (Orthoptera, Pyrgomorphidae):
caractéristiques morphologiques et biométriques des larves des popu-
lations des saisons séche et humide. Bulletin de la société d’histoire
naturelle de Toulouse 123: 29-44.

Default B (2012) Biométrie des types des Caeliféres de France (Orthop-
tera). 1. Définition des paramétres mesurés. 2. Mensurations chez
les Tridactylidae, Tetrigidae, Pyrgomorphidae, Pamphagidae et
Acrididae Calliptaminae. Matériaux Orthoptériques et Entomocé-
notiques 17: 21-56.

Descamps M (1953) Observations relatives au criquet migrateur africain
et A quelques autres espéces d’Acrididae du Nord Cameroun. Agrono-
mie Tropicale 8: 567-613.

Dhouib S (1994) Action de quelques substrats alimentaires sur la crois-
sance, le développement et la structure de la cuticule chez le criquet
pélerin Schistocerca gregaria (Forskal, 1775) (Orthoptera Acrididae).
Mémoire d’ingénieur agronome, Ouargla, Algeria: Institut National
de Formation Agronomique Saharienne.

Dirsh VM (1958) Synonymic and taxonomic notes on Acrididea (Orthop-
tera). Revista Espafiola de Entomologia. Eos 34: 25-32.

Dirsh VM (1965) The African Genera of Acridoidea. Anti-locust Research
Centre, London, 578 pp.

Duranton JE, Launois M, Launois-Luong MH, Lecog M (1982) Acridiens
(Orthopteres). In: Appert J, Deuse J (Eds) Les ravageurs des cultures
vivriéres et maraichéres sous les tropiques. Maisonneuve et Larose,
Paris, and ACCT, 61-74.

Duranton JF, Lecog M (1990) Le criquet pélerin au Sahel. Collection Acri-
dologie Opérationnelle n° 6, Comité Inter-Etats de Lutte contre la
Sécheresse dans le Sahel, Département de Formation en Protection
des végétaux, Niamey, and CIRAD/PRIFAS, Montpellier, 178 pp.

Dushimirimana S, Hance T, Damiens D (2012) Comparison of repro-
ductive traits of regular and irradiated male desert locust Schistocer-
ca gregaria (Orthoptera: Acrididae): Evidence of last-male sperm
precedence. Biology Open 1: 232-236. https://doi.org/10.1242/
bio.2012323

FAO (2010) Locust watch: Locusts in Caucasus and Central Asia. Food and
Agriculture Organization of the United Nations. http://www.fao.org/
ag/locusts-CCA/en/index.htm]

FAO (2018) Locust watch: Desert locust. Updated June 4. Food and Agri-
cultural Organization of the United Nations. http://www.fao.org/ag/
locusts/en/info/info/index.html

Gangwere SK, Muralirangan MC, Muralirangan M (1997) The Bionomics
of Grasshoppers, Katydids and their Kin. CAB International, Walling-
ford, UK, 83-101.

Ghidaoui H (1990) Elevage du criquet pélerin Schistocerca gregaria (For-
skal, 1775) et impact de divers substrats alimentaires sur la reproduc-
tion. Mémoire, ISH, Sousse, Tunisia, 44 pp.

Halouane F (1997) Cycle biologique de Schistocerca gregaria (Forskal,
1775) et de Locusta migratoria (Linné, 1758) (Orthoptera, Acrididae).
Efficacité de Metarhizium anisopliae (Meth) (Hyphomycetes, Deutero-
mycotina) et effet sur quelques paramétres physiologiques de Schis-
tocerca gregaria. Mémoire, INA, El Harrach, Algeria, 237 pp.

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)

154 A.L.D. NKWALA, ES. TALLA, C.O. NGOUTE, S$. KEKEUNOU, A.C. WANDJI, M.M. NZIKE, A.S. NOUTCHOM AND M. MBIDA

Harrat A, Moussi A (2007) Inventaire de la faune acridienne dans deux
biotopes de I’Est Algérien. Sciences & Technologie 26: 99-105.

Hernandez F, Presa JJ (1984) Sobre la biologia de Eyprepocnemis plorans
(Charpentier, 1825) (Orthoptera: Acrididae), en la huerta de Murcia
(S.E. Espana). Boletin de Sanidad Vegetal. Plagas 10: 245-249.

Hochkirch A, Groéning J (2008) Sexual size dimorphism in Orthop-
tera. Journal of Orthoptera Research 17: 189-196. https://doi.
org/10.1665/1082-6467-17.2.189

Jago ND (1963) Some observations on the life cycle of Eyprepocnemis plorans
meridionalis Uvarov, 1921, with a key for the separation of nymphs at
any instar. Proceedings of the Entomological Society of London, 38:
113-124. https://doi.org/10.1111/j.1365-3032.1963.tb00765.x

Joly P (1968) Endocrinologie des Insectes. Masson & Cie, Paris, 344 pp.

Kaufmann T (1965) Observations on the aggregation, migration and
feeding habits of Zonocerus variegatus in Ghana. Annals of the Ento-
mological Society of America 58: 791-801. https://doi.org/10.1093/
aesa/58.4.426

Kekeunou S (2007) Influence des différents types de végétations de jachéres
sur les populations de Zonocerus variegatus (Linné, 1758) (Orthoptera:
Pyrgomorphidae) dans la zone de forét humide du Sud-Cameroun.
Thése de doctorat, Département de Biologie Animale de la Faculté des
Sciences de l'Université de Yaoundé 1, Cameroun, 197 pp.

Kekeunou S, Mbeng D, Oumarou Ngoute C, Wandji AC (2015) Morpholo-
gy, development and reproduction of Pyrgomorpha vignaudii (Orthop-
tera: Pyrgomorphidae). Entomological Research 45: 58-70. https://
doi.org/10.1111/1748-5967.12097

Kekeunou S, Wandji AC, Oumarou Ngoute C (2018) Morphology, post-
embryonic development and reproduction of Taphronota ferruginea
(Fabricius, 1781) (Orthoptera: Pyrgomorphidae). Tropical Zoology
31: 68-84. https://doi.org/10.1080/03946975.2018. 1445686

Lecoq M (1978) Biologie et dynamique d’un peuplement acridien de zone
soudanienne en Afrique de l'Ouest (Orthoptera, Acrididae). Annales
de la Société Entomologique de France (NS) 14: 606-681.

Lecoq M (1980) Biologie et dynamique d’un peuplement acridien de zone
soudanienne en Afrique de l'Ouest (Orthoptera, Acrididae). Note
complémentaire. Annales de la Société Entomologique de France
(N.S.) 16: 49-73. http://agritrop.cirad.fr/390863

Lecoq M (1988) Les criquets du Sahel. Collection Acridologie Opération-
nelle n° 1, Comité Inter-Etats de Lutte contre la Sécheresse dans le Sa-
hel, Département de Formation en Protection des végétaux, Niamey,
and CIRAD/PRIFAS, Montpellier, 129 pp.

Mestre J, Chiffaud J (2006) Catalogue et atlas des acridiens de l'Afrique
de l'Ouest. J. Mestre & J. Chiffaud-Mestre, Groléjac, France, 350 pp.

Nakhla NB (1957) The life-history, habits and control of the bersim grass-
hopper, Eyprepocnemis plorans Charp., in Egypt (Orthoptera: Acridi-
dae). Bulletin de la Societé Entomologique d’Egypte 41: 411-427.

Nakhla NB (1976) The population density of the Berseem grasshopper, Ey-
prepocnemis plorans plorans Charp., as related to environment and con-
trol [in Egypt Arab Republic]. Plant Production and Protection Div.
Report N° FAO-AGP--DL/TS/16; EAO-AGP--INT/71/030, FAO, Rome.

Norris MJ (1952) Reproduction in the desert locust (Schistocerca gregaria
Forskal) in relation to density and phase. Anti-Locust Bulletin 13:
1-51.

Olmo-Vidal JM (1990) Atlas of the Orthoptera of Catalonia. Atlas of Bio-
diversity 1: 337-458.

Ouchene D (1995) Quelques aspects biologiques de Schistocerca gregaria
(Forskal, 1775) (Orthoptera, Acrididae) dans la région de Tamanrasset
et en conditions contrélées. Mémoire, INA, El Harrach, Algeria, 85 pp.

Ould El Hadj MD, Tankari Dan-Badjo A, Halouane F (2004) Etude du
cycle biologique de Schistocerca gregaria (Forskal, 1775) sur chou
(Brassica oleracea) en laboratoire. Université Mohamed Khider, Biskra,
Algeria, Courrier du Savoir 5: 17-21.

Peveling R (2001) Environmental conservation and locust control - pos-
sible conflicts and solutions. Journal of Orthoptera Research 10:
171-187. https://doi.org/10.1665/1082-6467(2001)010[0171:ECAL
CPI2.0 CO?

Popov GB (1958) Note on the frequency and the rate of oviposition in
swarms of the Desert Locust (Schistocerca gregaria Forskal). Entomolo-
gist’s Monthly Magazine 94: 176-180.

Ratte HT (1984) Temperature and Insect Development. Environmental
Physiology and Biochemistry of Insects. Springer, Heidelberg, Berlin,
304 pp. http://link.spriger.com/content/pdf/10.1007%2F978-3-642-
70020-Opdf

Sai-Keung L (1973) The postembryonic development of Atractomorpha sin-
ensis Bolivar with particular reference to the phallic structures (Or-
thoptera: Acridoide: Pyrgomorphidae). Master of Science, McGill
University Montreal, 179 pp.

Samways MJ (1997) Conservation biology of Orthoptera. In: Gangwere
SK, Muralirangan MC, Muralirangan M (Eds) Bionomics of Grass-
hoppers, Katydids and their Kin. CAB International, Wallingford,
481-496.

Samways MJ, Lockwood JA (1998) Orthoptera conservation: Pests and
paradoxes. Journal of Insect Conservation 2: 143-149. https://doi.
org/10.1023/A:1009652016332

Samways MJ, Stork NE, Cracraft J, Eeley HAC, Foster M, Lund G, Hilton-
Taylor C (1995) Scales, planning and approaches to inventorying and
monitoring. In: Heywood VH, Watson RT (Eds) Global Biodiversity
Assessment. United Nations Environment Programme, Cambridge
University Press, Cambridge, 517-475.

Schmidt GH, Friedel K, Rembold H (1996) Studies on the size of corpora
allata, the juvenile hormone III titre in the haemolymph and growth
of terminal oocytes throughout three consecutive gonadotropic cycles
in Eyprepocnemis plorans (Orthopteroidea: Caelifera: Acrididae). Euro-
pean Journal of Entomology 93: 131-144.

Seddik A (1994) Développement ovarien et charge alaire du criquet péler-
in : Schistocerca gregaria (Forskal, 1775) (Orthoptera-Acrididae) et du
criquet migrateur : Locusta migratoria cinerascens Bonnet et Finot, 1889
(Orthoptera-Acrididae) a Adrar. Cycle biologique du criquet pélerin
au laboratoire. Mémoire, INA, El Harrach, 141 pp.

Shine R (1989) Ecological causes for the evolution of sexual dimorphism:
A review of the evidence. Quarterly Review of Biology 64: 419-461.
https://doi.org/10.1086/416458

Suchel JB (1987) Les climats du Cameroun. Les climats du Cameroun.
Thése de doctorat d'état, Bordeaux, Université de Bordeaux III, France.

Symmons PM, Cressman K (2001) Desert Locust Guideline. Biology and
Behaviour. Food and Agriculture Organization of the United Nations,
Rome 25pp.

Uvarov BP (1966) Grasshoppers and Locusts. University Press, Cambridge,
481 pp.

Wang F, Sehnal F (2002) Ecdysteroid agonist RH-2485 injected into Schis-
tocerca gregaria (Orthoptera: Acrididae) females accelerates oviposi-
tion and enhances ecdysteroid content in eggs. Applied Entomology
and Zoology 37: 409-414. https://doi.org/10.1303/aez.2002.409

Whitman DW (2008) The significance of body size in the Orthoptera:
A review. Journal of Orthoptera Research 17: 117-134. https://doi.
org/10.1665/1082-6467-17.2.117

Zeug SC, Bergman PS, Cavallo BJ, Jones KS (2012) Application of a life cy-
cle simulation model to evaluate impacts of water management and
conservation actions on an endangered population of Chinook salm-
on. Environmental Modeling and Assessment 17: 455-467. https://
doi.org/10.1007/s10666-012-9306-6

Zhang L, Lecog M, Latchininsky A, Hunter D (2019) Locust and grasshop-
per management. Annual Review of Entomology 64: 15-34. https://
doi.org/10.1146/annurev-ento-011118-112500

JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)