Research Article

Journal of Orthoptera Research 2020, 29(1): 35-39

Mating behavior of the Persian boxer mantid, Holapftilon brevipugilis

(Mantodea: Mantidae)

MAHMOOD KOLNEGARI!

1 Department of Entomology, Islamic Azad University of Arak, Markazi Province, Iran.

Corresponding author: Mahmood Kolnegari (mahkolnegari@yahoo.com)

Academic editor: Matan Shelomi | Received 21 June 2019 | Accepted 7 July 2019 | Published 13 March 2020

http://zoobank.org/5F48711 C-1B2D-421 F-826E-CO7AE90CB62D

Citation: Kolnegari M (2020) Mating behavior of the Persian boxer mantid, Holaptilon brevipugilis (Mantodea: Mantidae). Journal of Orthoptera

Research 29(1): 35-39. https://doi.org/10.3897/jor.29.37595

Abstract

The Persian boxer mantid, Holaptilon brevipugilis, is the mantid most
recently described from Iran. Here, I present some aspects of the courtship
display and mating behavior of this species. I conducted 28 mating trials,
quantified the relative frequency of all mating behaviors, and estimated
the pre-copulation, copulation, and post-copulation periods. I also com-
pared the effects of frontal vs. lateral approaches of the male for mating
success, since frontal approach increases the risk that the male will be seen
and cannibalized by the female. In 64% of trials, the male approached
the female immediately, regardless of whether the female could see him
or not. Copulation was successful in 61% of trials. Male courtship con-
sisted of dorsoventral bending of the male’s abdomen and occurred in
10% of all trials, but only when the female was facing the male. In contrast,
trembling of the forelimbs was not associated with copulation, occurred in
10% of all trials, and was always followed by the male moving away from
the female. I observed one female cannibalizing a male post-copulation.
The Persian boxer mantid might be sexually cannibalistic, but confirming
this hypothesis would require further studies, including a focus on female
hunger level as a determining factor in sexual cannibalism and in male
courtship behaviors.

Keywords

courtship, deimatic behavior, experiment, forelimb trembling, Iran, sexual
cannibalism

Introduction

Descriptions of courtship displays and their prevalence are rela-
tively rare for Mantodea (Battiston 2008). The mating behavior of
mantids can be divided into two main categories: male-originated
mating behavior, or courtship; and female-originated mating be-
havior, or sexual cannibalism. These two types are interconnected.
A higher likelihood of sexual cannibalism can increase the rate of
courtship and, consequently, courting decreases the probability of
sexual cannibalism (Maxwell 1998, Lelito and Brown 2006, Barry
et al. 2008b, Jayaweera et al. 2015, Kadoi et al. 2017). The struc-
ture of courtship and the frequency of sexual cannibalism were the
subjects of a few research studies (Edmunds 1975, Loxton 1979,

Liske and Davis 1987, Battiston 2008). Male-originated courtship
often includes movement of body parts when approaching the fe-
male. Some of these courtship movements include “boxing” of the
prothoracic legs by Oxypilus hamatus Roy (Edmunds 1975), “sema-
phore” and “stamping” with the metathoracic legs by Ephestiasula
amoena (Bolivar) (Loxton 1979) and Acontiothespis multicolor (Sau-
ssure) (Quesnel 1967), “pumping” and “weaving” of the abdomen
by Tenodera aridifolia sinensis (Saussure) (Liske and Davis 1987), and
“trembling” by Oligonyx insularis Bonfils (Bonfils 1967). Female at-
tacks on a male can occur before, during, and after copulation (Le-
lito and Brown 2006, Jayaweera et al. 2015). The frequency of sexual
cannibalism differs from one species to another (Maxwell 1999)
and can be affected by factors such as female hunger levels and the
approach direction of the males (Maxwell 1998, Barry et al. 2008a).

In this study, I focused on courtship and sexual cannibalism
in a recently described mantid species, Holaptilon brevipugilis Kol-
negari, or the Persian boxer mantid. H. brevipugilis belongs to a
rare genus, having just one identified congeneric species with a
small distribution range (Beier 1964, Abu-Dannoun and Katbeh-
Bader 2007, Kolnegari and Vafaei-shoushtari 2018). This wingless
species, which was recently discovered in the center of Iran, is one
of the smallest mantids in the world with a body size range of
1.2-1.6 cm (Roy 1999, Kolnegari and Vafaei-shoushtari 2018).
The name of the species comes from the occasional trembling
movement of its oversized grasping forelimbs. Such behavior was
observed in both males and females, though it is apparently more
frequent in males (Kolnegari and Vafaei-shoushtari 2018). The be-
havior was observed in the laboratory mostly during encounters
with other individuals (different- or same-sex), and rarely arose
before hunting prey (e.g., housefly). In addition, numerous males
and females were observed performing characteristic forelimb
movement during specimen collection from their wild habitat,
but this behavior was not associated with escape from collectors
nor encounters with other mantids or prey.

The main question of this study is whether foreleg trembling
has a determinative function in the mating process of the mantid
as a possible courtship display (Bonfils 1967, Edmunds 1975, Bat-
tiston 2008). Additional questions include whether or not, and
how frequently, female-originated sexual cannibalism occurs in

JOURNAL OF ORTHOPTERA RESEARCH 2020, 29(1)

36

boxer mantids. Elucidating the behavioral complexities of mating
in this species could help to inform the systematic position and
evolutionary history of this rare genus.

Materials and methods

I collected adult individuals of Holaptilon brevipugilis from their
only known habitat around Arak City, Iran, during June-July 2017.
I collected 28 males and 28 females and reared them on a diet of
one small housefly (Musca domestica) three times a week. Animals
were kept individually within well-ventilated, 30-cm-diameter
opaque plastic containers in the laboratory, at a temperature of
20-22°C. The same conditions were used for 28 staged mating tri-
als that allowed an observation of general male mating behavior.
I paid particular attention to behaviors such as courtship display,
approach pattern, jumping distance, male mating success, and
copulation duration.

Habitat structure, particularly the type of flora, can impact
mating behavior based on the objects the mantids are situated on
(Younes 2007, Battiston 2008). The boxer mantid in the wild re-
sides in a stony habitat covered with low vegetation. Fortunately, I
was able to easily rebuild this environment in the laboratory. Fol-
lowing Liske and Davis (1987), I illuminated the mating arena in
an otherwise darkened room. This enabled me to observe the be-
haviors without disturbing or stressing the mantids. Since hungry
females are more likely to cannibalize males than well-fed females
(Liske and Davis 1987, Hurd et al. 1994, Kadoi et al. 2017), I pro-
vided a satiating diet for females. Experimental pairs were ran-
domly chosen for copulation three hours after feeding; therefore,
females were not hungry during the mating experiments. Pairs
were excluded after each trial, so each pair was used only once.

Approximately 30 min after the initial introduction of a fe-
male, a male was placed into the container at least 20 cm away
from the female. If an interaction did not occur within three hours,
the trial was terminated. Alternatively, if courtship and copulation
occurred, then the male approach conditions and duration of
mating were recorded. I examined the effects of two orientations
of encounter on courtship behavior according to previous stud-
ies (Lelito and Brown 2006, Barry et al. 2008b, Battiston 2008).
The approach orientations were ‘frontal’, where males approached
the female from the front and faced her within her visual field
of not more than 80°, and ‘lateral’, where the male approached
from completely outside the female’s visual field towards the rear
of the female. These were established by placing the male in the
container either in front of or laterally and somewhat behind the
female. For each approach orientation, 14 trials were carried out.

I used a Canon SX240HS digital camera to record all trials, and
a professional camera, Canon 7D (Mark 2), to take high-resolution
photos of any notable behaviors. The variables measured included
the distance from the female at detection, how the male detected
the female (based on signs of abundant antennal movements or
visual fixation), male jumping distance, pre-copulation duration,
copulation duration, and post-copulation duration. I also paid
attention to possible courtship behaviors as previously reported
from other mantodeans, such as lateral swaying, abdomen bend-
ing, and rhythmic movements of legs. Due to possible directional
changes by the sexes during the encounters, I considered the result-
ing direction instead of initial direction for jumping. I recorded
pre-copulatory mounting duration as the time from mounting to
the genital linkage, copulation duration as the time from linkage
to separation of the genitalia, and post-copulation duration as the
time from the end of intromission until the male leaped off the

M. KOLNEGARI

female (according to Lelito and Brown 2006). I used multivariate
ANOVA to analyze the data with SAS software (version 9.1). Mean
and standard deviation were calculated with Microsoft Excel.

Results

Components of male sexual behavior typically included the
following: oscillation of antennae, visual fixation on the female,
quick running, cessation of movement, repeated downward and
upward bending of the abdomen, and jumping on the female's
back from 2.2+0.4 cm away. The dorsoventral rhythmic movement
of the male’s abdomen was typical of courtship and started slight-
ly downward (plantar flexion), then continued with an upward
variable bending (dorsiflexion) at an angle of 0° to 90° (Fig. 1).
The male sexual behavior was comprised of three phases.

Phase 1: Male orientation.—The initial approach occurred when a
male sensed a female and began abundant antennal movements
and prolonged viewing of her. These behaviors occurred within
1541.9 cm of the females with no significant difference between
frontal and lateral male release (F = 2.68, df = 1, 22, p = 0.4).
In five of the 28 trials (one frontal and four lateral), the males
did not interact with the females within three hours; these were
excluded from the dataset. Lateral swaying was not observed in
any intersexual approaches during this experiment. Seventy-eight
percent of males that noticed a female moved quickly toward
the female. Sixty-seven percent of these moving males mounted
without courtship. Twenty-two percent of males that noticed a
female were motionless until the female began to advance. This
behavior occurred more frequently in frontal encounters than lat-
eral encounters (Fig. 2). Thirty-eight percent of initially frontal
encounters changed to lateral encounters as males changed their
approach route. Meanwhile, 20% of lateral encounters became
frontal encounters because of female awareness and subsequent-
ly turning to face the male. Flexion of the abdomen and fore-
limb waving occurred only when males and females were facing
each other. Regardless of initial approach, 21% of the trials (n =
6) resulted in face-face encounters, which led males to display
one of these rhythmic movement. While abdomen bending was
a typical form of courtship, forelimb waving was not followed by
mounting in the study.

Among frontal encounters (n = 13), five males started to
move then changed their orientation from frontal to lateral and
stopped within 2.2+0.4 cm of females (i.e., “jumping distance”).
Two males demonstrated flexion of the abdomen seven and
eight times in 10 and 11 seconds, respectively, in what could be
considered courtship behavior (Fig. 1), then reached the jump-
ing point. Another two males responded to the female by trem-
bling their forelimbs, displaying the patterned interior faces and
waving them in slow arcs, before moving away from the female.
Therefore, forelimb trembling did not seem to be a component of
courtship. Four males did not move but waited for the female to
approach to jumping distance.

Among lateral encounters (n = 10), one male did not move and
waited for the female to approach to jumping distance. Nine males
moved towards the females. Two of these moving males faced the
females frontally because she changed her direction. One of these
two males demonstrated flexion of abdomen (six times in 11 sec-
onds) and reached the jumping point, the other male trembled
his forelegs before moving away from the female who followed
after him (Fig. 3). The seven remaining males reached jumping
distance and did not show rhythmic movement.

JOURNAL OF ORTHOPTERA RESEARCH 2020, 29(1)

M. KOLNEGARI

37

a

Fig. 1. Orientation of male Holaptilon brevipugilis abdomen in a frontal encounter with a female prior to copulation. A. Plantar flexion
and B. Dorsiflexion of the abdomen. The male is in the foreground on the left and the female is to the rear and to the right of the male.

5 (38%) Changing the direction from frontal to lateral
due to male movement + mounting from lateral

9 (69%) Movement toward

—- 2 (15.5%) Abdomen bending + mounting from frontal
the female

Frontal release

|

2 (15.5%) Forelimbs trembling + move away from female

4 (31%) Motionless males +
mounting from lateral

7 (70%) Mounting from lateral

9 (90%) Movement toward

the female

1 (10%) Motionless males +
mounting from frontal

1 (10%) Abdomen bending +
mounting from frontal

%

2 (20%) Face-to-face encounter a

due to female awareness %

1 (10%) Forelimbs trembling +
move away from female

Lateral release
n=10

Fig. 2. The sequence of mating behavior of Holaptilon brevipugilis showing the number and the percentage of males at each stage. One frontal
encounter and four lateral encounters did not lead to any interaction between males and females, so they were excluded from the dataset.

Phase 2: Male mounting.—This phase was characterized by males
jumping onto the female for copulation (mounting) from a dis-
tance of 2.2+0.4 cm from the female. Nine males that initially
encountered females laterally and eleven males that initially en-
countered females from a frontal position entered the mounting
phase. Sixty percent of these males mounted the female from a
lateral position and 40% mounted from a frontal (face-to-face)
position. Almost all males leaped successfully, with just one male
with a frontal orientation miscalculating the distance and lying
under the female after jumping (Fig. 4A). The orientation prior to
the jump had a significant effect on jumping distance (F = 8.43,

df = 1, 19, p = .017), so males mounting from a frontal position
leapt from greater distances than males mounting females from a
lateral position.

Phase 3: Copulation.—As soon as the male mounted the female,
he began the characteristic, approximately 45° angle S-bending
mating movements of his abdomen similar to those described for
Tenodera aridifolia sinensis (Liske and Davis 1987, Lelito and Brown
2006). There was an interesting bias in abdomen S-bending direc-
tion not mentioned in prior literature, as males preferred to bend
the abdomen from the left side in 95% of trials (Fig. 4B).

JOURNAL OF ORTHOPTERA RESEARCH 2020, 29(1)

M. KOLNEGARI

Fig. 4. Copulation behavior in Holaptilon brevipugilis. A. Male mounting failure. Male is underneath the female. B. Copulation. Smaller
male is on top of the larger female.

Sixteen of the 28 trials led to copulations that occurred 5-28
seconds after mounting. One trial in which the male mounted in a
reverse position delayed this pre-copulation period for more than
four minutes. I terminated two trials after males mounted for 20-
24 minutes but did not successfully contact the female's genitalia.
Body measurement confirmed those two males (with 1.05 and
1.07 cm body length) were among the smallest males, while those
two females (with 1.77 and 1.86 cm body length) were larger than
the average female (1.6 cm body length).

Copulation lasted 5.76+1.06 hours and post-copulation dura-
tion was 9.88+1.4 minutes. Neither copulation duration nor post-
copulation duration differed significantly between frontal and lat-
eral encounters (F = 44.2, df= 1, 17, p = 0.71 and F = 9.6, df = 1,
17, P =0.26).

I recorded just one case of cannibalism, which occurred after
mating when a male separated from the female.

Discussion

The male mantid presents a complicated series of mating be-
haviors, which can differ between species. These behaviors induce
behavioral isolation as a barrier to mating with other species (re-
viewed in Gray 2005). Adult male Persian boxer mantids in this
study performed a rather simple mating pattern that included

moving closer to the female and leaping onto her back from a con-
served distance. Males most frequently mounted females from a
lateral approach, consistent with the idea that males try to reduce
the probability that they will be cannibalized during intersexual
encounters by avoiding the visual field of females (Liske and Davis
1987, Maxwell 1998). However, in face-to-face encounters, males
lifted and bent their abdomens, which may be a form of court-
ship. Male courtship frequency was inconsistent, which we would
expect if males adjust their behaviors in ways that minimize the
chance of being attacked (Jayaweera et al. 2015).

In this study, female H. brevipugilis rarely performed sexual can-
nibalism, though future studies could examine the effect of female
hunger level on this behavior. H. brevipugilis nymphs did not have
any cannibalistic activity (personal observation), and so it is pos-
sible that H. brevipugilis is an infrequently cannibalistic mantid.
On the other hand, hungry females might not be able to easily
consume males during copulation because of considerable sexual
dimorphism, although this conclusion needs further investigation.

Orientation of approach had a significant effect on the Persian
boxer mantid males’ jumping distance, while Lelito and Brown
(2006) found that factor did not have a significant effect on Chi-
nese mantid (Tenodera aridifolia sinensis (Saussure) ) male jumping
distance. Increased male jumping distance decreases the likeli-
hood of cannibalism (Lelito and Brown 2006), so future studies

JOURNAL OF ORTHOPTERA RESEARCH 2020, 29(1)

M. KOLNEGARI

on Persian boxer mantid should investigate the correlation of fe-
male hunger levels to male jumping distance. However, both the
frequency of female-on-male cannibalism and the jumping dis-
tance of males in the Persian boxer mantid could be dependent on
female hunger level and changeable under different conditions.

I did not identify when and why males and females of Persian
boxer mantids performed foreleg trembling, but I concluded that
this is not related to mating behavior because males that displayed
this behavior tended to move away from the female rather than mat-
ing with her. However, forelimb trembling could demonstrate threat
posture, which has been known as “deimatic behavior” in manto-
deans (Maldonado 1970, Umbers et al. 2015) and could explain
why this behavior was observed when specimens were being field
collected. By contrast, males of Ephestiasula amoena (Bolivar) move
their forelimbs to expose a bright pattern on the inside face of the
expanded, plate-like forefemora before mating (Loxton 1979). Flex-
ion of the abdomen, another rhythmic movement of Persian boxer
mantid, is more likely associated with mating. Bending of the abdo-
men in H. brevipugilis follows a different pattern from Hestiasula ma-
jor (Beier), which moves the abdomen laterally (personal observa-
tion). Additionally, the Persian boxer mantid male starts this rhyth-
mic motion with a slightly downward movement (Fig. 1A), unlike
Pseudomantis albofimbriata (Barry et al. 2008b) and Tenodera sinensis
(Liske and Davis 1987) that show only upward abdomen bending.

I did not observe any lateral swaying or side-to-side movement
in the boxer mantid, while this behavior is a component of Pseu-
domantis albofimbriata males’ sexual behavior (Barry et al. 2008b).
The Persian boxer mantid’s flexion of the abdomen only occurred
in some frontal encounters; however, Lelito and Brown (2006)
observed this behavior in lateral encounters of Tenodera aridifolia
sinensis, although they provided evidence that frontal encounters
induced Chinese mantid males to bend their abdomens with a
greater angle. In fact, both above-mentioned studies showed that
frontal encounters increase the degree of the male’s movements.

In a broader context, courtship display has some correlations
with taxonomic categories. “Abdomen movement” has been ob-
served in all four studied species in the Mantidae family (Hola-
ptilon brevipugilis, Tenodera aridifolia, Ameles decolor, Pseudomantis
albofimbriata) and only one third of the studied species in the
Hymenopodidae family (Hestiasula major) (Liske and Davis 1987,
Barry et al. 2008b, Battiston 2008). The similarity of courtship be-
havior in such taxonomically distant species of praying mantids
may suggest this behavior is quite old, and could have been pres-
ent in a common ancestor. Of course this might also be explained
as convergence, but using the same structures to signal in the same
way would seem an improbable result of separate evolution (Bat-
tiston 2008). Though we now know the courtship displays of the
Persian boxer mantid, we need to study such behaviors in other
members of the Mantidae in general and, more specifically, the
Amelinae subfamily, to understand their evolutionary history.

Acknowledgements

I would like to thank Dr. Matan Shelomi and Dr. Saeed Alaei
for English improvement of the manuscript, as well as Ms. Man-
dana Hazrati and Mr. Reza Babaei-pour for their help in the field
survey and laboratory trials.

References

Abu-Dannoun O, Katbeh-Bader A (2007) Mantodea of Jordan. Zootaxa
1617: 43-56. https://doi.org/10.11646/zootaxa.1617.1.2

39

Barry KL, Holwell GI, Herberstein ME (2008a) Female praying mantids use
sexual cannibalism as a foraging strategy to increase fecundity. Behav-
ioural Ecology 19: 710-715. https://doi.org/10.1093/beheco/arm156

Barry KL, Holwell GI, Herberstein ME (2008b) Male mating behaviour reduc-
es the risk of sexual cannibalism in an Australian praying mantid. Journal
of Ethology 27: 377-383. https://doi.org/10.1007/s10164-008-0130-z

Battiston R (2008) Mating behaviour of the mantid Ameles decolor (In-
secta, Mantodea): Courtship and cannibalism. Journal of Or-
thoptera Research 17: 29-33. https://doi.org/10.1665/1082-
6467(2008)17[29:MBOTMA]2.0.CO;2

Beier M (1964) Ein neues mantiden-genus aus Israel. Israel Journal of Zo-
ology 13: 184-186.

Bonfils J (1967) Contribution a l’etude des orthoptéroides des Antilles 111.
Une espece nouvell dugenre Oligonyx Saussure: description et notes
biologiques (digt.). Bulletin de la Société Entomologique de France
72: 243-248.

Edmunds M (1975) Courtship, mating, and possible sex pheromones in
three species of Mantodea. Entomologist’s Monthly Magazine 111:
53-57.

Gray DA (2005) Does courtship behaviour contribute to species-level re-
productive isolation in field crickets? Behavioural Ecology 16: 201-
206. https://doi.org/10.1093/beheco/arh144

Hurd LE, Eisenberg RM, Fagan WE, Tilmon KJ, Snyder WE, Vandersall KS,
Datz SG, Welch JD (1994) Cannibalism reverses male-biased sex ratio
in adult mantids: female strategy against food limitation? Oikos 69:
193-198. https://doi.org/10.2307/3546137

Jayaweera A, Rathnayake DN, Davis KS, Barry KL (2015) The risk of sexual
cannibalism and its effect on male approach and mating behaviour
in a praying mantid. Animal Behaviour 110: 113-119. https://doi.
org/10.1016/j.anbehav.2015.09.021

Kadoi M, Morimoto K, Takami Y, Ethol J (2017) Male mate choice in a
sexually cannibalistic species: Male escapes from hungry females in
the praying mantid Tenodera angustipennis. Journal of Ethology 37:
177-185. https://doi.org/10.1007/s10164-017-0506-z

Kolnegari M, Vafaei-shoushtari R (2018) The first Persian boxer mantid, a new
species of Holaptilon Beier, 1964 from Haftad-gholeh Protected Area, Iran
(Mantodea, Mantidae). Journal of Entomological Research 10: 9-17.

Lelito JP, Brown WD (2006) Complicity or conflict over sexual cannibalism?
Male risk taking in the praying mantis Tenodera aridifolia sinensis. The
American Naturalist 168: 263-269. https://doi.org/10.1086/505757

Liske E, Davis WJ (1987) Courtship and mating behaviour of the Chinese
praying mantis, Tenodera aridifolia sinensis. Animal Behaviour 35:
1524-1537. https://doi.org/10.1016/S0003-3472(87)80024-6

Loxton RG (1979) On display behaviour and courtship in the praying
mantis Ephestiasula amoena (Bolivar). Zoological Journal of the Lin-
nean Society 65: 103-110. https://doi.org/10.1111/j.1096-3642.1979.
tb01083.x

Maldonado H (1970) The deimatic reaction in the praying mantis Stagma-
toptera biocellata. Zeitschrift fiir vergleichende Physiologie 68: 60-71.
https://doi.org/10.1007/BF00297812

Maxwell MR (1998) Lifetime mating opportunities and male mating be-
haviour in sexually cannibalistic praying mantids. Animal Behaviour
55: 1011-1028. https://doi.org/10.1006/anbe.1997.0671

Maxwell MR (1999) Mating behavior. In: Prete FR, Wells H, Wells PH,
Hurd LE (Eds) The Praying Mantids. Johns Hopkins University Press,
Baltimore, 62-99.

Quesnel VC (1967) Observations on the reproductive behaviour of the
mantis Acontiothespis multicolor. Journal Trinidad and Tobago Field
Naturalist’s Club 1967: 53-56.

Roy R (1999) Morphology and Taxonomy. In: Prete FR, Wells H, Wells PH,
Hurd LE (Eds) The Praying Mantids. Johns Hopkins University Press,
Baltimore, 19-41.

Umbers KDL, Lehtonen J, Mappes J (2015) Deimatic displays. Current Bi-
ology 25: 58-59. https://doi.org/10.1016/j.cub.2014. 11.011

Younes A (2007) Laboratory study of cannibalism in Sphodromantis viri-
dis Forskal (Mantodea: Mantidae): Effects of prey availability, habitat
structure, and predator density. Egyptian Journal of Pest Control 17:
57-63.

JOURNAL OF ORTHOPTERA RESEARCH 2020, 29(1)