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Ent. Bl. Col. (2017) 113 (1): 213 - 218 ISSN 0013-8835
Entomologische Blätter und Coleoptera
© Wissenschaftlicher Verlag Peks
Adult leaf beetles of the subfamily Cassidinae (Coleoptera: Chrysomelidae)
preyed on by the digger wasp Cerceris albofasciata
(Hymenoptera: Crabronidae) in Japan
Tadashi Shinohara* & Yasuoki Takami
*corresponding author
Abstract
Leaf beetles of the subfamily Cassidinae Gyllenhal, 1813 (Coleoptera: Chrysomelidae) exhibit various external morphologies in all life stages,
and these may be anti-predator adaptations. We revealed the predator-prey relationship between Cassidinae and their specic predator Cerceris
albofasciata (Rossi, 1790) (Hymenoptera: Crabronidae: Philanthinae) in Japan. We collected the beetle prey from hunting Cerceris females and
larval cells at two study sites. We collected 11 Cassidinae species belonging to four genera (Aspidimorpha indica, Aspidimorpha transparipennis,
Cassida fuscorufa, Cassida japana, Cassida nebulosa, Cassida piperata, Cassida versicolor, Thlaspida biramosa, Thlaspida lewisii, Dactylispa
angulosa, and Dactylispa subquadrata), and species other than C. nebulosa and C. piperata were new prey records. Species with explanate margins
or short spines were prey for C. albofasciata, but the long-spined species D. higoniae was not, despite its occurrence in the same habitat around the
nesting site. These results give insight into the origin of morphological diversity in the subfamily Cassidinae.
Kurzzusammenfassung
Blattkäfer der Unterfamilie Cassidinae Gyllenhal, 1813 (Coleoptera: Chrysomelidae) weisen in allen Entwicklungsstadien verschiedentliche
Bildungen der äußeren Morphologie auf, die möglicherweise Anti-Prädator-Anpassungen darstellen. Wir haben die Pädator-Beute-Beziehungen
zwischen Cassidinae und ihrem spezischen Prädator Cerceris albofasciata (Rossi, 1790) (Hymenoptera: Crabronidae: Philanthinae) in Japan un-
tersucht. Wir sammelten die erbeuteten Käfer von jagenden Cerceris Weibchen und Larvenzellen in zwei Untersuchungsgebieten. Wir sammelten
11 Arten von Cassidinae aus vier Gattungen (Aspidimorpha indica, Aspidimorpha transparipennis, Cassida fuscorufa, Cassida japana, Cassida
nebulosa, Cassida piperata, Cassida versicolor, Thlaspida biramosa, Thlaspida lewisii, Dactylispa angulosa, and Dactylispa subquadrata), außer
C. nebulosa und C. piperata neue Meldungen von Beute. Arten mit verbreiterten Körperrändern oder kurzen Stacheln waren Beute von C. albo-
fasciata, die langstachelige Art D. higoniae jedoch nicht, obwohl sie im selben Habitat und um die Neströhren herum vorkam. Diese Ergebnisse
erlauben Erkenntnisse über den Ursprung morphologischer Vielfalt in der Unterfamilie Cassidinae.
Key words: predator-prey relationship, eld observation, specialist predator, prey, defensive morphology, predation avoidance, anti-predator
adaptation
Introduction
Predator-prey interactions are one of the major driv-
ing forces in the evolution of the morphology and be-
havior of organisms (
Dawkins
&
krebs
1979;
Vermeij
1994, 2002), and anti-predator adaptations may play
an important role in the remarkable morphological
diversication in insects. The family Chrysomelidae
(leaf beetles) is one of the most speciose animal fam-
ilies with nearly 40,000 described species (
Lawrence
1982;
joLiVet
&
Verma
2002). This diversity is reect-
ed in their morphological and ecological characteris-
tics. Cassidinae s.l. (about 6,000 species) is the second
largest subfamily after Galerucinae s.l. (about 12,800
species) among Chrysomelidae (
joLiVet
&
Verma
2002;
chaboo
2007). The adults of Cassidinae (tor-
toise and leaf-mining beetles) exhibit various peculiar
external morphologies, such as spines on the dorsal
surface and explanate margins of the pronotum and
elytra. These external morphologies are hypothesized
to be anti-predator adaptations (
Deroe
&
PasteeLs
1982;
oLmsteaD
1996;
joLiVet
&
Verma
2002;
cha
-
boo
2007). Although previous studies reported many
kinds of leaf beetle predators (e.g.
ohno
1955;
cox
1996;
oLmsteaD
1996;
nogueira-De-sá
&
Vascon
-
ceLLos-neto
2003), predator-prey relationships in
Cassidinae are still poorly understood. Thus, elucida-
tion of predator and prey species in the eld is vital
to test the hypothesis that the external morphological
features of Cassidinae are anti-predator adaptations.
Tadashi shinohara* & Yasuoki Takami
214
Cerceris Latreille, 1802 (Hymenoptera: Crabroni-
dae) is distributed worldwide and contains 910 spe-
cies (
terayama
&
suDa
2016). They hunt specic
prey groups (Coleoptera and Hymenoptera,
tsuneki
1965) and have a special ability to locate prey species
(e.g. Cerceris fumipennis, Marshall et al. 2005). Ow-
ing to this property, Cerceris fumipennis Say, 1837 has
been utilized to document the hidden biodiversity of
buprestid beetles in a given region. In three days in a
park in Ontario, C. fumipennis collected 12 bupres-
Fig. 1. Cerceris albofasciata, a specialist predator of Cassidinae, and its prey. A: a female wasp carrying her prey to the nest
(photo by Y. Tanaka); B: beetles stored in a larval cell.
tid species belonging to ve genera, three of which
were new species records for Canada (
marshaLL
et al.
2005). In addition, C. fumipennis has recently gained
attention as a ‘biosurveillance’ tool for the efcient
detection of pest buprestid beetles (
careLess
2009;
careLess
et al. 2009). Thus, clarifying the prey of Cer-
ceris digger wasps can reveal the diversity of certain
groups of insects and can provide crucial information
related to the ecology and evolution of predator-prey
relationships.
Cerceris albofasciata (Rossi, 1790) (Fig. 1A) is a soli-
tary digger wasp (
katayama
1933) distributed in the
trans-Palearctic region (
Lee
et al. 2008). This wasp
exclusively hunts adult in the subfamily Cassidinae
(
katayama
1933;
tsuneki
1942, 1965), carries the
prey by grasping the insect venter to venter, holding
its body from both their legs (
tsuneki
1942, 1965),
and stores prey which has been immobilized (
Fabre
1914) in its nests for larval food (Fig. 1B). Eleven prey
species in three cassidine genera have been reported in
previous studies (
roth
1923;
giorDani
soika
1932;
katayama
1933;
koLossoV
1934;
tsuneki
1942, 1965;
shkuratoV
2001;
ZetteL
et al. 2008), including ten
tortoise beetles, Cassida denticollis Suffrian, 1844, C.
viridis Linnaeus, 1758 (reported as C. equestris Fabri-
cius, 1787, which is currently treated as a synonym
of C. viridis), C. lineola Creutzer, 1799, C. murraea
Linnaeus, 1767, C. nebulosa Linnaeus, 1758, C. nobilis
Linnaeus, 1758, C. piperata Hope, 1842, C. rubiginosa
Muller, 1776, C. vibex Linnaeus, 1767, Hypocassida
subferruginea (Schrank, 1776), and one hispine bee-
tle, Dicladispa testacea (Linnaeus, 1767) (reported as
Hispa testacea), with long spines. These records indi-
cate that tortoise beetles, especially those in the genus
Cassida, are the main prey species for this wasp, while
spined Dicladispa beetles are rare and based on a sin-
gle record (
roth
1923).
The goal of the current study is to document the di-
versity of Cassidinae species preyed on by C. albofas-
ciata in Japan to evaluate the hypothesis that diversity
in external morphologies in Cassidinae is a result of
anti-predator adaptations. Here, we characterized the
prey of C. albofasciata in Hyogo and Chiba prefec-
tures based on surveys in two and one reproductive
seasons, respectively.
Materials and methods
Study sites
Field surveys were performed in Sanda City, Hyogo
Prefecture (Sanda site, 34.9205° N 135.2750° E) from
July to August 2014–2015 and in Yachiyo City, Chiba
Prefecture (Yachiyo site, 35.7348° N 140.1107° E) in
July 2015, when the wasps were actively provisioning
their nests. These study sites were approximately 450 km
apart. C. albofasciata females nested on a patch of open,
disturbed bare ground with hard-packed soil. About
20–30 female wasps were seen in both sites in all seasons.
Adult leaf beetles of the subfamily Cassidinae
215
Cassidines around nesting sites
We searched Cassidinae species around the nesting
site of the wasp to determine the fauna of its prey can-
didates. We walked around in the surrounding areas of
nesting sites (within about 200 m radius from a nesting
site), and almost all of host plants on which Japanese
cassidine can feed were investigated by sweeping, beat-
ing and looking.
Sampling from hunting females
Three techniques were used to collect Cassidinae
prey from hunting female wasps. First, female wasps
returning to the nest with prey (e.g. Fig. 1A) were
captured using a sweep net, from which the prey was
collected, and the wasp was released. Second, female
wasps occasionally dropped their prey in response to
disturbances and the prey item was collected. Third,
prey left near the entrance of the nest were collected. A
female wasp returning to the nest usually lays the prey
near the entrance, enters the burrow head rst, turns
around immediately, protrudes its anterior body from
the nest opening, grasps the prey with its mandibles,
and pulls it into the nest (
katayama
1933;
tsuneki
1965). This behavior is specic to C. albofasciata and
is not found in other Cerceris species (
tsuneki
1965).
To investigate the number of hunting wasps, captured
females were marked using waterproof paint in 2015
at both sites.
Prey sampling from larval cells
To estimate the number and composition of prey spe-
cies stored in each larval cell, wasp nests were excavat-
ed using a hoe in July 2015 at the Sanda site and prey
items were collected. As the cells are usually located
at 10–15 cm underground (
katayama
1933;
tsune
-
ki
1965), digging was performed down to 15 cm. All
stored prey items were collected, including pieces of
broken prey. This investigation was restricted to a clus-
ter of ve nests at the Sanda site in 2015 to avoid dam-
age to the nesting habitat.
Species determination
Prey species were identied based on the classication
system of
kimoto
&
takiZawa
(1994), except for Cas-
sida japana Baly, 1874 and Thlaspida biramosa (Bo-
heman, 1855), which were treated as synonyms of C.
piperata and T. cribrosa (Boheman, 1855) at the time,
respectively. Partial fragments of prey collected from
larval cells were identied based on morphological
characteristics of the elytra. All collected beetles, in-
cluding partial fragments, were successfully identied.
Specimens of beetles and wasps are preserved in the
rst author’s collection for ongoing study.
Results and Discussion
We detected novel prey species of C. albofasciata in
Japan, including many tortoise beetles and hispine
beetles with short spines. Eleven species representing
four genera in three tribes of Cassidinae were collect-
ed as prey of C. albofasciata in Japan in 2014 and 2015
(Table 1). Of these, nine species are new prey records
for C. albofasciata: Aspidimorpha indica Boheman,
1854, A. transparipennis (Motschulsky, 1860), Cassida
fuscorufa Motschulsky, 1866, C. japana, C. versicolor
(Boheman, 1855), Thlaspida biramosa, T. lewisii (Baly,
1874), Dactylispa angulosa (Solsky, 1872), and D.
subquadrata (Baly, 1874). The last two species belong
to the genus Dactylispa and have the dorsum of the
elytra with short spines. (Fig. 2). These species with
explanate margins are spineless, and those with short
spines lack explanate margins. Thus, C. albofasciata
can hunt Cassidinae species with multiple external
morphology types. The wasp did not hunt any prey
other than adult cassidines. Chemical defense (
gómeZ
et al. 1999) or fecal shield (
bLum
1994) of larvae may
hinder predation by the wasp.
Fig. 2. Morphology of prey leaf beetles. A: species with explanate margin (T. biramosa); B: species with short spines (D.
subquadrata); and C: species with long spines (D. higoniae), which was not preyed on by the wasp. Scale bar, 1 mm.
Tadashi shinohara* & Yasuoki Takami
216
At the Sanda site, 23 of 31 observed female wasps
carried prey in 2015. Although we did not identify
individual females in 2014, we observed a similar
number (i.e., about 30 females). We found four larval
cells below the cluster of ve nest entrances in 2015.
In total, we collected eight prey species belonging to
four genera (Aspidimorpha transparipennis, Cassida
fuscorufa, C. japana, C. versicolor, Thlaspida biramo-
sa, T. lewisii, Dactylispa angulosa, and D. subquadra-
ta) (Table 1). Of these, we collected A. transparipennis
and C. fuscorufa from hunting females only, and we
collected D. angulosa (one left elytron) from a larval
cell only. We collected T. lewisii (32.2%) and C. versi-
color (42.1%) most frequently in 2014 and 2015, re-
spectively. Although we recorded six species in larval
cells, most specimens were partial fragments. There-
fore, the number of prey individuals per cell was un-
clear, and we estimated the minimum number of in-
Table 1. Prey species composition and abundance for hunting females (F) and larval cells (L) of Cerceris albofasciata. The
number of observed hunting females is shown in parentheses (- not observed). * = new prey record for C. albofasciata.
dividuals based on the composition of the fragments.
Only one of the four cells was lled with six paralyzed
C. versicolor, a relatively small tortoise beetle species
in Japan (Fig. 1B, cell A in Table 1). In the remaining
three cells (B–D), we detected nine, 12, and 20 beetles
(Table 1). It was difcult to identify correspondence
between the four cells and the ve nest entrances ini-
tially observed, each of which may be owned by a
single female, because the tunnels of the nests are ir-
regularly bent and fairly compactly packed with soil
(
tsuneki
1965).
tsuneki
(1965) and
katayama
(1933)
revealed that each nest includes at least six cells and
each cell is stocked with 6–17 and 5–7 prey individu-
als, respectively. Nests were still provisioned by female
wasps when excavated in both the present and previ-
ous studies, indicating that the numbers of prey per
cell and cells per nest may be underestimates.
At the Yachiyo site, 14 of 23 female wasps carried
prey in 2015. Compared with the Sanda site, we re-
corded fewer prey species at the Yachiyo site, i.e., four
prey species belonging to two genera (Aspidimorpha
indica, Cassida japana, C. nebulosa, and C. piperata),
from hunting females. We collected C. japana (56.0%)
most frequently, which was the only prey species ob-
served at both study sites. The differences between
sites may be explained by a difference in survey meth-
ods, time spent for the survey, and the number of ob-
served female wasps. Additionally, the difference in
prey species composition may be inuenced by the
geographical distribution of beetles, host plant di-
versity in the vicinity of nests, foraging behavior of
wasps, and the degree of human activity around the
nest.
Most Cassidinae species observed around the
nesting sites were preyed on, but certain species were
underrepresented. Although we detected the hispine
beetle Dactylispa higoniae (Lewis, 1896) with dense
long spines at the Sanda site, this species was not
preyed on by the wasp. Since D. higoniae shares host
plants Callicarpa spp. (Verbenaceae) with the prey
species T. biramosa, the wasp could detect both spe-
cies while hunting. Six possible reasons can explain
this underrepresentation: (1) developed spines of D.
higoniae have a defensive function against the wasp,
(2) long spines are unsuitable for larval food and
avoided, (3) D. higoniae have another type of defense
(e.g., chemical, but see
Deroe
&
PasteeLs
1982), (4)
D. higoniae is infrequent around the nesting site, (5)
D. higoniae adults have not yet emerged during the re-
productive seasons of the wasp, or (6) D. higoniae is
much smaller than T. biramosa and unsuitable as prey.
Further studies are necessary to quantify non-random
prey hunting by the wasp and to examine the factors
Adult leaf beetles of the subfamily Cassidinae
217
allowing certain beetle species to avoid predation by
the wasp.
Acknowledgments
We always admired the work of the late Manfred
Döberl and dedicate this contribution to his memory.
We wish to express our sincere thanks to Y. Tanaka
and H. Yoshimura for their help in locating the nest-
ing sites and providing information about wasp prey.
We also thank the editor and two anonymous review-
ers for their constructive suggestions. This study was
nancially supported by a Sasakawa Scientic Re-
search Grant from The Japan Science Society (no. 27-
515).
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Author’s addresses
taDashi shinohara
Graduate School of Human Development & Envi-
ronment
Kobe University
3-11 Tsurukabuto, Nada
Kobe 657-8501
Japan
E-Mail: shinohara@stu.kobe-u.ac.jp
yasuoki takami
Graduate School of Human Development & Envi-
ronment
Kobe University
3-11 Tsurukabuto, Nada,
Kobe 657-8501
Japan
E-Mail: takami@people.kobe-u.ac.jp