Appl. Entomol. Zool. 42 (3): 337–346 (2007)

Review

http://odokon.org/

Applied evolutionary ecology of insects of the subfamily Bruchinae(Coleoptera: Chrysomelidae)
Midori TUDA*
Institute of Biological Control, Faculty of Agriculture, Kyushu University; Fukuoka 812–8581, Japan(Received 17 October 2006; Accepted 19 January 2007)

Abstract
Bean beetles of the subfamily Bruchinae (formerly, the family Bruchidae) include notorious pests of stored legumes,
Callosobruchus, Caryedon, Acanthoscelides and Zabrotes that are able to feed and reproduce on dried beans and peas.
Here, I review recent findings on the ecology, phylogeny, invasion and evolution in the bean beetles, based on field investigation of host plants and molecular studies. Possible future application of the new knowledge to weed and pest
control is proposed, such as potential utility of the seed predators for modest control of beneficial yet invasive (‘conflict’) plants and new control methodology of pest bean beetles.
Key words: Bruchidae; seed predators; stored product pests; biological weed control; molecular phylogeny

stored-bean pests. Strictly speaking, however, thegenus Bruchus is different from other stored-beanpests in that it does not reproduce on dried hardened beans/peas and thus cannot cause further
damage in storage.

INTRODUCTION
Beetles of the subfamily Bruchinae (Coleoptera:
Chrysomelidae) are specialized internal feeders ofbean family seeds (Fabaceae). They are frequently
and erroneously referred to as the bean ‘weevils’in spite of their affinity to the leaf beetles(Chrysomelidae). Here, I use the common name,the bean ‘beetle’ (or the seed ‘beetle’) to avoid taxonomic confusion. I also follow the recent taxonomic consideration that the bean beetle is notunique enough as a family but as a subfamily ofChrysomelidae (Lingafelter and Pakaluk, 1997).
The Bruchinae consist of about 1,700 species(Johnson et al., 2004). Although not very high inproportion of species, some of the bean beetles arenotorious pests of stored beans with the highest intrinsic rate of increase among stored-products pests(Imura, 1990). They include several species of Callosobruchus, Acanthoscelides and Zabrotes that infest beans (Tribe Phaseoleae: Vigna, Phaseolus,
Glycine, etc.) and Caryedon that feeds on peanuts
or groundnuts (Arachis hypogaea) (Southgate,
1979; Johnson, 1981). Bruchus species that infest
broad beans and peas (Fabeae: Vicia and Pisum) of
economic importance may also be categorized as

PHYLOGENY
Recent molecular studies support that theBruchinae are closely related to the frog-legged
beetle subfamily, Sagrinae, within the family
Chrysomelidae (Farrell and Sequeira, 2004).
Within the Bruchinae, the tribes Amblycerini andPachymerini are thought to be paraphyletic to amajor tribe Bruchini (Farrell, 1998; Table 1). Although recent evidence supports the previously
proposed phylogeny at the higher taxonomic levels,
an intriguing new view of bean beetle phylogeny atthe lower levels has been proposed. Kergoat et al.
(2005a, b) supported the previously suggested viewthat Acanthoscelides and Bruchidius are polyphyletic groups (Johnson, 1981; Borowiec, 1987).
However, some monophyletic groups of Acanthoscelides may be more closely related to those of
Bruchidius than the other congeneric groups (Alvarez et al., 2006; Tuda, Kergoat, Kato, Ito, Bu-* E-mail: tuda@grt.kyushu-u.ac.jp
DOI: 10.1303/aez.2007.337

337

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Table 1.

M. TUDA
Taxonomic position and composition of Bruchinae

FamilySubfamily
Tribe
Chrysomelidae
Bruchinae
Amblicerini—3 genera (Spermophagus, Zabrotes)
Bruchini—46 genera (Acanthoscelides, Bruchidius,
Bruchus, Callosobruchus, Mimosestes)
Eubaptini—1 genus (Eubaptus)
Kytorhinini—1 genus (Kytorhinus)
Pachymerini—12 genera (Caryedon)
Rhaebini—1 genus (Rhaebus)
The genera in bold include pest species.

ranapanichpan, Szentesi and Jermy, unpublished).
These molecular studies also indicate potential
problems about relative phylogenetic positions
among other recently described genera. For example, a recent molecular study found Tuberculobruchus to be polyphyletic (Kergoat, 2005b), indicating a plesiomorphic trait is used for the generic
key and revision of the genus using genital morphology may be necessary. Data on recently described species, synonymies and host plants havebeen actively accumulated from different biogeographic regions of Asia and Africa that would contribute to the understanding of evolutionary diversity of the Old World (e.g., Arora, 1977, 1980;
Egorov and Ter-Minassian, 1983; Morimoto, 1990;
Anton et al., 1997; Anton, 1999, 2000; Kingsolver,
1999; Tuda, 2003; Johnson et al., 2004; Tuda andMorimoto, 2004; Tuda et al., 2005) and the New
World (e.g., Johnson, 1970; Romero and Johnson,
2000) bean beetles (see also Zacher, 1952; Udayagiri and Wadhi, 1989 for overviews).
ECOLOGY
In most bean beetles, female adults deposit eggs
on pods and/or seeds, hatched larvae burrow into
seeds and emerge out as adults (Southgate, 1979).
Adults lay eggs singly and larvae feed only single
seeds (Center and Johnson, 1974). Exceptions to
the typical life history are Conicobruchus (Prevett,1967), Merobruchus (Johnson, 1967) and Sennius(Center and Johnson, 1972), which feed on several
seeds in a single pod and Bruchidius, which feeds
on multiple pods in single Trifolium inflorescences(Balachowsky, 1962; Tuda, pers. obs.). In bothcases, the host seeds are too small to support bean
beetle development into full adult. Finally, as an
exception to the general pattern of pupating withinseeds, the larvae of several species of Caryedon
emerge out of seeds to form cocoons either on
pods or on the ground for pupation (Center andJohnson, 1974; Southgate, 1979; Tuda, pers. obs.).
Batch egg laying is known only for a limited
number of species such as Pseudopachymerina
spinipes (Teran, 1962), Caryedon fasciatus (Prevett, 1966), Caryoborus serripes (Delobel et al.,1995a) and Stator beali (Nilsson and Johnson,
1993; Fox and Mousseau, 1995). The host pods
and seeds of these beetles are hard and relatively
large (Janzen, 1971; Moreno-Casasola et al., 1994;
Delobel et al., 1995a; Delgado et al., 1997). In Callosobruchus, such egg clustering had previously
not been observed but it was recently found in a
non-pest species, which develops in a large, hardseeded legume (Tuda and Buranapanichpan, unpublished). These examples imply that egg laying
pattern is not phylogenetically constrained but may
respond to selection imposed by host plant characteristics (the size and/or hardness of pods andseeds), parasitoid pressure and abiotic factors(Janzen, 1971; Mitchell, 1977; Delobel et al.,1995a).
Typical hosts of bean beetles are legumes(Fabaceae) (84% of the known hosts; Johnson,1970) but the palm (Arecaceae), morning glory(Convolvulaceae), mallow (Malvaceae) and about
30 other families are also used as hosts (Southgate,
1979; Johnson, 1981). Most bean beetles are either
monophagous or oligophagous; their host range islimited to restricted plant taxa, usually subtribes
and tribes at most (Jermy and Szentesi, 2003; Delobel and Delobel, 2003; Tuda et al., 2005; Kergoat
et al., 2007a, b), although there are a few generalists that utilize different subfamilies of legumes.
Evolutionary relation between bean beetles andtheir host plants has been actively discussed as amodel of plant-insect evolution. Proximate mechanisms for host-plant shifts are probably associatedwith chemical (Janzen, 1969), morphological(Janzen, 1969; Szentesi and Jermy, 1995) and geographical (Johnson and Siemens, 1991) proximity
between the current and potential hosts. Delobel
and Delobel (2006) suggest that the speciation in
European bean beetles is sequential evolution

Applied Evolutionary Ecology of Bruchinae(sensu Jermy, 1984) or sequential radiation (sensu
Abrahamson et al., 2003) that follows plant diversification, which contrasts to the reciprocal coevolution model that assumes plant evolution in response to insect evolution against plant defensive
traits (sensu Ehrlich and Raven, 1964; Futuyma,
1983; Becerra, 2003).

339

ture studies, hardness of dried seeds will be one of
the foci of research because the hardness per se canserve as a deterrent against seed predators, including bean beetles (Janzen, 1977; Southgate, 1979;
Kitch et al., 1991; Dongre et al., 1993). The loss of
toxic chemicals during post-maturity drying
processes may also increase survival of such granivores, which promotes host range expansion.

EVOLUTION OF STORED PRODUCT PESTS
Evolution of stored bean pests is likely a twostep process. The first is preadaptation to utilize
dried hard seeds (Watanabe, 1985) and the second
is the evolution of dispersal, reproductive and competitive polymorphism to adapt to cultivated seeds
and storage environments (Utida, 1954, 1981;
Caswell, 1960; Nakamura, 1966; Sano, 1967; Ouedraogo and Huignard, 1981; Messina, 1984; Toquenaga, 1990; Tuda, 1997, 1998; Tuda and Iwasa,
1998; Takano et al., 2001). Hence, an ability tofeed on dried mature host seeds is an inevitableprerequisite for bruchids to become pests. This requires first, female adults to deposit eggs on/neardried mature seeds and second, hatched larvae toburrow into the hard seeds to feed on.
What is it then that promotes evolution of utilization of dry, hard seeds? Using a comparative
approach to study Callosobruchus pest and nonpest species, the potential effects of climate, hostplants, phylogeny and endosymbiotic bacterium
were examined (Tuda et al., 2006). Long dry season was shown to be the most important factor for
evolution towards preadaptive stage to become
stored bean pests (i.e., ability to use dry hardbeans) when evolutionary history was accountedfor (Tuda et al., 2006). Phylogenetic history of Callosobruchus and idiosyncrasy of their host plants
also had significant effects on the evolution towards stored bean pests (Tuda et al., 2006). In fuTable 2.

INVASION
With human aid, dispersal and invasion of livingorganisms in recent centuries are occurring at a
speed that has been unattainable with plate tectonics and glacial dynamics. In Japan, examples ofbean beetle invaders are Bruchus rufimanus andBruchus pisorum, the pests of broad beans andpeas, respectively (Table 2). Bruchus loti has also
been considered to be an alien species but our recent finding indicates the current status as an introduced species may require reconsideration, as described later in this section. We found two additional bean beetle species have invaded Japan(Tuda et al., 2001; Tuda, Tateishi, Niyomdham,
Morimoto, Chen, Zhu, Zhang, Murugan, Chou andJohnson, unpublished).
One recent invader is a bean beetle Acanthoscelides pallidipennis (A. collusus) that feeds
on a fast-growing, nitrogen-fixing legume, Indigobush (or False indigo; Itachi-hagi), Amorphafruticosa. The legume had invaded from North
America and established in England, Europe andEast Asia except Japan by the mid 20th century(Szentesi, 1999; Tuda et al., 2001). In Japan, thebean beetle was first found at two locations in thecentral and southwestern parts of the country in1997 (Tuda et al., 2001) and later in several areasin the southwestern Japan as well (Ishihara, unpublished). A molecular analysis of A. pallidipennis

Bean beetle invasion to Japan

Bean beetle

Time of invasion

Source population

Bruchus pisoruma
Bruchus rufimanusa
Callosobruchus maculatusb
Acanthoscelides pallidipennisc
Acanthoscelides macrophthalmusd

1888
1921
1950
1970s–1997
recent (–2000)

USA
England/Europe?
Korea and China?

a
Yoshida, 1990; b Morimoto and Kiritani, 1995; c Tuda et al., 2001; d Tuda, Tateishi, Niyomdham, Morimoto, Chen, Zhu, Zhang,
Murugan, Chou and Johnson, unpublished.

340

M. TUDA

from four States of the USA and from East Asia revealed that Japanese populations consist of several
unrelated haplotypes that are shared by Chineseand Korean populations and individuals interceptedby import inspection at Japanese seaport quarantines (Tuda, Ishihara, Wasano, Morimoto, Paik,
Houck and Johnson, unpublished). This molecularevidence supports our hypothesis (Tuda et al.,2001) that A. pallidipennis established in Japan
was transported from the introduced populations in
nearby East Asian countries. Indeed, from these regions, the host seeds (A. fruticosa) have been imported for erosion control since the 1970s (Tuda etal., 2001).
The other invader is Acanthoscelides macrophthalmus (Tuda, Tateishi, Niyomdham, Morimoto,Chen, Zhu, Zhang, Murugan, Chou and Johnson,
unpublished). It is a Neotropical species that feeds
on Wild tamarind, or Gin-nemu, Leucaena leucocephala. Leucaena leucocephala is a fast-growing
nitrogen-fixing leguminous tree that is cultivatedfor fodder (Elharith et al., 1980), green manure(Chagas, 1981), reforestation, windbreak, fuel,pulp and erosion control (Kondo et al., 1987; Satake et al., 1989). Because A. macrophthalmus isspecialized to Leucaena species (e.g., Johnson,
1979; Hughes and Johnson, 1996; Delobel andJohnson, 1998), L. leucocephala is the only Leucaena species that has been introduced to Japan,
and airborne long-distance dispersal is highly unlikely for bean beetles (Tuda et al., 2001), there islittle doubt that A. macrophthalmus has been introduced with the host seeds.
Accelerated long-range human transportation
promotes unexpected dispersal of animals andplants that eventually become pests in the areas
where they are introduced. As a consequence, it issometimes difficult to determine geographic origins of widely distributed organisms. Whether
local populations are native or of relatively recent
introduction from foreign populations can be estimated by statistics based on population genetics
theory if DNA sequence or restriction site data are
available (e.g., Templeton et al., 1992; Templeton,
1998). Our recent findings regarding Japanese populations of Bruchus loti may be a good example.
Palearctic fauna and flora share many species including B. loti. The Japanese populations of B. loti
are currently listed as an alien species that would
become a target of eradication. We found that hap-lotypes found in the Japanese populations areclearly different from those in European populations, which indicates that Japanese B. loti is not
introduced from Europe and likely originated fromthe Far East including Japan (Tuda, Ichita and Kergoat, unpublished). The genetic uniqueness of theJapanese population indicates that B. loti should
perhaps be conserved in this country. The status ofJapanese Callosobruchus chinensis is also controversial. Our molecular study shows that populations of C. chinensis in agricultural habitats are genetically homogeneous, whereas those from natural
habitats are heterogeneous, indicating a bottleneck
event caused by human agricultural practice andtransportation (Tuda et al., 2004).
APPLICATION TO BIOLOGICAL CONTROLAs natural enemy of conflict plants. A control
agent should ideally be a specialist feeding only ontargets of control and not harm beneficial organisms (Sweetman, 1936; Huffaker, 1964). Internal
feeders (‘endophages’) tend to have narrower dietbreadth than external feeders (‘exophages’)(Lewinsohn, 1991; Frenzel and Brandl, 1998) andare probably more suitable as biological control
agents. Indeed, bean beetles have been used as biological control agents of weedy plants and provento be effective, to some extent, once established in
the release areas (Table 3; c.f., Julien, 1992).
I propose two bean beetle species that have been
accidentally introduced and can be used for biological control of new leguminous weeds in Japan.
The first is A. pallidipennis. The narrow diet rangeof A. pallidipennis and the absence of congenericrelatives of Indigobush and naturally associatedparasitoids of the beetle are preferable features as acontrol agent, in contrast with the case of Bruchidius villosus that attacked not only the target but
also non-target (but non-indigenous) congeners
after its introduction to New Zealand (Paynter etal., 2004). In this respect, A. pallidipennis is suitable as an agent that controls escape of Amorphafruticosa from cultivation by seed dispersal. The
suitability of A. pallidipennis as a control agent has
also been pointed out in the native distribution areaof Indigobush (Rogers and Garrison, 1975). The
bean beetle would be even more suitable if it would
be applied for control in introduced areas where
its naturally associated enemies (i.e., parasitoids,

Applied Evolutionary Ecology of Bruchinae
Table 3.

341

Bean beetles used as biological control agents of weeds (modified from Julien, 1992; ARC-PPRI, 2003)

Control agent

Target weed

Location of release

Acanthoscelides macrophthalmus
Acanthoscelides puniceus
Acanthoscelides quadridentatus
Algarobius bottimeri
Algarobius prosopis
Bruchidius villosus
Bruchidius sahlbergi
Sulcobruchus subsuturalis

Leucaena leucocephalaMimosa pigra
Mimosa pigra
Prosopis glandulosa
Prosopis velutina
Cytisus scoparius
Acacia nilotica
Caesalpinia decapetalaSouth Africa
Australia, Thailand, Vietnam (Malaysia, Myanmar)
Australia, Thailand, Vietnam (Malaysia, Myanmar, USA)South Africa
South Africa
New ZealandAustralia
South Africa

Locations in parentheses are due to natural spread of released agents.

predators, parasites, and pathogens) and competitors (e.g., Acanthoscelides submuticus) are rare orabsent (Tuda et al., 2001). Acanthoscelides pallidipennis feeds only on Amorpha and related genera (Amorpheae: Errazurizia and Parryella) that
distribute naturally only in North America (Center
and Johnson, 1974).
The second is A. macrophthalmus. Leucaena
leucocephala, initially introduced as a beneficial
tree in the 19th century, escaped from cultivation
by seed dispersal and has become weedy in tropicalregions of Japan and other introduced areas (e.g.,Smith, 1985; Henderson, 2001; Wu et al., 2003).
Its seed predator, A. macrophthalmus, satisfies theabove criteria as a control agent in Asia, i.e., narrow host range and scarcity of parasitoids. In fact,
this bean beetle has already been deliberately introduced to South Africa for the control of L. leucocephala (ARC-PPRI, 2003; Olckers, 2004; Table
3). Nevertheless, there remains a risk that the control agent could easily accumulate local generalist
parasitoids and in the long term the control effectcould decrease as observed in West Africa (Delobel and Johnson, 1998).
Control of bean beetles. Fumigation has been
widely applied to stored products as an effective
method of control of stored products pests. However, methyl bromide, used for fumigation of grain
legumes (Yoneda et al., 1990) has been recognized
as one of the chemicals that deplete the stratospheric ozone layer and, hence, was called for its
controlled use by the Montreal Protocol (UNEP,
2000).
Alternatively, parasitoids (e.g., a trichogrammatid egg parasitoid Uscana, larval-pupal parasitoids, pteromalid Dinarmus, Anisopteromalus, aneupelmid Eupelmus, and a braconid Heterospilus;

e.g., Southgate, 1979; Steffan, 1981; Fujii and Wai,
1990; Mitsunaga and Fujii, 1999; Schmale et al.,
2001; Tuda et al., 2001; Kobayashi et al., 2003;
Jaloux et al., 2004; Tuda and Shimada, 2005; Wu
et al., 2005; Vamosi, Hollander and Tuda, unpublished) and plant extracts (e.g., Lambert, 1985;
Rahman, 1990) have been actively explored for biological control (see Fujii et al., 1990; Huis, 1991
for review). In addition to biological and botanicalcontrol, controlled temperature (e.g., Rahman,1990), mechanical control (e.g., Quentin et al.,1991), controlled atmosphere (e.g., Oosthuzien andSchmidth, 1942) and radiation (e.g., Kiyoku andTsukuda, 1968; Hossain et al., 1972; Reddy et al.,2006) have been proposed as effective control
methodology (see also Highley et al., 1994). I suggest an endosymbiotic bacterium, Wolbachia, frombean beetle pests and its functional relation withthe host (Kondo et al., 2002) may be applied to biological control of stored product pests. When theabove-mentioned multiple methods are used in
combination, the possibility of one agent negating
the other must be taken into account (e.g., Boeke etal., 2003).
Identification of pest species. External and internal morphology of the adult stage is used for
identification to species. Most recently male genital
traits for Callosobruchus were compared and summarized by Tuda et al. (2006). Compared to adultmorphology, egg and larval morphology is lesswell studied because they are not readily available(but see Pfaffenberger and Johnson, 1976; Arora,
1978; Delobel et al., 1995b), which makes identification based on pre-adult stages difficult. In contrast to the differential accessibility among developmental stages of morphological characters, molecular characters can be more stable and useful as342

M. TUDA

keys for identification. Using the PCR-RFLP technique, which is relatively easy and inexpensive,
species of all developmental stages of important
stored bean pests in the genus Callosobruchus havebeen successfully distinguished (Tuda et al., 1995).
CONCLUSION
Bean beetles, as other phytophagous insects, exhibit significant conservatism in host utilization.
Feeding on dried seeds not only enables repeatedgenerations but also broadens the diet of somebean beetle pests. Our study based on molecularphylogenetics indicates this preadaptation to use
dry, hard beans that precedes human store of beans
has been selected for by arid habitat climate (Tudaet al., 2006). Recent investigations of Asian bean
beetle fauna have revealed diversity of the species
and ecology of the seed predators. This also led to
the finding of invasions of alien bean beetles (Tudaet al., 2001; Tuda et al., unpublished). Invasionroutes estimated by our molecular approach indicated the invasion of the bean beetle was associated with imported alien host seeds. I propose therecent bean beetle invaders may be used for modest
control of the seed dispersal of beneficial but invasive alien plants (‘conflict plants’ (Neser, 1994)).
ACKNOWLEDGEMENTS
I am grateful to the Japanese Society of Applied Entomology and Zoology for the honorable award and the opportunity
to write this review. Thanks are also due to Alex Delobel andSteven Vamosi for their valuable comments on the manuscript.
This study was supported partly by the Fujiwara Natural
History Foundation, the Sumitomo Foundation, and Grant-inAids for International Scientific Research (Field Research09041145) and for Scientific Research (A) (08304049,
15208007), (B) (14405003, 17405005) and for Young Scientists (B) (15770011) from MEXT. This paper is dedicated to
my collaborators, the late Prof. Shwu-Bin Horng for his work
on behavioral ecology of Callosobruchus and the late Dr.
Liang-Yih Chou for his contribution to applied entomology.

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