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Biological Invasion Caused byCommercialization of Stag Beetles in Japan
Kouichi GOKA1, Hiroshi KOJIMA2 and Kimiko OKABE3
1National Institute for Environmental Studies
16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan
E-mail: goka@nies.go.jp
2
Nifty Insect Forum, 2-21-5 Nakacho, Meguroku, Tokyo 153-0065, Japan
3
Forestry and Forest Products Research Institute
1 Matsunosato, Kukizaki, Ibaraki 305-8687, Japan

Abstract
The breeding of stag beetles has come to be very popular in Japan, and over one million exotic stag
beetles are imported into Japan every year. This unusual boom has even led to criminal smuggling ofstag beetles from the countries prohibiting the collecting of any wild organisms. There is real concernthat ecological risks will result from this unprecedented business in insects. Native stag beetles willprobably suffer from serious and direct impacts because of the similarity of ecological niches. It isthought that the first impact will be competition for food and habitat, the second, genetic introgression
as a consequence of hybridization between the exotic and the native beetles, and the third, invasion ofimported parasites. We are studying the second and third impacts. Our molecular genetic analysis of
populations of Dorcus titanus, which is a major native species, indicates signs of genetic introgression
by exotic strains imported from South-east Asia. Moreover, our investigation of stag beetles imported
and sold shows that a lot of mites are coming into Japan attached to the beetles. We have to reconsider
and be more wary about importation of exotic stag beetles.
Key words: beetles, ecological risk, genetic introgression, invasive species, naturalization, parasite

1. Commercialization of Stag Beetles in Japan
Recently, the breeding of stag beetles as pets has
become a very popular hobby in Japan. Both nativeand exotic stag beetles have been commercialized anda large number of individuals are being transported
widely throughout Japan. In particular, importationof exotic stag beetles is increasing greatly, with overone million beetles imported into Japan every year
from all over the world (Fig. 1). The Plant Protection Law of Japan used to prohibit the importation ofstag beetles, but the prohibition was suddenly lifted in
1999 and subsequently the importation of 34 species
was accepted. Since then the number of permitted
species has increased year-by-year, reaching 505
species in 2003. So, we can say that the habitat
maintaining the highest biodiversity of stag beetles isJapanese pet shops.
This unusual boom has even led to criminal smuggling of rare or endangered species from every cornerof the world. For example, in Japan one can buy arare species of stag beetle (Dorcus antaeus), native to
Bhutan, Nepal and India, although in these countries it
is absolutely prohibited to collect any wild organisms.
Global Environmental Research8(1)/2004: 67-74
printed in Japan

The price of this beetle is as incredibly high as
600,000 Japanese yen (5,000 US dollars) per individual (Fig. 2). As there is no law in Japan prohibiting
importation of insects even from such prohibited areas,a lot of Japanese insect collectors or traders go abroad
everywhere to smuggle stag beetles.
The market size of the stag beetle commerce isconsidered to be over ten billion Japanese yen (onehundred million US dollars). Many ecologists andentomologists have warned ecological risks that will
be caused by the unprecedented insect business. At
the beginning of the importation of exotic beetles, notonly the general public but also even many entomologists thought that tropical large insects can notpass the winter in Japan even if they escape into thefield. However, most stag beetles in tropical andsubtropical areas actually inhabit in relatively highaltitude, where the climate is not so much different
from that of Japan. Furthermore, almost all stag beetles spend their larval stage in decayed trees or in soilthat are stable habitats. These ecological characteristics suggest that many species of exotic stag beetles
have potential to be naturalized in the Japanese field(Araya, 2002). So we must consider and assess©2004 AIRIES68

K. GOKA et al.

ecological impacts which will be caused by thenaturalization of exotic stag beetles.
Probably the native stag beetles whose ecologicalniche is similar to that of exotic stag beetles willcertainly suffer serious and direct impacts. The wild
populations of Japanese native stag beetles are rapidly
decreasing because of artificial disturbance of habitats
and some species are already close to endangered(Kojima, 2002). Biological invasion by the exotic
stag beetles will accelerate the decay of the native
species.
What impacts will the exotic beetles have? It isthought that the first impact will be competition forfood and habitat, depending on how well the exotic
beetles adapt to the Japanese field. Ecologicalaspects of stag beetles have been little revealed, so wewill need to accumulate ecological data for estimating
the fitness of the exotic beetles. The second impact
will be genetic introgression as a consequence of hybridization between the exotic and the native beetles.
In particular, the exotic stag beetles are imported
mainly from Southeast Asian countries, where many
species and/or populations are genetically closely
related to Japanese stag beetles. The third impact

Fig. 1 An illustration of exotic stag beetles imported into Japan for commerce andtheir distribution in the world.

Fig. 2 The price (US dollars) for an individual stag beetle, Dorcus antaeus, fromeach habitat country, when sold in Japan. Individuals collected from Nepal,
Bhutan and India where insect collecting is prohibited sell for incredibly highprices.

Biological Invasion Caused by Commercialization of Stag Beetles in Japan

will be unknown species of parasites brought by theexotic beetles into Japan, spreading disease among
Japanese beetle populations.
In this paper, we focus on and consider the second
and the third impacts, genetic disturbance and parasite
invasion, based on our on-going investigations. And
through this big insect business we would like to discuss the Japanese values and the status of biodiversity
in Japan.

2. Genetic Diversity among Stag Beetles in
the Japan Islands − the Case of Dorcus
titanusIn this paper we would like to introduce our studyof genetic constitutions in natural populations of aJapanese stag beetle (Dorcus titanus), which is one of
the most popular species in Japan. D. titanus is
widely distributed among the Japan Islands and subdivided into 12 subspecies endemic to each island or
local region based on morphological characters (Fig. 3).
Originally, many Japanese collectors enjoyed themorphological variation among populations and traded
them. D. titanus subspecies and closely related species are also widely distributed on the Asian Continentand the Southeast Asian Islands (Mizunuma & Nagai,1994). These exotic subspecies have come to be
popular among Japanese breeders because of theirlarge body size and unique morphology, and a lot of
individuals have been imported since 1999 (Fig. 4).
As genetic and systematic relationships between

69

the Japanese and the exotic populations have been
little revealed, we cannot estimate the ecological riskof genetic introgression caused by naturalization of
the imported exotic beetles. Thus, a DNA databasefor the stag beetle would be a useful basis for monitoring genetic introgression and furthermore for establishing conservation units not only among Japanese
populations but also among other Asian populations
that are being over-exploited. We are therefore
studying and accumulating variations in nucleotide
sequences in populations of D. titanus collected fromvarious sites in and around the Japan Islands. We
have sequenced 1,948 base pairs of a region of
mitochondrial DNA (mtDNA) including the cytochrome oxidase subunit 1 (CO1) gene and cytochromeoxidase subunit 2 (CO2) gene of each individual.
Figure 5 shows a phylogram illustrating phylogenetic relationships among mtDNA haplotypes in
D. titanus individuals from the Japan Islands using
Thai, Indonesian and Philippine populations as
out-group taxa. The phylogram clearly shows separate lineages corresponding to each phylogeographic
group, with strict geographical distributions. According to the tree, Japanese D. titanus groups wereconsidered to be monophyletic, and the sub-tree wascharacterized by clades, each comprising individuals
from each island.
We are trying to construct the evolutionary
scenario for Japanese D. titanus based on the phylogenetic pattern of the tree. The present data suggestthat the D. titanus population entered Japan repeatedly
during the early geological history of the Japan
Islands when they were linked to and in turn separated
from the Asian Continent. The population probably
became fragmented and isolated into many islandgroups during post-glacial insular isolation. We cansay precisely that Japanese D. titanus populations
were formed along with the formation of the JapaneseIslands.

3. Genetic Diversity in D. titanus Species
Groups throughout Asian Countries

Fig. 3Sub-species of Japanese Dorcus titanus and theirgeographic distribution.

Exactly where, however, did the ancestor ofJapanese D. titanus come from? Analysis of mtDNA
haplotype variation over a wider area may provide theanswer. We have also constructed a phylogram of
mtDNA haplotypes from D. titanus individuals collected in various Asian countries, and included
members of the out-group taxa, D. alcides, D.
eurycephalus, and D. metacostatus (Fig. 6). The tree
indicates that not only Japanese groups but also thosefrom other countries consist of phylogenetic lineages
corresponding to each phylogeographic population.
The Asian D. titanus group was divided into two mainclades. One clade comprised individuals from the
Malay Peninsula, China, Taiwan, the Korean Peninsula, and the Japan Islands, and the other comprised
those from the Indonesian and Philippine Islands.

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K. GOKA et al.

Of course, additional individuals from more sites
must be studied, but the present data suggest an overall evolutionary scenario for the Asian D. titanus
group. An ancestor population of D. titanus occurring around the Malay Peninsula came to be divided
into two groups; one of them migrated northward,
evolving to small sized types; the other advanced
southward, forming subdivided geographical populations having large sized bodies (Fig. 7).
Biodiversity can be defined in terms of genetic

diversity (Avise, 1996; Crozier, 1997). Consequently,
the genetic diversity and localities of D. titanus groups
as determined by the phylogenetic analysis of mtDNA
are issues that should be carefully considered informulating conservation policies. Each clade in thephylogram must be defined as an evolutionarily
significant unit (ESU), because it is composed of a setof populations with a distinct long-term evolutionary
history, in accordance with Ryder’s definition of ESU(Ryder, 1986). However, these unique ESUs of D.

Fig. 4

Exotic D. titanus sub-species and closely related Dorcus species inSoutheast Asia, those are imported into Japan.

Fig. 5A Neighbor-Joining (NJ) tree illustrating the phylogenic relationships
among mitochondrial DNA (mtDNA) cytochrome-oxidase gene (CO)haplotypes (about 2,000bp) extracted from D. titanus in the Japan Islands
and neighboring countries. Thai, Indonesian and Philippine D. titanus areused as out-group taxa.

Biological Invasion Caused by Commercialization of Stag Beetles in Japan

Fig. 6

A Neighbor-Joining tree showing phylogenetic relationships among mtDNA
CO haplotypes (about 2,000bp) of D. titanus collected from various sites in
East and Southeast Asia, including the Japanese Islands. D. alcides,
D. eurycephalus, and D. metacostatus are considered out-groups.

Fig. 7

An evolutionary scenario for the Asian D. titanus group.

titanus can be easily disrupted by genetic introgression as a consequence of hybridisation between localgroups.

4. Frankenstein Stag Beetle Obtained from
Crosses between Exotic and Native
Populations
To test the ability of geographically distant strains
to hybridise, we made crosses in the laboratory
between exotic and Japanese D. titanus that differedconsiderably in body size and mandible morphology.
When a male of the Sumatran strain (90 mm bodylength), which is the most popular strain marketed in

71

Japan, and a female of the Japanese strain (30 mm)
were put together in a plastic case for mating, the maleaggressively pursued the female for mating regardlessof the body-size difference (Fig. 8(a)). The female
resisted mating and was finally killed by the male.
In the reciprocal cross, a male of the Japanese strain(50 mm) was able to mate with a female of theSumatran strain (50 mm), in spite of violent cruelty by
the female (Fig. 8(b)). Hybrid larvae were hatchedand grew to adults. The hybrid males possessedlarge bodies (85 ± 2.5 mm, N = 9) and intermediate
mandible morphology (Fig. 8(c)).
Furthermore,these hybrids were fertile, since crosses between themalso produced progeny. The results of the crossing

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K. GOKA et al.

Ferrell et al., 1980; Brochmann, 1984; Allendorf &Leary, 1988; Lehman et al., 1991; Riesberg, 1991;
Browne et al., 1993; Levin et al., 1996). In the caseof stag beetles, importation of numerous exotic strains
will continue from now on, resulting in higher invasive pressures. Thus, hybridization between strains
will be accelerated.

6. Parasite Invasion Accompanying
Importation of Stag Beetles

Fig. 8 Crossing experiments between Japaneseand Indonesian strains of D. titanus: D.
titanus castanicolor and D. titanus titanus,
respectively.
(a) A male of the Indonesian strain (90 mmlong) pursuing a female of the Japanesestrain (30 mm) for mating. (b) A male of
the Japanese strain (50 mm) suffering
violent cruelty from a female of theIndonesian strain (50 mm). (c) An F1
hybrid male obtained from the crossshown in panel (b). Its body size isappreciably larger (85 mm) than that of its
father.

experiments suggest that there is indeed little
reproductive isolation between exotic and Japanese D.
titanus and that genetic introgression is likely to occur
as a consequence of naturalisation of exotic strains.

5. Signs of Genetic Introgression
We actually did collect individuals in the field inJapan in 2002 that possessed mtDNA from exotic
populations or from far-distant Japan island populations. For example, individuals collected in Fuji
and Sasebo cities possessed the mtDNA haplotype ofThai D. titanus, and individuals collected in Fujisawa
city had the mtDNA haplotype of Sumatran D. titanus.
These beetles possessing exotic DNA had morphological characters different from those of the native
populations, especially in their mandibles. Furthermore, allozyme electromorph data providing nuclear
genotype information indicated that these individuals
were F1 hybrids. Apparently, females transported long
distances for commercialisation escaped into the field
and mated with native males. These observations
strongly indicate that genetic introgression due tocommercialisation and importation has already begun.
Natural hybridization and consequent genetic
introgression have been viewed as deleterious to biodiversity (Avise, 1994). Numerous examples havebeen cited for both plants and animals where rarer
species are considered to be threatened by natural
hybridization with individuals from invasive or
introduced relative taxon (e.g., Heusmann, 1974;

Transportation of parasite invaders will be themost serious impact caused by biological invasion.
As an example, the varroa mite (Varroa destructori),
which is a virulent parasite of the European honeybee,(Apis mellifera), is native to eastern Asia, where it
parasitizes the eastern honeybee (A. cerana)(Oudemans 1904). The mites were introduced into
the Western Hemisphere from Japan through thetransportation of European honeybee colonies. The
mite is now responsible for enormous losses in
European bee colonies worldwide.
As the parasites of stag beetles have been little
investigated, it is very difficult to estimate the ecological risks caused by the invasion of parasites.
However, we actually found many species of mites
attached to commercial exotic individuals. Furthermore, one of them, the Lucanid uropodin mite (Fig. 9)
is considered to be pathogenic to stag beetles. Ourlaboratory test showed that even newly emerged D.
titanus males and D. alcides females weakened and to
died as a result within one month after infection withthis mite (Fig. 10). The biological mechanism of theFig. 9Photographs of Lucaid uropodin mites
attached to a female beetle. The mite has
not been identified yet.

Fig. 10

Photograph of D. titanus male, which
weakened and died after parasitization by
Lucanid uropodin mites.

Biological Invasion Caused by Commercialization of Stag Beetles in Japan

pathogenesis has not been revealed yet and is underinvestigation, but such drastic cases of disease havebeen seldom reported. These observations suggest
strongly enough that commercialization and circulation of stag beetles may cause outbreaks of alien pests
from jungles of Southeast Asia.
Recently, we have also investigated genetic variation of an endoparasitic mite (Coleopterophagous
berlesei), which is one of the most common mites
living on the surface of stag beetles (Fig. 11). We
collected the mite from individuals of native andexotic D. titanus, and analyzed the sequence variationof the mtDNA extracted from them. Just as for the
mtDNA of D. titanus, we are constructing aphylogenetic tree of mtDNA haplotypes in the mite(Fig. 12). The tree indicates genetic divergenceamong the mite’s strains. Furthermore, associationsof the host stag beetle and the parasitic mite phylogenies shows that the mites are considered to be
diverged into strains specific to host strains. Suchhost specificities indicate that associations between
the host and the parasite transcend speciation eventsand are therefore relatively old (Whitfield, 2002;

Fig. 11

Photograph of an endoparasitic mite, Coleopterophagous
berlesei, attached to a male D.
titanus.

Fig. 1273

Perlman et al., 2003). These investigations alsosuggest that the importation and commercialization ofstag beetles will disturb not only the stag beetles’
evolutionary process but also the co-evolutionary
associations between the stag beetles and theirparasites, which will have an unexpected influence on
the native stag beetle populations.

7. What Will Become of JapaneseBiodiversity?
The unusual overheating boom of commercialization of stag beetles symbolizes the status of Japanesebiodiversity. We Japanese are now importing an
incredible number of “live” organisms from various
countries. The total number of live animals imported
into Japan in 2000 and 2001 were recorded as862,365,416 and 729,776,001, respectively, according
to the statistics of declarations for importation
reported by the Department of Treasury in Japan. Amuch larger number of plants and seeds are thought tobe imported every year. Some of these imported
organisms are used for industries, such as agriculture
and forestry, as foods for hatchery fishes and domestic
animals, insects for pollination, natural enemies
against agricultural pests, and so on. Others areimported for the purpose of breeding as pets or
decorative plants.
Many such imported species have escaped andbecome invasive species in the Japanese field (theEcological Society of Japan, 2002), and they arethreatening Japanese biodiversity. Of course, biological invasion is recognized as a serious ecologicalproblem in Japan, and a law for restricting and managing importation of organisms including stag beetles isnow being prepared by the Environmental Agency of

Phylogenetic associations between host D. titanus and parasitic mite
(C. berlesei), based on NJ trees of mtDNA CO gene haplotypes.

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K. GOKA et al.

Fig. 13 The Japanese trade status as a major economic power. Japan buys andimports all natural resources from other countries, consuming thebiodiversity of those countries.

Japan for enactment. However, many Japanese already take the ability to buy any natural resource including pets from other countries for money for
granted (Fig. 13). At the same time, we cannot live
without importation and purchase of natural resourcesfrom other countries. Such an economic status ofJapan will make it difficult to prevent invasions ofspecies. We Japanese have to reconsider the status of
our country in the world economically and ecologically, and be more wary regarding importation oforganisms.

Acknowledgements
We are grateful to the beetle-loving people forcollecting samples. Our study is supported by the
Ministry of the Environment as a Global Environment
Research Programme.
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