29

Species Diversity and Conservation of Mandarina,
an Endemic Land Snail of the Ogasawara Islands
Satoshi CHIBA
Graduate School of Life Sciences, Tohoku University, Aobayama,
Sendai, 980-8578 Japane-mail: s-chiba@mbf.sphere.ne.jp

Abstract
The endemic land snails, genus Mandarina of the Ogasawara Islands, have diversified into
arboreal, semi-arboreal and ground ecotypes. Shell morphologies of Mandarina species have a clear
relationship with their respective ecotypes. In addition, marked geographical variations in morphology
and genes are found within species. Phylogenetic relationships based on mitochondrial DNA(mtDNA) sequences suggests that Mandarina evolved from Euhadra, a genus distributed on themainland of Japan. The inferred phylogeny suggests that similar morphologies and ecotypes appeared
independently and rapidly in different lineages and islands at different times. This rapid evolution produced some incongruities among phylogenetic relationships, morphology, species taxonomy, and thelevel of reproductive isolation. Interspecific hybridization occurs between sympatric species due toenvironmental change, resulting in an admixture of genetic and morphological characteristics. Thesefindings reveal the importance of Mandarina as a model system for evolutionary study. However, apredatory land snail and flatworm have recently been introduced into the Ogasawaras. These predators
may rapidly cause the extinction of Mandarina, and thus, a conservation program is needed for
Mandarina. In the conservation program for Mandarina, species taxonomy should not be used as acriterion for selection of populations for captive breeding because of incongruence among thephylogeny, morphology, ecology, species taxonomy and reproductive isolation. In addition, the dangerof interspecific hybridization should be considered when captive-bred snails are reintroduced into
restored or secure habitat.
Key words: adaptive radiation, conservation, hybridization, Mandarina, Ogasawara Islands

1. Introduction
Organisms in small isolated locations have great
potential in evolutionary studies. Adaptive radiationin endemic organisms inhabiting isolated islands andlakes have been used as general evidence for major
evolution. Examples of such adaptive radiations include Darwin’s finches in the Galapagos Islands,
Hawaiian honey creepers, and African cichlids (e.g.,Lack, 1947; Grant, 1986; Freed et al., 1987; Schliewen
et al., 1994). Detailed studies of the processes andcauses of adaptive radiation of island organisms haveprovided excellent data for understanding the processof character divergence.
The endemic Mandarina land snails of the
Ogasawara Islands offer an exceptional example ofcharacter divergence. Mandarina has diversified
into taxa occupying many habitats, (e.g. arboreal,semi-arboreal, terrestrial, dry, and wet habitats) andshows remarkable diversity in shell and genital morphology (Emura, 1943; Habe, 1969; Minato, 1978;

Chiba, 1996). Shell diameters range from 15 mm to
80 mm, and 17 species including five extinct species
have been described.
The Ogasawara Islands are located in the northwest Pacific, about 1,000 km south of Japan, and they
consist of about 30 small volcanic islands. The biggest island among them is only 25 km2 in area. The
Ogasawara Islands have been entirely isolated fromother regions, and the biota of these islands (plants,
birds, insects and land snails) are characterized byseveral peculiarities as are the biota in other oceanicislands.
In the last 10 years there have been several studies
on the population genetic structure, community
structures, the evolutionary history and the process of
speciation of Mandarina. These studies suggest thatlarge ecological and morphological differences among
the species of Mandarina have evolved despite asmall genetic differentiation among these species.
However, these ecological and morphological differences easily disappear when hybridization occurs

30

S. CHIBA

between different species. Reproductive isolation
among the species is easily broken in Mandarina,
resulting in complex geographical variations in morphology and genetics. In this article, I show how
morphologically and ecologically divergent species
have evolved during a relatively short time, and how
morphologically distinct species have hybridized. In
addition, I describe how rapid diversification andhybridization is causing a problem with regard to theconservation of island organisms such as Mandarina.

2. Divergences in Habitat Preference andMorphology
The Ogasawara Islands are composed of threegroups of islands, the Mukojima, Chichijima, andHahajima groups. Four extant species and fiveextinct species have been recorded in the Chichijima
Group, one extant species has been recorded in the
Mukojima Group and six extant species have beenrecorded in the Hahajima Group. These species are allendemic to each group of islands (Fig. 1). Eachspecies is composed of many local populations with
distinctive shell or genital morphologies. In addition,some parapatric species are producing hybrid zones(Chiba, 1997), and thus, geographical variations of
Mandarina species are markedly complex.
Habitat preference of Mandarina was examinedfor each species in previous studies and the species
were divided into arboreal, semi-arboreal and groundecotypes (Fig. 2) (Minato, 1978; Chiba, 1996). The
arboreal ecotypes were found only in trees. These

included M. suenoae from the Chichijima Islands andM. hahajimana from the middle to northern parts ofHahajima. Most of the arboreal species were foundat a height of more than 1 m from the ground. Semiarboreal ecotypes are found both in trees and on the
ground, and rest between the trunk and leaf or in thespace between thick leaves of pandanus trees or palm
trees when they are inactive. These include M.
hirasei from the Chichijima Islands and M. exoptata
from Hahajima and M. hahajimana from the southernparts of Hahajima, Anejima and Mukoujima. The
ground ecotypes are found on the ground and arenever found in trees. These include three species
from the Chichijima Islands (M. chichijimana, M.
mandarina and M. anijimana), four species from the
Hahajima Islands (M. ponderosa, M. conus, M.
aureola and M. polita), M. hahajimana from
Imotojima and Meijima, and M. trifasciata from the
Mukojima Islands. There are also differences in
preference of microhabitat among the ground ecotypes.
The species that have the exposed-ground ecotype
prefer to rest or forage in more exposed, thinner, dryer
litter than the species that have the hidden-groundecotype (Chiba, 1999b). For example, M. anijimana,
which coexists with M. mandarina in the central partof Anijima, was found in bushes or in forest litter thatwas dominated by leaves of pandanus trees and broadleaved trees, but not in litter dominated by leaves ofpalm trees. M. mandarina was found in all kinds ofhabitat, but it was relatively rare in bushes or in forest
litter that was dominated by leaves of broad-leaved
trees when it coexisted with M. anijimana.

Fig. 1 The Ogasawara Islands, with distributions of species of Mandarina indicated.

Species Diversity and Conservation of Mandarina

Fig. 2

31

Diversity of morphology and habitat use in Mandarina. 1: M. hahajimana N type (Mt. Sakaigatake, Hahajima), 2: M.
aureola (Minamizaki, Hahajima), 3: M. polita (Chibusa-yama, Hahajima), 4: M. hahajimana S type (Minamizaki,
Hahajima), 5. M. exoptata (Chibusa-yama, Hahajima), 6: M. mandarina (Yoake-yama, Chichijima), 7: M. ponderosa N
type (Chibusa-yama, Hahajima), 8: M. suenoae, (Anijima), 9: M. hirasei S type (Takayama, Chichijima).

There is a clear association between ecotypes andshell morphologies (Fig. 3). The shells of grounddwelling snails are consistently thicker and heavier,and have a smaller aperture than those of arboreal orsemi-arboreal populations. Populations with a similar habitat have similar shell morphology. The
remarkable divergence in shell morphology in
Mandarina is associated with the differences in its
habitats (Chiba, 1996). The thinner, larger apertureshells of the arboreal and semi-arboreal populations
are possibly adapted for living in trees because they
allow the snails to adhere better to trunks andleaves. The species with the exposed-ground ecotype
possess flatter and brighter shells than the species withthe hidden-ground ecotype. Shells of species withthe arboreal and semi-arboreal ecotypes are alsobrighter than shells of species with the ground ecotype.
This relationship between shell color and particular
habitats is consistently found in all of the pairs ofground species in Mandarina. Bright shells would
be expected to have an advantage in sites where snails
are largely exposed, because they do not heat up as
much as dark shells in the sunlight. Snails withbright shells would be able to avoid overheating in thesun.

3. Parallel Adaptive Radiation of Mandarina
in the Ogasawara Islands
A comparison between (i) the ecotype and (ii) thephylogenetic relationship of Mandarina species estimated by mitochondrial 16SrRNA and 12SrRNA genesequences suggests that radiation and divergence ofarboreal, semi-arboreal, ground ecotypes have occurred repeatedly at different times and in different areas
and lineages (Chiba, 1999a). The consistent topology between the 16SrRNA and 12SrRNA trees suggests that radiation and divergence of arboreal andterrestrial species first occurred in the Chichijima
Islands. The species migrated to the Hahajima andMukojima Islands from the Chichijima Islands anddiversified on Hahajima, leading to a second radiation.
Divergence of different lineages of arboreal, semiarboreal and terrestrial species occurred repeatedly in
the Hahajima Islands.
Although details of the mitochondrial DNA(mtDNA) tree and the population tree may differ
because of hybridization between different species,
the mtDNA tree suggests that there has been repeateddivergence of arboreal and ground ecotypes, because
no examples have been found of hybridization
between species with the ground ecotypes and those32

S. CHIBA

with the arboreal ecotypes. Species with similarshell morphologies appear repeatedly in different
lineages (Fig. 3) because shell morphologies areclosely related to life habits (Chiba, 1996). Extreme
ecological and morphological differences have beenfound between the arboreal M. hahajimana (N type)
and the ground-dwelling M. aureola (Chiba, 1996).
Phylogenetically, however, these populations are very
close. Large differences in shell forms and life
habits have also been found between (i) phylogenetically close lineages such as M. exoptata and M.
ponderosa and (ii) populations of M. hahajimana (Stype) from Imotojima and Mukoujima (Fig. 3).
Remarkable differences in genitalia occur between

genetically and phylogenetically close species. For
example, the size of the penis of M. chichijimana is no
more than 1/5 that of M. mandarina, but the genetic
distance between these species is only 1.4%. Thissuggests that shell morphology, genital morphology
and the ecotypes of Mandarina have all evolved
rapidly.
There are some incongruities between phylogenetic patterns of mtDNA and species taxonomy (Fig.
3). The species taxonomy of Mandarina is based
mainly on differences in genital morphology (Emura,
1943; Minato, 1978). Therefore, some incongruities
between species taxonomy and the phylogenetic
relationship observed in Mandarina can be attributed

Fig. 3 A neighbor-joining tree for 18 populations of Mandarina on combined sequences of 16SrRNA and 12SrRNA
genes. Numbers above selected nodes are percentage of times in 500 bootstrap replications that populations
occurred in these clades. Bootstrap values lower than 50% were exhibited by (-). Populations with thearboreal ecotype, semi-arboreal ecotype and ground-dwelling ecotype are indicated by green, yellow andblack circles respectively. Distribution of each population are also shown in parentheses (NH: north
Hahajima, MH: middle Hahajima, SH: south Hahajima, Mk: Mukoujima, Im: Imotojima, Na: Nakodojima(Mukojima Islands), SC: south Chichijima, NC: north Chichijima, An: Anijima. (Modified from Chiba,
1999a).

Species Diversity and Conservation of Mandarina

to the rapid morphological evolution of this species
and to convergent evolution. M. hahajimana (Ntype) from the northern part of Hahajima is phylogenetically closer to M. aureola and M. polita thanother populations of M. hahajimana. A similar caseis found in the northern and southern populations of M.
hirasei. The southern populations of M. hirasei are
phylogenetically closer to the Hahajima species thanto other species of Chichijima, and thus, the northernand southern populations of M. hirasei should be
separated as different species. In addition, the
mtDNA tree shows that M. ponderosa (N type) fromthe northern part of Hahajima is phylogeneticallycloser to M. exoptata than to M. ponderosa (S type)from the southern part of Hahajima, and these
populations of M. ponderosa also may be separated as
different species. However, these populations of M.
ponderosa are producing a hybrid zone in the middle
range of Hahajima without assortative mating (Chiba,1993). The incongruence among the morphology,
phylogeny, and condition of reproductive isolation
makes it difficult to determine the taxonomic positionsof these populations.
Mandarina has been generally included in the
Camaenidae and is believed to have evolved from
Camaenid ancestors distributed in southeast China(Minato, 1978). However, a recent study has suggested that Mandarina is not phylogenetically close toCamaenid genera but is closer to Bradybaenid genera(Chiba, 1999a).
Phylogenies based on mtDNA
showed that Mandarina is closest to Euhadra, a genus
from the mainland of Japan (Chiba, 1999a). The
shell and genital morphologies and mating behavior of
Euhadra distinctly differ from those of Mandarina.
For example, Euhadra possess a dart sac, a mucus
gland and complex courtship, all of which are absent
in Mandarina. Mandarina lays a small number oflarge eggs (one to three eggs larger than 1/5 of adultshell size, see Fig. 4), while Euhadra lays a larger
number of smaller eggs (more than 20 eggs smaller

33

than 1/10 of adult shell size). Mandarina has anextremely solid shell. This suggests that Mandarina
has changed its reproductive organs, mating behavior,
egg size, and morphology to such an extent that it has
been placed in a different family. This is also
supported by the occurrence of an extinct species, M.
luhuana, which has a shell morphology similar to thatof Euhadra from Pleistocene deposits on Chichijima.
Although the 16SrRNA sequences of the Mandarina species diverge considerably among the speciesof Mandarina, this does not imply that the diversifycation of Mandarina has a long history, because thedivergence rate of the mitochondrial 16SrRNA geneof land snails is extremely fast, approximately 10%
per Ma (Hayashi & Chiba, 2000; Thacker & Hadfield,2000).
Sequence divergences among sympatric species of
Mandarina from Hahajima (2% - 6%) were mostly
smaller than those among local populations within
species of Euhadra (1% - 14%) (Hayashi & Chiba,
2000; Watanabe & Chiba, 2001). The mean genetic
distance of 16SrRNA between Mandarina andEuhadra (0.188) (Chiba, 1999a) is much smaller thanthe maximum level of intraspecific genetic distance inCepaea nemoralis (0.25) (Thomaz et al., 1994) andAinohelix editha (0.23) (Teshima et al., 2003). These
results imply that the morphological and ecologicalevolution of Mandarina has been accelerated in the
Bonin Islands.
Studies of organisms from remote islands such as
the Galapagos and Hawaii (Carson & Kaneshiro, 1976;
Schluter, 1988, 2000) suggest that morphological andecological divergence is accelerated in depauperateenvironments where competitors and predators arefewer. A rapid morphological and ecological evolution of Mandarina in the Ogasawara Islands, wherecompetitors and predators are fewer than on themainland, is consistent with this view. A rapid ecological divergence has also been reported in Hawaiian
land snails (Thacker & Hadfield, 2000). These findings suggest that a scarcity of sympatric species soonafter the establishment of an island species of landsnail will accelerate its ecological divergence.

4. Interspecific Hybridization

Fig. 4

An adult snail of M. ponderosa and its huge eggs.

Recent studies have shown that the loss or partial
loss of reproductive isolation between sympatricspecies of animals is not as rare an event as was previously thought (Grant & Grant, 1992; Dowling &DeMarais, 1993; Chiba, 1993; Falniowski et al., 1993;
Byrne & Anderson, 1994; see a review by Arnold,1997). Furthermore, such hybridization may havesevere effects on genetic variation in island populations (Johnson et al., 1993; Clarke et al., 1998). The
influence of sympatric hybridization is especiallyserious for organisms with geographically limited
gene flow.
Genetic and morphologic analyses of populations

34

S. CHIBA

of Mandarina suggest that hybridization between
sympatric species has occurred on different islands.
In the middle range of Hahajima Island, hybridization
between M. ponderosa and M. aureola has occurredand a complex admixture of genes of these species has
been created (Fig. 5) (Chiba, 1993). Although mostof these populations are described as M. aureola basedon their genital morphology, the shells have intermediate characteristics between M. aureola and M.
ponderosa. However, such intermediate shells are
not found in the fossil samples (2,000 - 13,000 yearsago) collected from Hahajima except for one locality,
and thus hybridization between these species has
occurred recently (Fig. 6). The past distribution andgeographic variation of M. ponderosa can be traced
from the distribution of M. ponderosa-derived genotypes (Chiba, 1993). For example, populations of M.
aureola in the eastern parts of the middle range of
Hahajima possess marker alleles of M. ponderosa.
M. ponderosa is not distributed in this area at present.
However, fossils of M. ponderosa occur in this area.
Thus, the M. ponderosa alleles in the populations of M.
aureola in this area are derived from M. ponderosa
that has become extinct (Chiba, 1993).
Another example of hybridization is found between the two sympatric species M. mandarina and M.
anijimana on Anijima Island (Chiba, 1998). Intermediate shells and the coexistence of marker alleles
between these species are found in populations occupying transitional zones between forest and shrub.
These findings suggest that some ecologicalfactors are causing a partial breakdown of the reproductive isolation between these species. One plausible scenario is “frequency-dependent” hybridization(Chiba, 1998). If one species is rare at a given siteand cannot find individuals to mate with, it would
mate with individuals of the other sympatric species.

Fig. 5This hypothesis seems to be supported by the fact thathybrids have been found in high frequencies in thetransitional zone between shrub and forest where M.
anijimana becomes rare but M. mandarina isabundant. Although the exact mechanism of reproductive isolation between sympatric species of
Mandarina is not clear, it may depend on pre-zygotic
isolation by a simple ecological difference as has beenshown to be the case with the land snail Partula(Johnson et al., 1977; Murray et al., 1982). Thiskind of isolation would be easily broken and fertile
offspring would be produced.

5. Endangerment of Mandarina and its
Conservation
Human colonization of the islands affects native
wildlife both through habitat destruction and throughthe introduction of domesticated animals and othernonindigenous species. The most prominent cases of
the influence of introduced animals are the extinctionof Partula in Tahiti and the marked decline ofendemic land snail faunas of Hawaii and Mauritius
due to predation by an introduced carnivorous landsnail Euglandina rosea (Clarke et al., 1984; Hadfield,
1986; Murray et al., 1988; Griffiths et al., 1993; Wells,
1995). E. rosea was introduced (Fig. 7) to control a
giant African snail (Achatina fulica), a serious agricultural pest. Although E. rosea was not the solecause of the extinction of native snail species, it was a
critical factor.
Mandarina has suffered serious destruction of
habitat due to cultivation since 100 years ago(Kurozumi, 1988; Tomiyama, 1994). However, themost serious problem is predation by introduced
species. For example, a predatory flatworm, Platydemus monokwari (Fig. 4) was introduced to theGeographical variation in an allozyme locus, Lap-1 and mtDNA (16SrRNA) for M. aureola-M. polita (left)
and M. ponderosa (right).

Species Diversity and Conservation of Mandarina

Fig. 6

Fig. 735

Historical changes in shell morphologies in living and fossil samples of M.
aureola, M. polita and M. ponderosa. The horizontal axis indicates principal
component scores on the second principal component. The scores on theprincipal component were obtained by principal component analysis using 13
shell characters. (Modified from Chiba, 1993).

Introduced predators: a predatory land snail,
Euglandina rosea (upper), and a predatory flatworm,
Platydemus monokwari (lower).

Ogasawaras. This predatory flatworm was introduced to several islands in the Pacific and Indian
Oceans as a biological control agent for Achatina
fulica, and has become a serious threat to the native
gastropod fauna of Guam. Some other predatory
flatworms were also found in the Ogasawaras, andthese flatworms may be one of the causes of the recent
decline in land snail species in the Ogasawaras(Kawakatsu et al., 1999; Ohkouchi et al., 1999;
Tomiyama, 2002). In addition, the carnivorous landsnail Euglandina rosea, that led to the extinction of
the Tahitian snails, was also introduced to Chichijima.
The effect of these introduced predators on native landsnail fauna is so serious that they may rapidly cause
the extinction of many of the native land snails in the
Ogasawaras. The history of disasters caused bythese snails to the land snails of Hawaii, Tahiti andother Pacific islands strongly suggest that the same
sort of disaster will occur with Mandarina in the near
future. A conservation program is needed to avoid
the extinction of Mandarina.
Protection of the native habitat is not enough to
avoid the influence of introduced predators such as
flatworms and Euglandina rosea. The best way toprotect Mandarina and other endemic land snail
species would be to remove all flatworms andEuglandia rosea from the Ogasawaras. However,36

S. CHIBA

the cases of extinction of land snails in the Pacificislands show that it is very difficult to destroy thesealien predators. One approach to avoid the extincttion of Mandarina would be captive breeding. Reintroduction of captive-bred snails into restored or
secure habitats may be one way of preserving
Mandarina. In the case of Partula, more than thousand of these snails are being bred in captivity. The
London Zoological Society released the first captivebred Partula into a protected area on the island of
Moorea in 1994 (Pearce-Kelly et al., 1995).
However, the captive breeding and re-introductionof Mandarina species face several problems. First,
each species of Mandarina is segregated into many
genetically and morphologically different local populations. In addition, these local populations produce
hybrid zones with complex geographical patterns inmorphology and genetics. The best way to recover
the present geographical variation is to collect all of
the populations living in the islands for captive breeding, and after removing the predators, re-introduce thecaptive-bred snails to exactly the same sites where thesnails were collected. Although this program is not
impossible, it is not feasible. Second, the incongruence among morphology, phylogeny, and condition of
reproductive isolation make it difficult to identify
units for captive breeding and select suitable source
populations. For example, taxonomic species should
not be used as a unit of conservation, because a
species of Mandarina includes populations that are
genetically and phylogenetically distant from otherpopulations of the same nominal species. In addition,
a population reproductively isolated from other populations is not necessarily more distantly related tothese populations than a population that is not
reproductively isolated from these populations (seesection 4). Third, reproductive isolation among sympatric species of Mandarina is easily broken byenvironmental change. Human alterations of environmental conditions and habitats have been shown tohave resulted in hybridization in several animals(McDonnell et al., 1978; Harrison & Arnold, 1982;
Hillis, 1988). Changes in habitat conditions andpopulation density through the re-introduction of
captive-bred snails may result in hybridization among
species, and thus, the genetic and morphological characteristics of each species may be lost as a result of
this program. What is most urgent at this time isresearch on the breeding of Mandarina snails in
captivity and at the same time, research on how individuals and populations differ genetically from eachother. If we have genetic information for all populations on the islands, we can reconstruct the genetic
diversity of Mandarina after their extinction in nature,even if we can save only a small part of these
populations.

6. Conclusion
Mandarina provides an excellent natural laboratory in which we can test various ecological theories
because of its high phenotypic diversity and accelerated evolution. In addition, a high level of geographical variation in Mandarina provides an excellent
model system for the study of population genetics andspeciation processes. The divergence of habitat preference among sympatric species and independent
diversification in arboreal, semi-arboreal and groundecotypes in different lineages at different times on
different islands reveal importance of ecologicalfactors in species coexistence and speciation. Hybridization among genetically and phenotypically divergent species suggests that the reproductive isolation of
Mandarina depends on pre-zygotic isolation bysimple ecological differences. These findings should
contribute largely to understanding the process ofadaptive radiation and evolution. However, at thesame time, these findings reveal that it will be difficult
to conduct conservation programs for Mandarina.
Detailed ecological and genetic information as well as
captive breeding is needed to keep the loss of genetic
diversity of Mandarina to a minimum.

Acknowledgments
I express my sincere thanks to K. Tomiyama, A.
Davison, I. Okouchi, T. Oubayashi, I. Hayami and K.
Tanabe for helpful advice and assistance. This study
was supported by grants from the Japan Society for
the Promotion of Science and the Nippon Life
Insurance Foundation.

References(J: in Japanese)
Arnold, M. L. (1997) Natural Hybridization and Evolution,
Oxford University Press, Oxford.
Byrne, M. and M. J. Anderson (1994) Hybridization of
sympatric Patiriella species (Echinodermata: Asteroida) in
New South Wales. Evolution, 48:564-576.
Carson, H. L. and K. Y. Kaneshiro (1976) Drosophila ofHawaii: systematics and ecological genetics. Annual Review
of Ecology and Systematics, 7:311-345.
Chiba, S. (1993) Modern and historical evidence for natural
hybridization between sympatric species in Mandarina(Pulmonata: Camaenidae). Evolution, 47:1539-1556.
Chiba, S. (1996) Ecological and morphological diversifycationand character displacement in Mandarina, an endemic landsnail of the Bonin Islands. Journal of Evolutionary Biology,
9:277-291.
Chiba, S. (1997) Novel color polymorphisms in a hybrid zoneof Mandarina (Pulmonata). Biological Journal of theLinnean Society, 61: 369-389.
Chiba, S. (1998) Genetic variation derived from natural geneflow between sympatric species of land snails. Heredity, 80:
617-623.
Chiba, S. (1999a) Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: evidence from mitochondrial DNA sequences. Evolution, 53:460-471.

Species Diversity and Conservation of Mandarina
Chiba, S. (1999b) Character displacement, frequency-dependent
selection, and divergence of shell colour in land snails
Mandarina. Biological Journal of the Linnean Society,66:465-479.
Clarke, B. C., J. J. Murray and M. S. Johnson (1984) The extinction of endemic species by a program of biologicalcontrol. Pacific Science, 38:97-104.
Clarke, B. C., J. J. Murray and M. S. Johnson (1998) How
molecular leakage can mislead us about island speciation.
In: P. R. Grant, ed., Evolution on Islands, Oxford University
Press, Oxford, pp. 181-195.
Dowling, T. E. and B. D. Demarais (1993) Evolutionary
significance of introgressive hybridization in cyprinid fishes.
Nature, 362: 444-446.
Emura, S. (1943) On the systematic position of the genera
Mandarina and Dolicheulota. Venus, 13:34-38. (J)Falniowsyi, A., A. Kozik and M. Szarowska (1993) Two
common European viviparid species hybridize. American
Malacological Bulletin, 10: 161-164.
Freed, L. A., S. Conant and R. C. Fleischer (1987) Evolutionary
ecology and radiation of Hawaiian passerine birds. TREE,
2:196-203.
Grant, P. R. (1986) Ecology and Evolution of Darwin's Finches.
Princeton University Press, Princeton.
Grant, P. R. and B. R. Grant (1992) Hybridization of bird
species. Science, 256: 193-197.
Griffiths, O., A. Cook and S. M. Wells (1993) The diet of theintroduced carnivorous snail Euglandina rosea in Mauritius
and its implications for threatened island gastropod faunas.
Journal of Zoology, 229: 79-89.
Habe, T. (1969) Mollusca in the Bonin Islands. Iden, 23: 19-25.
(J)
Hadfield, M. G. (2000) A mitochondrial phylogeny of extant
Hawaiian tree snails (Achatinellinae). Molecular Phylogenetics and Evolution, 16:263-270.
Hadfield, M. G. (1986) Extinction in Hawaiian achatinelline
snails. Malacologia, 27: 67-81.
Harrison, R. G. and J. Arnold (1982) A narrow hybrid zone
between closely related cricket species. Evolution, 36:
535-552.
Hayashi, M. and S. Chiba (2000) Intraspecific diversity of
mitochondrial DNA in the land snail Euhadra peliomphala(Bradybaenidae). Biological Journal of the Linnean Society,70:391-401.
Hillis, D. M. (1988) Systematics of the Rana pipiens complex:
Puzzle and paradigm. Annual Review of Ecology and
Systematics, 19:39-63.
Johnson, M. S., B. Clarke and J. Murray (1977) Genetic
variation and reproductive isolation in Partura. Evolution,
31:116-126.
Johnson, M. S., J. Murray and B. Clarke (1993) The ecologicalgenetics and adaptive radiation of Partula on Moorea. In:
D. Futuyma and J. Antonovics, eds., Oxford Surveys in
Evolutionary Biology, 9. Oxford University Press, Oxford,
pp. 167-238.
Kawakatsu, M., I. Okochi, H. Sato, T. Ohbayashi, K. Kitagawa
and K. Totani (1999) A preliminary report on land planarians(Turbellaria, Seriata, Tricladida, Terricola) and land Nemertine(Enopla, Hoplonemertea, Monostylifera) from the Ogasawara
Islands. Occ. Publ., Biol. Lab. Fuji Women’s College, Sapporo(Hokkaidô), Japan, (32): 1-8.

37

Kurozumi, T. (1988) Species composition and abundance ofland mollusks and factors affecting their extinction in the
Ogasawara (Bonin) Islands. Ogasawara Research, 15:
59-109. (In Japanese with English summary)Lack, D. (1947) Darwin’s Finches. Cambridge University Press,
Cambridge.
McDonnell, L. J., D. F. Gartside and M. J. Littlejohn (1978)
Analysis of a narrow hybrid zone between two species of
Pseudophryne (Anura: Leptodactylidae) in south-eastern
Australia. Evolution, 32:602-612.
Minato, H. (1978) Speciation of the genus Mandarina from theBonin Islands (Pulmonata, Camaenidae). Mem. Natn. Sci.
Mus. Tokyo, 11:37-51. (In Japanese with English summary)
Murray, J., M. S. Johnson and B. C. Clarke (1982) Microhabitat
differences among genetically similar species of Partula.
Evolution, 36:316-325.
Murray, J., E. Murray, M. S. Johnson, and B. C. Clarke (1988)
The extinction of Partula on Moorea. Pacific Science,
42:150-153.
Okouchi, I., T. Satou and T. Oubayashi (1999) Does a flatworm
cause extinction of land snails in Ogasawra? Proceedingsof the 46s meeting of Japanese Society of Ecology, p.250. (J)Pearce-Kelly, P., G. Mace and G. Clarke (1995) The release of
captive bred snails (Partula taeniata) into a semi-naturalenvironment. Biodiversity and Conservation, 4: 645-663.
Schliewen, U. K., D. Tautz, and S. Paabo (1994) Sympatricspeciation suggested by monophyly of creater lake cichlids.
Nature, 368:629-632.
Schluter, D. (1988) The evolution of finch communities on
islands and continents: Kenya vs Galapagos. Ecological
Monograph, 58:229-259.
Schluter, D. (2000) The Ecology of Adaptive Radiation.
Oxford University Press, Oxford.
Teshima, H., A. Davison, Y. Kuwahara, J. Yokoyama, S. Chiba,
T. Fukuda, H. Ogimura and M. Kawata (2003) The evolutionof extreme shell shape variation in the land snail Ainohelix
editha: a phylogeny and hybrid zone analysis. Molecular
Ecology. (in press)
Thomaz, D., A. Guiller and B. Clarke (1996) Extreme divergence of mitochondrial DNA within species of pulmonate
land snails. Proceedings of Royal Society of London B,
263: 363-368.
Tomiyama, K. (1994) Extinction and conservation of landsnails in the Ogasawara Islands: Factors for extinctions ofland snails in the Ogasawara Islands. Venus, 53:152-156. (InJapanese with English summary)Tomiyama, K. (2002) Land snails in Ogasawara: endangered
endemic species of oceanic islands and factors of their
extinction. Shinrin-Kagaku, 34:25-28. (J).
Watanabe, Y. and S. Chiba (2001) High within-population
mitochondrial DNA variation due to microvicariance andpopulation mixing in the land snail Euhadra quaesita (Pulmonata, Bradybaenidae). Molecular Ecology, 10:2635- 2645.
Wells, S. M. (1995) The extinction of endemic snails (genus
Partula) in French Polynesia: is captive breeding the only
solution? In: E. Alison Kay, ed., The Conservation Biology of
Molluscs. IUCN Species Survival Commission, World
Conservation Union, pp. 25-28.

(Received on 20 March 2003, Accepted on 4 July 2003)