and Amphibians of the Ryukyu Archipelago and

12 Pages·2008·1 MB·English

TROPICS Vol. 10 (1): 5L-62 Issued May 30, 2000
The Curent Geographic Faunal Pattern of Reptiles
and Amphibians of the Ryukyu Archipelago and
Adjacent Regions
Hidetoshi Ou Tropical Biosphere Research Center, University of the Ryukyus, Nishihara,
Okinawa 903-0213, Japan
ABSTRACT The Ryukyu Archipelago accomrhodates 52 native species/subspecies (26 genera
belonging to ten families) of tenestrial reptiles and 22native species/subspecies (ten genera belonging to
six families) of amphibians. This paper reviews the geographic similarity and diversity pattemJoflhe
current herpetofauna of the Ryukyus and adjacent regions, and discusses factors influencing the
formation of it in this archipelago. Cluster analyses of similarity indices for both reptiles and amphibians
indicate that the Ryukyu herpetofauna is strongly influenced by geohistory ofthis archipelago involving
long isolation especially in its north-cenhal part (i.e., southem Tokara, Amami, anA Oiinawa Groupsf
Correlation analyses suggest that the faunal diversity on each island is significantly influenced by iis
habitat diversity as reflected by the island area (for reptiles) or height (amphibians).
Key words: herpetofauna / isolation / paleogeography / habitat diversity
The Ryukyu Archipelago is an assemblage of old continental islands located in the humid subtropical
area of the western Pacific (Takara, 1962l' Kizaki, 1985: Fig. 1). This archipelago accommodates a
diverse biota including various reptiles and amphibians (e.g., Ikehara & Kato, 1997).
Several previous authors have analysed the Ryukyu herpetofauna (e.g., Inger, L947; Koba, 1962;
Kuramoto, 1979) and argued the predominaace of Oriental elements (i.e., taxa having closest relatives
in southeastern China and Southeast Asia) over Palearctic elements (i.e., those most closely related to
taxa in the main-islands of Japan and eastern China). Since then, a number of taxonomic changes have
been made for the Ryukyu herpetofauna as a result of discoveries of new taxa, as well as of
philosophical and methodological improvements of biological systematics [see Ota (2000) for
example].
In this paper, I briefly review the geographic similarity and diversity patterns of the current
herpetofauna of the Ryukyu Archipelago and adjacent regions by incorporating information recently
added to our knowledge. I then discuss factors influencing the formation of that herpetofauna in this
region.
H. OtA
52
GaP*-
Tokara
-}-
rokara Group
C
\.o Amami GrouP
'
/ t SeKnerkamaakuua-\ p \r -'nkinawa Group
I Group -; \
' A \. "N MiYako GrouP
tai{ant \ YaeYamaGrouP
Fig. 1. Map of East Asia showing
.b \ /. the location of the RYukYu
\a Archipelago.
HERPETOEATJNAL DIVERSITY OF TIIE RYUKYU ARCHIPEI,AGO
The native herpetofauna of the Ryukyus (here defined as an assemblage of continental islands located
between the Tokara Tectonic Strait and the Yonaguni Strait) consists of 52 species/subspecies (26
genera belonging to ten families) of terrestrial reptiles and 22 species/subspecies (10 genera belongrng
to six families) of amphibians (Tables 1 and 2). These numbers, respectively, correspond to 68'4Vo and
36.7Vo ofthe total numbers of native tenestrial species/subspecies of reptiles and amphibians so far
known from the whole Japan. These values are surprisingly high, especially when considering the fact
that in area the Ryukyu Archipelago constitutes only about Llo of the whole Japan.
GEOGRAPHIC PAITERN OF EAUNAL SIMII,ARITY
Biogeographical subdivision of the Ryukyu Archipelago. Based on the geographic pattern of
endemism in the terrestrial reptiles and amphibians, the Ryukyu Archipelago as defined here could be
divided into six areas (Hikida & Ota, 1997; Ota, 1997, 19982 note that these works incorporated the
Daito Group, an assemblage of purely oceanic islands southeast of the Ryukyu Arc, into the Ryukyu
Archipelago): Area I, a few small islands of the Tokara Group south to the Tokara Strait; Area II'
northern half of the Amami Group; Area III, the Okinawa Group, including a few islands "politically"
Geographic faunal pattern of reptiles and amphibians of the Ryukyus 53
Table 1. Terrestrial reptiles of Japan. Their occurrences in Taiwan and Fujian (southeastern
continental China) are also indicated. Data are taken from Hikida & Ota (L997) and Ota (1998),
with slight modifications as indicated in foot-notes. Asterisks (*) denote populations of artificial
origins. Abbreviations are: MJ, the Main-islands of Japan and adjacent islands (including the lzu
Group and the Tsushima Islands); TK, Tokara Group south of the Tokara Tectonic Strait; AM,
Amami Group; OK, Okinawa Group; MY, Miyako Group; yy, yaeyama Group; SE, Senkaku
Group; DA, Daito Group; oG, ogasawara and Iou Groups; TW, Taiwan; FJ, Fujian (the province
of continental China nearest to Taiwan).
Ryukyu Archipelago
MJ TK AM OK MY YY SE DA OG TW FJ
TESTUDINES
Bataguridae
Chinemys reevesii +l +*
C i s to c le mmy s fl av om a r ginata
Ci. f. evelynae
Geoemyda japonica
Mauremys japonica +l
M. mutica
M. m. mutica +*
M. m. kami +* +* +*
Emydidae
Trachemys scripta
2" s. elegans +*l +* +* +*
Trionychidae
Pelodiscus sinensis +1 +* +* +* +*
LACERTILIA
Agamidae
Japalura polygonata
J. p. polygonata
J. p. ishigakiensis
Eublepharidae
Goniur osaurus kur oiwae
G. k. kuroiwae +
G. k. orientalis
+
G. k. splendens
G. k. toyamai
+
G. k. yamashinge +
Gekkonidae
Gehyra mutilata
Gekko japonicus +1
Gk. hokouensis +1 + +
Gk. tawaensis +l
Gk. yakuensis +l
H emidacty lus bow rin gii + + +
Hd. frenatus +* +* +* +* +* +* +*
H emiphy llodacty lus typus +* +* +{'
Lepidodacty lus lugubris +* +{' +* + +{'
Perochirus ateles
+
Iguanidae
Anolis carolinensis +* +*
Lacertidae
Lacerta vivipara
54 H. Ora
Ryukyu Archipelago
MJ TK AM OK MY YY SE DA OG T'TW FJ
Takydromus amurensis
T. dorsalis
T. smaragdinus
T. tachydromoides +1
T. toyamai
Scincidae
At euchos aurus p ellop leurus +t
C ry p tob I epharu s b outonii
C. b. nigropunctatus
Eumeces barbouri
E. elegans
E. kishinouyei
E. latiscutatus +t
E. marginatus
E. okadae
E. stimpsonii
Emoia atrocostata
Scincella boettgeri
S. formosensis +2
S. vandenburghi +
SERPENTES
Typhlopidae
Ramphotyphlops br aminus +*l +*
Colubridae
Achalinus formosanus
A. f. chigirai
A. spinalis +t
A. werneri
Amphiesma concelarum
Am. ishigakiense
Am. pryeri
Am. vibakari
Am. v. vibakari +1
Am. v. danioense +
Calamaria Pavimentata
C. p. miyarai
C. pfefferi
Cyclophiops herminae
Cy. semicarinatus
Dinodon orientale +t
D. rufozonatum
D. r. rufozonatum
D. r. walli
D. semicarinatum
Elaphe carinata
E. c. carinata
E. c. yonaguniensis
E. climacophora +t
E. conspicillata +t
E. quadrivirgata +1
E. taeniura
E. t. friesi +*
E. t. schmackeri
Geographic faunal pattern of reptiles and amphibians of the Ryukyus 55
Ryukyu Archipelago
MJ TK AM OK MY YY SE DA OG TW FJ
Lycodon ruhstrati
L. r. multifasciatus
Opi sthot r opis kikuzatoi
Pareas iwasakii
Rhabdophis tigrinus
R. t. tigrinus +l
Elapidae
Hemibungarus j aponicus
H. j. japonicus
H. j. boettgeri
j.
H. subsp.
H. macclellandi
H. m. iwasakii
Viperidae
A gki s tr o do n b I omhoffii +1
A. tsushimaensis +
Trimeresurus elegans +*
T. flavoviridis +
T. mucrosquamatus +{'
T. tokarensis
Ovophis okinavensis +
1, Distributed in Kyushu (including the Osumi Group),
2, S.-L. Chen, unpublished data.
regarded as the southern half of the Amami Group; Area IV, the Miyako Group; Area V the yaeyama
Group; and Area VI, the Senkaku Group.
Of these, Area I accommodates seven species of terrestrial reptiles, including one endemic snake
(Trimeresurus tokarensis), and only a single amphibian species (Buergeria japonica). In Area II, L9
species of terrestrial reptiles and 12 species of amphibians are distributed, of which two reptiles
(Goniurosaurw karoiwae splendens and Hemibungarus japonicus japonicus) and three amphibians
(Rana amamiensis, Babina subaspera, and Rhacophorus viridis amamiensis\ are endemic to this
region. Area III accommodates 3L terrestrial reptiles including six endemic species/subspecies
(Geoemyda iaponica, Goniurosaurus k kuroiwae, G. k orientalis, G. k yamashinae, G. k toyamai,
and Opisthotropis kifuzatoi), and 15 amphibians including four endemic species/subsp ecies (Rana
narina, R. namiyei, B. holsti, and Rhacophorus v. viridis). Of the species/subspecies not strictly
endemic to the Area III, 1.1. reptiles (Japalura polygonata polygonata, Ateuchosaurus pellopleurus,
Eumeces barbouri, Talcydromus smaragdinus, Dinodon semicarinatwn, Cyclophiops semicarinatus,
Amphiesma pryeri, Achalinus wemeri, Hemibungarus japonicus boettgeri, Trimeresurus flavoviridis,
and Ovophis okinavensis) and five amphibians (Cynops ensicauda, Tllototriton andersoni, Hyla
hallowellii, Rana okinavana, and R ishikawae) are exclusively shared with Area II, or Areas I and IL
In Area Iv 19 terrestrial reptiles including three endemic species (Tatqtdronus toyanai,
Calatnaria pfefferi, and Amphiesma concelarum) and three amphibians including one endemic
subspecies (Bufo gargarizans miyakonis) are distributed. Area V accommodates 27 species/subspecies
of terrestrial reptiles and L0 species of amphibians, of which lL reptiles (Cistoclemmys
flavomarginata evelynae, Mauremys mutica kami, Eumeces stimpsonii, Talrydromus dorsalis,
Calatnaria pavimentata miyarai, Pareas iwasakii, Etaphe carinata yonaguniensii, Amphiesma
56 H. Ore
Table 2. Amphibians of lapan. Their occurrences in Taiwan and Fujian (southeastern continental
China) are also indicated. Data were taken from Kuramoto (1996: for Japanese urodelans),
Maeda & Matsui (1999: for Japanese anurans), and Zhao & Adler (1993: for Taiwanese and
Fijian species), with modifications as indicated in foot-notes. Asterisks (*) denote populations of
artificial origins. Abbreviations are: MJ, the Main-islands of Japan and adjacent islands
(including the Izu Group and the Tsushima Islands); TK, Tokara Group south of the Tokara
Tectonic Strait; AM, Amami Group; OK, Okinawa Group; MY, Miyako Group; YY, Yaeyama
Group; SE, Senkaku Group; DA, Daito Group; OG, Ogasawara and Iou Groups; TW, Taiwan; FJ,
Fujian (the province of continental China nearest to Taiwan).
Ryukyu Archipelago
MJ TK AM OK MY YY SE DA OG TW FJ
URODELA
Hynobiidae
Hynobius abei +
H. boulengeri +1
H. dunni +l
H. hidamontanus +
H. kimurae +
H. lichenatus +
H. naevius +l
H. nebulosus +l
H. nigrescens +
H, okiensis +
H. retardatus +
H. stejnegeri +l
H. takedai +
H. tenuis +
H. tokyoensis +
H. tsuensis +
Ony cho dacty lus i aPonicus +
S alamandr e I la key s e r lin gii +
Cryptobranchidae
Andrias iaponicus +1
Salamandridae
Cynops ensicauda
C. pyrrhogaster +1
Ty lototriton ander s oni
ANURA
Bufonidae
Bufo gargarizans
B. g. miyakonis +* +*
B. japonicus
B. j. iaponicus +l
B. i. formosus +
B. marinus +* +* +*
B. torrenticola
Hylidae
Hyla hallowellii
H. japonica +1
Ranidae
Babina holsti
B. subaspera
Geographic faunal pattern of reptiles and amphibians of the Ryukyus 57
Ryukyu Archipelago
MJ TK AM OK MY YY SE DA OG TW
FJ
amamiensis
Rana +
R. catesbeiana +* +* +* +* +*
R. dybowskii +
R, ishikawae + +
japonica
R. +t
R. limnocharis +t + + +* + +
R. narina +
R. namiyei +
R. nigromaculata +r +
R. okinavana + +
R. ornativentris +l
pirica
R. +
R. porosa
R. p. porosa +
R. p. brevipoda +
R. psaltes + +
R. rugosa +1
sakuraii
R. +
supranarina
R, a
R. tagoi
R. t. tagoi +r
yakushimensis
R. t, +1
R. tsushimensis +
R. utsunomiyaorum +
R.sP. +
+
Rhacophoridae
Buergeria buergeri +t
B.japonica + + + +
+
Chrixalus effingeri +
+
Polypedates leucomystax +.
Rhacophorus arboreus +
owstoni
R, +
schlegelii
R. +t
R. viridis
R. v. viridis +
R. v. amamiensis +
Microhylidae
Microhylaornata + + + + +
+
I, Distributed in Kyushu (including the Osumi Group).
ishigakiense' Achalinus fornosanus chigirai, Hemibungarus macclellandi iwasakii, and Trimeresurus
elegans) and three amphibians (Rana supranarina, R utsunomiyaorwn, and Rhacophorus owstoni)
are endemic to this area. Of the remainder, seven species/subspecies of reptiles (Japalura polygonata
ishigakiensis, Eumeces kishinouyei, Scincella boettgeri, Elaphe taeniura schmackeri, Dinodon
rufozonatunt walli, Lycodon ruhstrati multifasciatus, and Cyclophiops herminae) and one undescribed
Rana (toda et al., 1997; Maeda and Matsui, 1999) are exclusively shared with Area IV. Area VI
accommodates six terrestrial reptiles, all common to Taiwan and mostly to continental China. Of
these, only two are also shared with other parts of the Ryukyu Archipelago. No amphibians are known
fromArea VI.
58 H. Ore
AMPHI BIA REPTILIA
I I
0.0 0.5
Fig.2. UpGMA (Sneath & Sokal, 1973) clusters on the basis of pairwise values of Nomura'Simpson's
similarity index for amphibian fauna (left) and reptile fauno (right) in the Ryukyu Archipelago
and a{iacent regions.
Faunal shnilarities cmong geographic units recognized in the Ryulcyus and adiacent regions.
Analyses using pairwise values of the Nomura-simpson's similarity index (the number of
species/subspecies common to two communities in comparison divided by the total species/subspecies
number in the smaller community) for indigenous terrestrial reptile fauna and amphibian fauna
yielded clusters that are almost identical in topology (Fig. 2). In reptiles, the faunal similarity is
greatest between Area VI and Taiwan, followed by Areas I, II and III, and then by Areas IV and V'
The Area Vl-Taiwan cluster is first connected with a cluster of southeastertr continental China, and
then with the Areas IV-V cluster and the Areas I-I[ cluster in order. Kyushu is most distant from all
other geographic units considered in the analysis. The cluster for amphibians, excluding Areas I and
VI due to the scarcity or complete absence of representatives (fable 2), shows identical topology with
the reptile cluster except for the initial connection of Taiwan with the Areas IV-V cluster rather than
with southeastern continental China. Branches in the cluster for amphibians are mostly longer than
corresponding branches in the cluster for reptiles.
EACTORS INFLUENCING THE ALPHA DIVERSITY OF REPTILES
AND AMPHIBIANS ON ISI.AI\TDS OF THE RYUKYUS
In the theory of island biogeography (MacArthur & Wilson, 1967), the alphd divetsity (i'e', the
number of species/subspecies) of fauna on a given island is generally expected to be a function of size
and distance from the faunal source of the island. There is, however, apparently little doubt that the
Geographic faunal pattern of reptiles and amphibians of the Ryukyus 59
B
go gd
#C' tC'
o
ro- rots
.Loo oLo
zJ z5
Area (kma) Hclght (m)
Fig.3. Relationshlps between the number of species/subspecies, and island area 16,; aa6
island height @) in rcptiles (circles) and amphibians (triangles) of the Ryukyu
Anchipelago.
diversity of reptiles and amphibians within the Ryukyus does not sirnply correlate with the distance
from their hypothetical sources (southeastern continent for most lineages, and Kyushu and eastern
cotrtinent for the remainder: Hikida & Ota, 1997; Ota, 1998). I thus limit my investigations here to the
influence of island size, as expressed by area ltmz; ana maximum height (m), on the faunal diversity.
Tlvelve islands, for which the herpetofauna has been well documented on the basis of field
suryeys, were selected from the northern, central, and southern Ryukyus. These are: Takarajima of the
Tokara Group, Amamioshima, Tokunoshima and Okierabujima of the Amami Group, Okinawajima,
Tokashikijima and Kumejima of the Okinawa Group, Miyakojima of the Miyako Group, Ishigakijima,
kiomotejima and Yonagunijima of the Yaeyama Group, and Uotsurijima of the Senkaku Group. Areas
and maximum heights of these islands are taken from Takara (1962). Analysis was carried out to test
the significance of correlation between the number of species/subspecies and each island dimension,
both as log-transformed.
In reptiles, the number of species/subspecies (Y) is significantly conelated with the island area
(X) (Y = OJ6TX + 0.783: r = 0.7'1.6, t = 3.24, P < 0.01), whereas it shows no correlation with the
island height (r = 0.412, t = 1.43, P > 0.05). The number of amphibian species/subspecies is
significantly correlated with both island area (Y = 0.189X + 0.4O2) and heighr (y = 0.896X - l.4g').
Nevertheless, the significance level is much higher with height (r = 0.896, t = 5.33, p < 0.001) than
with area (r = 0.603, t=2.OO, P < 0.05) (Fig.3).
GENERAL DISCUSSION
Results of cluster analyses of faunal similarity in reptiles and amphibians largely confirm a
geographic pattern assumed by some previous authors (e.g., Koba, 1962; Kuramoto, 1979; Hikida er
al., 1989; Hikida & ota, 1997; ota, 1997). such a pattern is also analogous with the
phylogeographical pattern illustrated by a number of reptile and amphibian lineages, which could be
H. OtA
summarized as: (((Area VI, Taiwan, eastern continent)(Area IV, Area V))(Atea I, Area II, Area
III))Kyushu. The latter is considered to reflect a spatiotemporal pattern of vicariance in the Ryukyus
and adjacent regions, which involves the effective geographic isolation first for Kyushu, and then for
Areas I-III, Areas IV-Y and Area Vl-Taiwan-continental China in order (Hikida & Ota, L997; Ota,
1998; Hikida & Motokawa, 1.999; Toda et al., 1999; Yasukawa & Ota, 1999). Resuls of the present
faunal analyses indicate that such paleogeographical events have significantly influenced the
formation of the cunent faunal pattern.
Each branch in the amphibian cluster is longer than the conesponding branch in the reptile cluster.
This indicates a lesser similarity in the amphibian fauna between the areas designated above, and
suggests that the straits separating those areas have functioned as isolation barriers more effectively
for amphibians than for reptiles (but see Toda et al. ll99711 for an example of extensive oversea
dispersals by afrogRana limnocharis in the Ryukyus).
Results of correlation analysis indicate that in reptiles alplw diversity on an island of the Ryukyus
largely depends on its area, but not on its maximum height. This is concordant with results of a few
other studies dealing with the reptile fauna in other island groups (e.g., Perry et al',1998i Woinarski et
a1.,I999), suggesting that area is a good predictor for the diversity of habitats available to reptiles on
an island. On the other hand, present results indicate a stronger correlation of the number of
amphibian species/subspecies with maximum height rather than with area of an island. This predicts a
stronger association of the maximum height with the diversity of habitats available to amphibians on
an island. Apparent greater prevalence on lower islands of the Ryukyu limestone bed (Kizaki' 1985),
which easily absorbs the surface water and thus possibly reduces the diversity of inland water habitats
(Toyama, t976; Ota, 1983), may explain such an association. Further analyses using data for more
islands and additional parameters reflecting the habitat diversity (e.g., vegetation complexity:Petry et
al.,1998\ are strongly desired to verify these assumptions.
ACKI\OWLEDGMENTS I wish to express my sincere thanks to Tsutomu Hikida, Masafumi
Matsui, Mamoru Toda, Junko Motokawa, Yuichirou Yasukawa, and many other colleagues in Kyoto
University and the University of the Ryukyus for stimulating discussions and for provision of
pertinent literature, and to Hiroyuki Otsuka, Mitsuru Hotta, and other members of the executive
committee for inviting me to the International Symposium, "The Ryukyu Islands: Arena of Adaptive
Radiation and Extinction of Island Fauna" (6-7 November 1998, at Kagoshima University), in which I
gave a major part of this paper. I am also much indebted to Szu-Lung Chen for his permission to refer
to the results of his study on the East Asian Scincellc in advance of their publication, to T. Hikida for
helping with preparation of a map of the Ryukyus for Fig. 1, and to H. M. Smith and an anonymous
reviewer for critical reading of the manuscript.
This research was partially supported by a grant from the Fujiwara Natural History Foundation,
Grants-in-Aid from the Japan Ministry of Education, Science, Sports and Culture (C-09839024 and
1183301.3 ro H. Ota), and U.S. National Geographic Society grant (No. 4505-91 to M. Matsui).