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The discovery of Mauremys iversoni-like turtles at a turtle farm in Hainan Province, China: The counterfeit golden coin

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2001 Asiatic Herpetological Research Vol. 9, pp. 71–76
© 2001 by Asiatic Herpetological Research
Introduction
Mauremys iversoni Pritchard and McCord 1991 is one
of ten new Chinese chelonians described from speci-
mens purchased through the pet trade since 1987.
From the beginning, our knowledge of this species’
geographical distribution has been fraught with confu-
sion. The type specimen of Mauremys iversoni (UF
71866; institutional abbreviations follow Leviton et
al., 1985) and 19 other individuals are reported to
have come from Fujian province (Fig. 1a), but eight
additional specimens from a locality in Guizhou (over
1000 km away) were also reported (Fig. 1b). Prit-
chard and McCord (1991) propose two hypotheses to
explain this disjunct distribution: 1) The distribution
is (or was) continuous between these localities; 2)
One of the localities (perhaps the type locality) is the
result of turtles being relocated by traveling Bud-
dhists.
An additional wrinkle is provided by Iverson and
McCord (1994) who suggest that the type series of
Mauremysguangxiensis” (=“Clemmys guangxien-
sis” Qin 1992) from Guangxi (Fig. 1c) is actually a
composite of Mauremys mutica and Mauremys iver-
soni-like specimens. However, some differences
between the M. “guangxiensisiversoni-like speci-
mens, the Guizhou M. iversoni specimens, and the
Fujian M. iversoni specimens have been noted (Prit-
chard and McCord, 1991; Iverson and McCord,
1994). The result is the occurrence of different-look-
ing M. iversoni-like turtles from three disparate
regions in China between the years of 1986 and 1991
(Fig. 1). Based on observations from a breeding facil-
ity located on Hainan Island (Fig. 1d), we propose a
third hypothesis that might explain all of the available
data and possibly alleviate much of the confusion: All
Mauremys iversoni-like turtles are the result of the
The Discovery of
Mauremys iversoni
-like Turtles at a Turtle Farm in Hainan
Province, China: The Counterfeit Golden Coin
JAMES FORD PARHAM
1
AND HAITAO SHI
2
1
Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA, email:
parham@socrates.berkeley.edu.
2
Department of Biology, Hainan Normal University, Haikou City, Hainan
Province 571158, China
Abstract.- During a visit to a turtle farm in Hainan Province, we discovered turtles that closely resemble
Mauremys iversoni. The Mauremys iversoni-like turtles at the turtle farm were intentionally produced hybrids of
two commonly reared species, Mauremys mutica and Cuora trifasciata. According to the turtle farmer, the
intentional production of hybrids between these two turtles is a common practice. The hybrids fetch extremely
high prices (~1000 USD/kg) since they are sold as Cuora trifasciata, the “golden coin” turtle, to unsuspecting
buyers. We suggest, but cannot prove, that all Mauremys iversoni-like turtles might be turtle farm hybrids. This
hypothesis could explain all of the available evidence and could alleviate a lot of the confusion surrounding this
species unusual geographical distribution, sudden appearance in the pet trade, as well as its variable morphology.
Key words.- Turtles, Bataguridae, Geoemydidae, Mauremys, Cuora trifasciata, Mauremys iversoni, China,
Hainan, hybrids, turtle farm
Figure 1. The reported localities of
Mauremys iversoni
-
like turtles in China: A) Type locality, Nanping, Fujian
Province (Pritchard and McCord, 1991); B) Kweiying,
Guizhou Province (Pritchard and McCord, 1991); C)
Nanning, Guangxi Province (Qin, 1992); D) Tunchang,
Hainan Province (This study).
Vol. 9, p. 72 Asiatic Herpetological Research 2001
hybridization of Mauremys mutica and Cuora trifasci-
ata in captivity.
Chinese turtle farms
The role of turtle farms in the Asian turtle trade is
often overlooked. The primary reason for this is the
secrecy of the turtle farmers themselves. Despite our
ignorance, the practice of farming turtles in China is a
widespread, lucrative endeavor. As far back as 1991,
Zhou and Zhou report that Cuora trifasciata is being
bred “everywhere”. In the past ten years, the number
of turtle farms is rumored to have increased dramati-
cally. Although it is not possible to provide exact
numbers, there are estimated to be at least ten breed-
ing facilities on Hainan alone. In an attempt to assess
the impact of this burgeoning business to the Asian
turtle trade, one of us (HS) has gained access to a
large turtle farm in Tunchang, Hainan province (Fig.
1d) from 1996 to the present. This paper represents
the second report of this effort (see also Shi and Par-
ham, 2001).
According to the owner of the turtle farm, the Tun-
chang breeding facility was first established in 1983.
The foundation of its breeding stock came from doz-
ens of wild collected Cuora trifasciata, Mauremys
mutica, and Ocadia sinensis from Hainan as well as
additional specimens from a farm in Guangdong that
was established in 1978. It currently houses an esti-
mated 15,000+ geoemydids. Early on, the number of
breeding ponds and turtles was limited and the estab-
lishment of breeding stocks proceeded without clear
aim. Almost all the local species of turtles were col-
lected from the field or bought from villagers and
often kept in the same pond or enclosure.
In November of 1999, the authors visited a smaller
facility that included several indoor breeding ponds.
Although numerous species were observed, Maure-
mys mutica and Cuora trifasciata were the most abun-
dant. Many of the C. trifasciata were kept separately,
but one pond included C. trifasciata, M. mutica, and
even a Chelydra serpentina. When asked if any of the
turtles ever hybridized, the workers of the farm pro-
duced several animals that closely resembled Maure-
mys iversoni. One of these hybrids, a subadult male,
was procured as a voucher (MVZ 230475; Fig. 2, 3h).
JFP was given permission to photograph two other
hybrids (Fig. 3e,f).
The turtle farm hybrids
As with the three previously reported incidences of M.
iversoni (Fujian, Guizhou, and Guangxi), there are
some differences in the Hainan farm specimens.
Unfortunately, it is difficult to understand these differ-
ences because of inconsistencies in the reporting of
previous measurements, small sample sizes, and the
fact the most important specimens remain in private
hands. For example, Pritchard and McCord (1991)
present bivariate plots of measurements for adult
Mauremys iversoni, but inexplicably include only five
of the adult males. It is not stated from which locality
(Fujian or Guizhou) these specimens are from or why
the measurements of all 10 of the adult males from
Fujian (the type locality) are not included. Table 1 of
Pritchard and McCord includes 10 shell measure-
ments for all the specimens, but excludes the two
Figure 2. An intentionally produced hybrid from a Chi-
nese turtle farm (MVZ 230475) that closely resembles
Mauremys iversoni
. Photo by JFP.
Figure 3. A comparison of
Mauremys iversoni
plastra
from the type description with turtle farm hybrids and
putative parental species: A)
Mauremys mutica
from a
turtle farm in Tunchang, Hainan Province (MVZ
230477); B-D)
Mauremys iversoni
from the type
description. They are either from Fujian or Guizhou
Province; E-F) Intentionally produced hybrids from a
turtle farm in Tunchang, Hainan Province; G)
Maure-
mys iversoni
from the type description. It is either from
Fujian or Guizhou Province; H) An intentionally pro-
duced hybrid from a turtle farm in Tunchang, Hainan
Province (MVZ 130475); I)
Cuora trifasciata
from Tai
Pin, central Hainan Province (MVZ 23932); J)
Cuora
trifasciata
from the pet trade (MVZ 230636). Photos by
JFP [a,e-f,h-j] and Pritchard and McCord (1991)[b-d,g].
2001 Asiatic Herpetological Research Vol. 9, p. 73
measurements (the interpectoral length [IPL] and the
interanal length [IAN]) that would have allowed the
type series to be included in the bivariate plot. Iver-
son and McCord (1994) perform a more detailed
study of variation within East Asian Mauremys, but do
not present the raw data and only include one speci-
men of Guizhou Mauremys iversoni (no voucher).
The relevant shell measurements of MVZ 230475
are as follows: IAN= 1.4 cm, IPL= 1.1 cm, CL= 11.4
cm, IAN/CL= .1228, IPL/CL=.096. MVZ 230475 is
a juvenile and smaller than three specimens excluded
from the adult category by Pritchard and McCord
(1991). Bearing this consideration, a comparison
shows that the morphology of MVZ 230475 is unlike
the type series of Mauremys iversoni, and apparently
unlike the other Mauremys. It is uncertain what the
variation between and among the Mauremys iversoni
series (from Guizhou and Fujian) is fully represented
by the polygon in Pritchard and McCord (1991).
Since the relevant scale ratios from their entire series,
including the subadult specimens, are not reported,
we are forced to rely on the close phenetic similarity
between the turtle farm hybrids and M. iversoni for
our conclusions. It is important to emphasize that if
all M. iversoni are turtle farm hybrids, then we should
expect them to have an extremely variable morphol-
ogy, especially if they are the result of separate hybri-
dogenic events. This pattern is borne out by the
previously reported M. iversoni-like turtles (Pritchard
and McCord, 1991; Qin, 1992; Iverson and McCord,
1994).
In terms of coloration, MVZ 230475 and the
hybrids photographed at the Tunchang turtle farm
closely resemble Mauremys iversoni. The head color-
ation of MVZ 230475 is lighter than that of the speci-
men figured by Pritchard and McCord (1991), but a
variation in head coloration in Mauremys iversoni was
noted by Fritz and Obst (1999). MVZ 230475 is
almost identical to the lighter individual figured in
that work. The variable head coloration in M. iversoni
can be linked to the variation in C. trifasciata. For,
while most C. trifasciata have dark postorbital mark-
ings, C. trifasciata with light head coloration are
known (Fig. 4), especially in turtle farms. Pritchard
and McCord (1991) state that M. iversoni can be dis-
tinguished from M. mutica by a horseshoe-shaped
coalescence of blotches from the pectorals to the anals
(with the open end anterior). Although they state that
this pattern is not found in Mauremys mutica, Zhou
and Zhou (1991, p. 38) illustrate a M. mutica (locality
not stated) with this this plastral pattern. Later, Iver-
son and McCord (1994) illustrate a M. mutica from
Taiwan (FMNH 127181) that also has a clear horse-
shoe-shaped coalescence of blotches. Even without
this character, M. iversoni can be distinguished from
M. mutica by its more rounded anterior lobe that lacks
a prominent gular projection. Furthermore, many M.
iversoni specimens, including some of the type series
of M. iversoni and the Hainan farm hybrids (Fig. 3b-f)
have transverse trending blotches on the pectorals, a
feature not known to occur in Mauremys, but common
in juveniles of C. trifasciata.
The variation among the figured specimens in the
type description is extreme (Fig. 3b-d,g). It is not
stated whether these specimens are from Fujian or
Guizhou. Comparisons of the plastral figures from
Pritchard and McCord (1991) with the specimens
from the Tunchang farm show that the latter speci-
mens lie within the range of variation of M. iversoni.
The most notable differences are that one (Fig. 3e) has
more irregularly shaped plastral blotches and MVZ
230475 (Fig. 3h) has only a narrow, light, central fig-
ure on the plastron. Perhaps the most important fea-
ture to be noted is that no two specimens look alike.
In the type description, Pritchard and McCord (1991)
describe the plastral pigmentation as “very variable in
intensity”, but it is unclear whether the figured speci-
mens represent the most typical patterns of Mauremys
iversoni or the entire range of variation.
Luckily, there are three characters of M. iversoni
that clearly set it apart from other East Asian Maure-
mys: 1) its olive or yellow head, 2) rounded end of
anterior lobe of the plastron and 3) red coloration on
the underside of the limbs. Until the description of
Mauremys iversoni, the red coloration of the limbs
was a diagnostic characteristic of C. trifasciata. The
light head coloration and rounded lobe are also remi-
Figure 4.
Cuora trifasciata
from a Chinese turtle farm
showing light head coloration. Photo by HS.
Vol. 9, p. 74 Asiatic Herpetological Research 2001
niscent of C. trifasciata. Furthermore, in Mauremys
iversoni the sulcus between the humeral and abdomi-
nal scutes lies closer to the hyo/hypoplastral suture
than it does in other Mauremys. An alignment of this
sulcus with the junction of these bones is a character
shared by C. trifasciata and other taxa with a kinetic
plastron. In other words, the morphology of Maure-
mys iversoni is intermediate between C. trifasciata
and M. mutica, and therefore consistent with a hybrid
origin. A detailed comparison of the mitochondrial
DNA and allozymes of this specimen and other pet
trade “species” is currently under way (Parham et al.,
2000; in prep.).
Discussion
During our joint visit to the Tunchang turtle farm, the
workers stated that production of Mauremys iversoni-
like turtles was the result of infrequent, accidental
hybridization events. Since that time, the owner of
the farm has confided that the intentional production
of C. trifasciata X M. mutica hybrids is a common
practice undertaken by several turtle farmers.
Because practitioners of Chinese traditional medicine
claim that C. trifasciata has many medicinal proper-
ties, and recently it has also been suggested that it has
the ability to cure cancer, it is highly valued. As a
result, it is often called the “golden coin” turtle. The
price of turtles is determined by their weight. In the
year 2000, 1 kg of M. mutica sold for approximately
100-120 yuan (~15 USD) whereas 1 kg of C. trifasci-
ata sold for 6,000-8,000 yuan (~1000 USD). Accord-
ing to the turtle farmer, it is possible to sell the
hybrids of C. trifasciata and M. mutica as pure C. tri-
fasciata since, to the untrained eye, these species
closely resemble one another, especially in the yellow
coloration of the head. The confusion of these two
forms should not be surprising since Timmins and
Khounboline (1999) report that even people familiar
with C. trifasciata have mistakenly identified juvenile
M. mutica as this species. Therefore, it is possible to
produce and sell large numbers of counterfeit “golden
coins” to unsuspecting buyers without having to
obtain large numbers of adult Cuora trifasciata.
The high degree of phenetic similarity between
the C. trifasciata X M. mutica hybrids from Hainan
and the M. iversoni-like turtles reported from Fujian,
Guizhou and Guangxi strongly suggests that all of
these animals may be the product of accidental or
intentional hybridization in turtle farms. This hypoth-
esis explains the unusual morphology, its sudden
appearance in the pet trade, absence in historical col-
lections, and the confusion surrounding the distribu-
tion of this taxon. The timing of the discovery of
these turtles shortly follows the increased demand for
Cuora trifasciata as a reputed cure for cancer (van
Dijk et al., 2000). This increased demand may have
initiated the establishment of numerous turtle breed-
ing facilities that led to the production of Mauremys
iversoni-like turtles.
We stress that the practice of housing and breeding
several species of chelonians in a single enclosure or
pond is probably not restricted to the Tunchang farm
alone. If the establishment of other facilities mirrors
the one on Hainan, the sudden appearance of new and
unusual turtles in the pet trade would be expected.
The ability of turtles to hybridize is well documented
(Fritz and Baur, 1994; Fritz, 1995). Certain species,
such as Mauremys pritchardi McCord 1997, have
already been implicated as possible hybrids (Artner et
al., 1998). Others, such as Sacalia pseudocellata
Iverson and McCord 1992, Ocadia glyphistoma
McCord and Iverson 1994, and Ocadia phillipeni
McCord and Iverson 1992 are known from a paltry
number of specimens which might be indicative of an
accidental production in a turtle farm (van Dijk, 2000;
Lau and Shi, 2000). It is probably not a coincidence
that many of the newly described species (O. phil-
lipeni, S. pseudocellata, and M. iversoni) can be dis-
tinguished from their congeners by characters found
in the commonly reared and highly valued C. trifasci-
ata. Studies of the DNA of the holotypes of these
species, compared with multiple, field-collected,
vouchered specimens of established species from
known localities, could easily determine the validity
of these taxa.
Conclusions
It is uncertain whether all of the reported collection
data from the pet trade, such as the distributional data
for Mauremys iversoni are actual or fabricated. The
rest of the available evidence strongly suggests, but
does not prove, that all M. iversoni-like turtles could
have a turtle farm origin. Parham and Li (1999)
openly question the Yunnan locality of Cuora pani
that was provided by the same pet dealer credited with
collecting the original Mauremys iversoni series. The
high prices that unusual turtles with locality data can
fetch from turtle fanciers could serve as incentive to
fabricate collection data. Furthermore, there is also
incentive to hide the true locality as a trade secret,
especially if the locality is a Chinese turtle farm. Of
course, given the current scarcity of turtles in Asia it is
difficult to prove that a locality is in error or whether
the turtles have been extirpated. Verified distribution
data for rare chelonians (e.g., Iverson, 1992) are criti-
cal to understanding their current and historical status.
2001 Asiatic Herpetological Research Vol. 9, p. 75
False localities unnecessarily complicate our meager
understanding of turtle distributions. In light of the
confusion surrounding pet trade data, we recommend
that workers should treat them with utmost caution
until they are supported by evidence that is more reli-
able.
Given the seemingly uncontrollable Asian Turtle
Crisis, determining which species are valid evolution-
ary lineages and which are turtle farm hybrids is
important. Otherwise, crucial resources could be
wasted on invalid taxa. For example, the Red data
Book of Endangered Animals (Wang, 1998) suggests
that Fujian and Guizhou provinces protect M. iversoni
and that surveys and ecological studies should be per-
formed in order to determine the proper conservation
strategies. We concur with van Dijk’s (2000) asser-
tion that researchers should make the investigations
on the validity of the pet trade species a priority so
that the limited resources for conservation can be
directed towards established taxa that are undergoing
unimagined, precipitous declines.
Acknowledgments
The authors would like to thank John Iverson for
prompting a comparison between the turtle farm
hybrids and the type description of Mauremys iver-
soni. We would also like to thank Dr. Jaeger, the edi-
tor of Herpetologica, for granting us permission to
reproduce part of Figure 1 from Pritchard and
McCord (1991). Ted Papenfuss and Jim Buskirk pro-
vided helpful comments. JFP is also grateful to Carl
Gillies, Kevin Padian, and Tonya Van Leuvan-Smith.
This project was funded by the National Science
Foundation (JFP), the University of California
Museum of Paleontology (JFP), The National Natural
Science Foundation of China (HS), The Provincial
Natural Science Foundation of Hainan (HS), and the
Hainan Provincial Ecological Key Discipline Fund
(HS).
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... Scientists have never observed C. picturata in the wild, and its origin remains unknown. Some poorly known Asian turtles that were recently described as new species on the basis of trade animals have since been shown to be only recent hybrids of better known species, including inter-generic hybrids (Parham et al., 2001; Dalton, 2003; Stuart and Parham, 2007). Some of these hybrids have a wild origin (Shi et al., 2005), while others originated from farming operations (where parental species are co-housed) that supply the Chinese turtle trade (Parham and Shi, 2001; Parham et al., 2001; Shi et al., 2008). ...
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In recent years, the number of sequences of diverse species submitted to GenBank has grown explosively and not infrequently the data contain errors. This problem is extensively recognized but not for invalid or incorrectly identified species, sample mixed-up, and contamination. DNA barcoding is a powerful tool for identifying and confirming species and one very important application involves forensics. In this study, we use DNA barcoding to detect erroneous sequences in GenBank by evaluating deep intraspecific and shallow interspecific divergences to discover possible taxonomic problems and other sources of error. We use the mitochondrial DNA gene encoding cytochrome b (Cytb) from turtles to test the utility of barcoding for pinpointing potential errors. This gene is widely used in phylogenetic studies of the speciose group. Intraspecific variation is usually less than 2.0% and in most cases it is less than 1.0%. In comparison, most species differ by more than 10.0% in our dataset. Overlapping intra- and interspecific percentages of variation mainly involve problematic identifications of species and outdated taxonomies. Further, we detect identical problems in Cytb from Insectivora and Chiroptera. Upon applying this strategy to 47,524 mammalian CoxI sequences, we resolve a suite of potentially problematic sequences. Our study reveals that erroneous sequences are not rare in GenBank and that the DNA barcoding can serve to confirm sequencing accuracy and discover problems such as misidentified species, inaccurate taxonomies, contamination, and potential errors in sequencing.
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New Late Oligocene (Chattian) remains of the terrapins Palaeoemys hessiaca Schleich, 1994 and Palaeomauremys tuberculata (Portis, 1882), the soft-shelled turtles Allaeochelys parayrei Noulet, 1867 and Trionyx cf. triunguis Forskål, 1775, and the snapping turtle Chelydrasia decheni (H. V. Meyer, 1852) from lacus-trine sediments of the Oberleichtersbach doline (Lower Franconia, Bavaria, Germany) are reported. The morphological features of these five species, their taxonomic position and their palaeobiological implications are discussed. The new Palaeomauremys material suggests that P. mlynarskii (Hervet & Lapparent de Broin, 2000) is a junior synonym of P. tuberculata (Portis, 1882).
A new species of Ocadia (Testudines:Batagurinae) from southwestern China
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McCord, W. P. and J. B. Iverson. 1994. A new species of Ocadia (Testudines:Batagurinae) from southwestern China. Proceedings of the Biological Society of Washington 107:52-59.
A new species of genus Clemmys: C. guangxiensis. Pp. 60-62
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Animal Science Research. A Volume issued to celebrate the 90 th birthday of Mangven L
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Zhao (eds.), Animal Science Research. A Volume issued to celebrate the 90 th birthday of Mangven L.-Y.