Please cite this article in press as: Attwood, S.W., et al., Update on the distribution and phylogenetics of Biomphalaria (Gastropoda:
Planorbidae) populations in Guangdong Province, China. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.04.032
ARTICLE IN PRESS
G Model
ACTROP-3369; No. of Pages 13
Acta Tropica xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Acta Tropica
jo ur nal home p age: www.elsevier.com/locate/actatropica
Update on the distribution and phylogenetics of Biomphalaria
(Gastropoda: Planorbidae) populations in Guangdong Province, China
Stephen W. Attwood
a,b,∗
, Guan-Nan Huo
a
, Jian-Wen Qiu
c
a
State Key Laboratory of Biotherapy, West China Hospital, West China Medical School, Sichuan University, Chengdu, People’s Republic of China
b
Department of Life Sciences, The Natural History Museum, London, United Kingdom
c
Department of Biology, Hong Kong Baptist University, Hong Kong, China
a r t i c l e i n f o
Article history:
Available online xxx
Keywords:
Biomphalaria
China
Gastropoda
Invasive species
Phylogenetic
Schistosomiasis
a b s t r a c t
In 1973 planorbid snails then identified as Biomphalaria straminea were discovered in Hong Kong, China.
It was assumed that these snails had been introduced to Hong Kong via the import of tropical fish by air
from South America. In 2012 Biomphalaria were found for the first time in Guangdong Province, China.
In view of the renewed interest in these invasive snails, a morphological and DNA-sequence based phy-
logenetic study was undertaken for seven populations of Biomphalaria snails collected in Guangdong.
Morphologically and phylogenetically, five of the populations clustered more closely with Biomphalaria
kuhniana than with B. straminea. Levels of genetic diversity among the populations were about half those
of autochthonous populations in Brazil, the phylogenetic relationships did not correlate with a radia-
tion from any one international port in China, and different lineages appeared associated with different
ports. Consequently in explaining the current distribution of the snails, multiple colonization events,
each establishing a new local snail population near to maritime international container ports, were con-
sidered more likely than the spread of snails from Hong Kong to China. The displacement of B. straminea
by B. kuhniana in Guangdong is considered as an explanation for the habitat changes observed among
the snails between Hong Kong in the 1980s and the present. The conclusions of the study are that any
risk of Schistosoma mansoni transmission in China is more likely to come from parasite importation in
the intramolluscan stage, than from transmission by migrant workers from South America or Africa. In
addition, although likely to be rare, sporadic outbreaks of imported schistosomiasis (caused by invading
infected snails) could be a threat to public health in the vicinity of International container ports (not only
in Guangdong Province). Further work is called for to investigate further the presence of B. kuhniana and
its potential interactions with B. straminea (the former is thought to be incompatible with S. mansoni), and
the responses of Chinese Biomphalaria to potential competitors such as Thiaridae. The current expansion
of container ports in Brazil and Venezuela, and the increase in trade with China, is likely to accentuate any
current risk of imported schistosomiasis, and surveillance around ports in China, together with further
research, are necessary.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Schistosomiasis is a debilitating parasitic disease caused by
infection with blood-flukes of the genus Schistosoma (Trematoda:
Digenea). Schistosoma mansoni, which is transmitted by several
species of freshwater snails of the genus Biomphalaria (Preston,
1910), infects over 80 million people in the tropical and sub-tropical
∗
Corresponding author at: State Key Laboratory of Biotherapy, #1 Ke Yuan 4 Lu,
Hi-Tech Development Zone, Chengdu 610041, Sichuan, People’s Republic of China.
Tel.: +86 13551859727.
E-mail addresses: swahuaxi@yahoo.com, s.attwood@nhm.ac.uk (S.W. Attwood).
regions of Africa, the Middle East (Egypt, Iraq), and South America
(Crompton, 1999). Biomphalaria straminea (Dunker, 1848) is one of
three species transmitting S. mansoni in Brazil, where 6–10 million
people are infected by S. mansoni (see Coura and Amaral, 2004).
Among its congeners, B. straminea is known for its long-distance
dispersal and colonization capabilities, which are attributed to
a greater ability to endure desiccation and to greater fecundity
(Barboza et al., 2012). The prehistoric distribution of B. straminea
is considered to have been neotropical South America (Pointier
et al., 2005), mainly Brazil (focused on the coastal Northeast), with
later peripheral range expansion to include the Caribbean, namely
Colombia in 1966 (Barbosa, 1968) and Costa Rica in 1976 (Paraense
et al., 1981), as well as several islands of the Lesser Antilles,
http://dx.doi.org/10.1016/j.actatropica.2014.04.032
0001-706X/© 2014 Elsevier B.V. All rights reserved.