全 文 ：小型哺乳类食果动物可能对蛇菰科葛菌种子散布的初次报道
CONRAN John G1, 李摇 捷2*
(1 澳大利亚阿得莱德大学, 地球与环境科学学院, 澳大利亚 南澳州 阿得莱德摇 5005; 2 中国科学院
西双版纳热带植物园植物系统发育与保护生物学实验室, 云南 昆明摇 650223)
摘要: 初次报道了哺乳类食果动物可能对蛇菰科葛菌 (Balanophora harlandii) 的种子散布, 葛菌具有酷似
蘑菇且醒目显著的肉质佛焰状果序, 食菌的啮齿类动物很可能由于对其进行取食而起到种子散布的作用,
本文对此现象进行了初步探讨。
关键词: 寄生植物; 蛇菰科; 可能的食菌类; 啮齿动物; 种子散布
中图分类号: Q 948. 12摇 摇 摇 摇 摇 文献标识码: A摇 摇 摇 摇 摇 摇 摇 文章编号: 2095-0845(2012)05-466-05
A Preliminary Report of Small Mammal Frugivory on
Balanophora harlandii (Balanophoraceae)
CONRAN John G1, LI Jie2*
(1 ACEBB, School of Earth & Environmental Sciences, The University of Adelaide, Benham Bldg DX 650 312, North Terrace,
SA 5005 Australia; 2 Lab of Plant Phylogenetics & Conservation, Xishuangbanna Tropical Botanical Garden,
Chinese Academy of Sciences, Kunming 650223, China)
Abstract: Mammal frugivory and apparent seed dispersal of Balanophora harlandii (Balanophoraceae) in Xishuang鄄
banna, Yunnan Province, China is reported for the first time. The possibility of the conspicuous, fleshy, spadici鄄
form infructescences mimicking mushrooms for dispersal by mycophagous rodents is discussed.
Key words: Parasitic plants; Balanophoraceae; Possible Mycophagy; Rodents; Seed dispersal
摇 Balanophora J. R. Forst. & G. Forst. (蛇菰
属) is a genus of leafless holoparasitic plants in the
Santalales (APG III, 2009), or related Balanopho鄄
rales (Nickrent et al., 2010). There are ~ 19 spe鄄
cies, mainly in the Old World tropics and the Pacific
Islands, with 12 species in China, one of which is
endemic (Huang and Murata, 2003). The different
species are either monoecious or dioecious and are
subterranean root parasites on a range of hosts. They
generally only emerge above ground to flower and
fruit ( Fig. 1 ), when they produce conspicuous,
brightly鄄coloured, often mushroom鄄like spadiciform
inflorescences (Huang and Murata, 2003; XTBG,
2010).
Balanophora harlandii J. D. Hook. (葛菌) is
a dioecious species that grows in shady, moist moun鄄
tain forests between ~ 600-2 100 m in southern Chi鄄
na, India and Thailand (Xing and Li, 1992; Huang
and Murata, 2003), where the host plants are usu鄄
ally Cannabis (大麻属: Cannabaceae) and Puerar鄄
ia (葛属: Fabaceae) species (Huang and Murata,
2003). Although used medicinally, B. harlandii is
rare and considered threatened, mainly due to habi鄄
tat loss or disturbance (XTBG, 2010). In China,
flowering occurs from September to November, with
fruits taking several months to mature. The infruct鄄
escence is a mass of tiny, more or less syncarpous
fleshy依achenes, creating a vividly red, fleshy mush鄄
植 物 分 类 与 资 源 学 报摇 2012, 34 (5): 466 ~ 470
Plant Diversity and Resources摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 DOI: 10. 3724 / SP. J. 1143. 2012. 12039
* Author for correspondence; E鄄mail: jieli@ xtbg. ac. cn
Received date: 2012-03-22, Accepted date: 2012-05-20
room鄄like structure borne above the leaf litter on a
short scape emerging from a cluster of leafy red
bracts (Fig. 1B).
During floristic surveys for a range of plant
groups in reserves around Xishuangbanna in southern
Yunnan Province fruiting plants of B. harlandii were
encountered where mature infructescences had been
stripped of their achenes by small mammals, most
probably rodents. Balanophoraceae fruit dispersal
has been little studied, but seed dispersal by rodents
has been suggested for at least one South American
genus (Borchsenius and Olesen, 1990). According鄄
ly, the phenomenon is reported here for Balanophora
and the possible role of fungal mimicry by the infruc鄄
tescences for mycophagy by rodents is discussed.
Materials and methods
As part of searches for various plant taxa for on鄄
going research projects between the CAS and Univer鄄
sity of Adelaide, treks through the native forests in
the Xishuangbanna Tropical Botanic Gardens (XT鄄
BG), Menglun (21毅41忆 N, 101毅25忆 E, 570 m);
Rainforest bordering a creek running into the Nanla鄄
he R, Bubeng near Mengla (21毅36忆 N 101毅35忆 E)
were undertaken by both authors in Jan. 2008. Dur鄄
ing these searches, five clumps of B. harlandii were
encountered, two at XTBG and three at Bubeng. All
were growing at moderate altitude (7 -800 m) and
mostly in drier, bamboo鄄dominated rainforest forest
margins.
At each Balanophora clump, the number of
mature versus immature and damaged versus entire
infructescences was recorded, as well as any dam鄄
age. Due to the small numbers involved, both within
clumps as well as due to the rarity of the colonies,
the data were not amenable to detailed statistical a鄄
nalysis and this paper is intended as a preliminary
report of the phenomenon requiring further investiga鄄
tion, rather than a conclusive study.
Results
Infructescence number varied from 3-8 (4. 6依
2. 1 mean and SD), with 1-3 mature fruiting stalks
present on each clump (Fig. 1A). Although most of
the colonies appeared to be untouched, two ( one
each at XTBG and Bubeng) showed evidence of
mammalian (probably rodent) frugivory, with sever鄄
al mature infructescences having been obviously
chewed, more or less completely stripping them of
the fleshy syncarpous achenes (Fig. 1C), as well as
leaving a mass of seed鄄filled material on the ground
surrounding the colony (Fig. 1D).
Discussion
Balanophoraceae dispersal
The presence of mature infructescences with
conspicuous rodent damage is significant given the
rarity of the species. Either this is an example of
fruit predation, or it may represent part of the dis鄄
persal mechanism of the species. The fact that only
mature fruits were targeted suggests possibly the lat鄄
ter, but it may also be a reflection of the food value
and / or palatability of the infructescences at different
stages of maturity.
Fruit dispersal in the family is little studied.
Rain wash dispersal in Costa Rican Balanophoraceae
was reported by G佼mez (1983), but Borchsenius
and Olesen (1990) reported that 100% of L. mirab鄄
ile fruits placed in water sank within 24 h. Neverthe鄄
less, they did suggest that the achenes may be trans鄄
ported short distances by water, as well as dispersed
by rodents.
The fruits of Dactylanthus taylorii in New Zeal鄄
and form small achenes with a tough, almost woody
endocarp. The species is thought to be water or
gravity dispersed ( Ecroyd, 1996) and feeding on
infructescences by introduced Kiore ( Rattus exu鄄
lans) is seen as detrimental to the survival of this
endangered plant species (Ferreira, 2005).
Rodents, dispersal and predation
Rodents are common frugivores, though most ro鄄
dent dispersal is thought to be a result of transporting
and / or caching seeds and fruits for later consumption
(Dennis and Westcott, 2006; Westcott et al., 2009)
7645 期摇 摇 摇 摇 CONRAN and LI: A Preliminary Report of Small Mammal Frugivory on Balanophora harlandii … 摇 摇 摇 摇
Fig. 1摇 Balanophora harlandii infructescences near Bubeng, Xishuangbanna, Yunnan
A. Colony showing fruits in different stages of maturity; B. Spadiciform, mushroom鄄like infructescence showing the more or
less syncarpous, fleshy achenes and prominent inflorescence bracts below the scape, arrow indicates seed鄄bearing frass from ro鄄
dent feeding; C. Mature fruiting body showing extensive damage and chew marks from small mammals, probably rodents; D.
Seed鄄filled frass left behind after infructescence feeding by the small mammals. Scale bars A=50 mm, B-D=20 mm
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and an example of dispersal through ineffective dyszoo鄄
chory, with effective endozoochory in small mammals
and especially rodents considered to be less common
(van der Pijl, 1982; Traveset et al., 2007).
Nogales et al. (2005) found that Rubia frutico鄄
sa (Rubiaceae) seeds ingested by squirrels (Atlan鄄
toxerus getulus) or rabbits (Oryctolagus cuniculus)
showed significantly reduced viability and germina鄄
tion, possibly because of long gut retention times.
This was also suggested for some mammal鄄dispersed
endozoochorous seeds in the Mediterranean (Trave鄄
set et al., 2001), but frugivore taxon versus germi鄄
nation results can vary widely ( Traveset and Will鄄
son, 1997; Nogales et al., 2005; Rodr侏guez鄄P佴rez
et al., 2005), and even non鄄flying mammalian dis鄄
persers still showed reasonable, albeit lower germi鄄
nation levels. Nevertheless, in general although bat
and bird dispersal encourages germination, non鄄fly鄄
ing mammals have only minor positive effects (Tra鄄
veset and Verd俨, 2002).
The small seeds of Balanophora may be able to
avoid being chewed themselves when the fruits are
being ingested and it is possible that they are being
dispersed through the faeces of the rodents. The re鄄
semblance of the infructescences to fungi could well
be an example of mimicry to attract mycophagous
small mammals, which are known to disperse fungal
spores in their faeces (Claridge and May, 1994),
as well as seeds of the fungus鄄like subterranean or鄄
chid Rhizanthella gardneri ( Orchidaceae ) from
Western Australia (Dixon, 2003). Similarly the ti鄄
ny seeds of the root holoparasite Cytinus hypocistis
(Cytinaceae) has been shown recently to be able to
survive ingestion of the seeds by tenebrionid beetles
( de Vega et al., 2011). Some rainforest rodents are
also known to disperse fungal fruiting bodies before
consuming them ( Dennis and Westcott, 2006;
Westcott et al., 2009).
The fact that frass from the chewed infructes鄄
cences as left lying on the ground (Fig. 1D) also sug鄄
gests that the damage may actually help fragment the
syncarpia, which otherwise tend to become rather dry
and crustaceous at senescence (Huang and Murata,
2003), which would hinder seed dispersal. This
would then allow more effective dispersal of the seeds
by gravity or water away from the parent colony.
The presence of rodent damaged infrucescences
of Balanophora harlandii raises interesting questions
needing further study and more direct observation. Is
this an example of predation, making this rare spe鄄
cies even rarer, or is it a case of mutualism, the ro鄄
dents feeding on the fruits as if they were mushrooms
and dispersing the small seeds? We hope that by re鄄
porting this phenomenon, further observations can
be made to determine the answers to these ques鄄
tions, allowing for the limitations of studying rare
and relatively hard to find taxa.
Acknowledgements: The Chinese Academy of Sciences is
thanked for support for this work which was undertaken as
part of a collaborative research project with the CAS Kunming
and Xishuangbanna Tropical Botanic Gardens on evolution in
the Chinese Flora. The School of Earth & Environmental Sci鄄
ences and The University of Adelaide are thanked for the pro鄄
vision of Special Study Leave to undertake this work.
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