Abstract
Though some hypotheses have obtained theoretical and empirical supports,
it remains largely unknown in the aspect that how deception increases
orchid fitness. This study used food-deceptivePapilionanthe
teres as experimental material to explore the ecological significance
of orchid deceptive pollination. Deception together with obvious
pollinarium bending increases P. teres fitness by means of
decreasing geitonogamy under the natural conditions. The proportions of
full seeds, single fruit weight and seed weight per fruit after
self-pollination and nectar addition were significantly lower than that
after cross-pollination and natural conditions
(all
p < 0.05). Seed viability (seed growth and development rate) after
cross-pollination and natural condition were significantly higher than
that after self-pollination and nectar addition (all p < 0.05).
However, there was no significant difference in all the above parameter
values of fruits and seeds between cross-pollination and natural
conditions (all p > 0.05). These results confirmed that P. tereshas high level of genetic load, and self-fertilization or geitonogamy
will cause serious inbreeding depression. These conclusions support the
outcrossing hypothesis that ecological significance of P. teresdeception is to promote outcrossing and improve the ability of the
offspring to adapt to the environment.
Keywords: Papilionanthe teres, deception, geitonogamy,
inbreeding depression, outcrossing
Introduction
Orchidaceae is a large family of plants, with about 763 genera and 28000
species (Crain & Tremblay, 2014; Christenhusz & Byng, 2016; Zhang et
al., 2018). Of the 7500 angiosperm species that are pollinated through
deception, approximately 6500 are orchids (Renner, 2006), suggesting
that deception mainly occurs in orchids. Food deception is most
prevalent in the orchid family, and several thousand species are found
in 38 genera (Dafni, 1984; Ackerman, 1986; Nilsson 1992; Jersáková et
al., 2006). The second is sexual deception, and about 400 orchid species
are found in 18 genera (Dafni & Bernhardt, 1990; Cozzolino & Widmer,
2006; Jersáková et al., 2006).
Visit frequency and natural fruit set of no rewarding species are lower
than that of rewarding ones due to pollinator learning behavior. So the
fitness of deceptive plants remains a focus for debate among biologists.
Besides four orchid-specific hypotheses (Jersáková et al., 2006;
Cozzolino & Widmer, 2006; Scopece et al., 2010), there are two general
hypotheses, resource-limitation hypothesis and outcrossing hypothesis,
to explain how deception increases plant fitness (Jersáková et al.,
2006).
Plant sexual reproduction, such as flower production and fruit set, is
mainly limited by resources (Calvo, 1992; Mattila & Kuitunen, 2000).
The aim of deception is to invest more resources to maintain plant
development and ensure a certain seed set (resource-limitation
hypothesis) (Ackerman & Montalvo, 1990; Barrett & Harder, 1995).
However, the sexual reproduction of deceptive orchids is often severely
limited by pollens over a lifetime (Calvo, 1993; Tremblay et al., 2005).
Hence, it is difficult to understand why resources in these orchids are
not allocated to a component of pollinator attraction such as nectar.
One possibility is that the attraction of investing more resources in
floral display is more efficient than that in rewarding substances.
Deception results in lower visitation rates, fewer flowers probed per
visit, lower level of
geitonogamy,
more pollen output and outcrossed progeny
(outcrossing
hypothesis) (Jersáková et al., 2006). Based on the above conclusions, it
is widely believed that loss of rewarding substances contributes to
decreasing geitonogamy and promoting outcrossing (Dressler, 1981;
Nilsson, 1992; Johnson & Nilsson, 1999). Outcrossing hypothesis
emphasizes the importance of pollen resource and genetic quality in
reproductive success, and postulates that self-fertilization or
geitonogamy will cause inbreeding depression (Lammi & Kuitunen, 1995).
Therefore, the first problem of outcrossing hypothesis is to test
whether self and cross-pollination result in different female
reproductive success (Lammi & Kuitunen, 1995). Though previous case
studies confirm that deception promotes outcrossing, whether actual
outcrossing rates are generally higher in deceptive orchids remains
unknown (Jersáková et al., 2006).
Pollinarium bending occurres in many orchid species, it will result in a
time delay before the pollinium assumes a position from which it can
strike a stigma (Darwin, 1877; Johnson & Edwards, 2000). The phenomenon
will decrease geitonogamy when pollinators visit fewer flowers and stay
for shorter time per visit. Some case studies confirm that
pollinarium
bending is an anti-selfing mechanism (Darwin, 1877; Johnson et al.,
2004). These results suggest that pollinarium bending may increase
orchid fitness under certain conditions. But it still requires further
study that how pollinarium bending increases fitness in orchid deceptive
pollination systems.
Papilionanthe teres is only found in a very limited region of
southeast Xishuangbanna in China. It has adapted to high temperature,
humidity and sunlight conditions. Its flowers exhibit color polymorphism
of the corolla, such as white lateral sepal, purplish red petal, dorsal
sepal and labellum (Zhou & Gao, 2016). Its single inflorescence may
bear 1-16 flowers. Floral longevity may reach more than 30 days under
the conditions of no pollinarium removal, pollinia deposition and floral
damage. P. teres is a typical food-deceptive species, with no
reward in its flowers. The techniques of symbiotic and asymbiotic seed
reproduction in P. teres were established in previous studies
(Chen et al., 2007; Mazumder et al., 2010; Zhou & Gao, 2016; Vishal,
2020). This study utilized these techniques and used P. teres as
material to understand the ecological significance of orchid deceptive
pollination. The following questions were addressed: (1) What are the
mechanisms of promoting outcrossing in P. teres ? (2) What are the
effects of self-pollination and nectar addition on fruit and seed
development and seed viability of P. teres ? (3) Does self and
cross pollination result in different female reproductive success? (4)
Does P. teres have a high outcrossing rate (high levels of
genetic load) under natural conditions?
Material and Methods