production of secondary metabolites and biological factors to gain an understanding of the evolutionary ecology of pollinator trapping in carnivorous plants.
Keywords
Carnivorous plants · Pollinator · Pollinator–prey conflict · Anthocyanin ·
Predator–prey interactions
1
Introduction
Carnivorous plants are an intriguing group of angiosperms that reverse the usual
trophic interaction between plants and animals, with the plant acting as the predator
and the animal becoming the prey [1], and consequently have attracted the attention
of scientists since Darwin’s time [2]. Carnivorous plants mainly use their trap leaves
to capture and digest small invertebrates and absorb nutrients such as N and P from
them [3], which increase plant growth [4] and seed and fruit set [5–7]. This trait
allows them to live in nutrient-poor habitats (e.g., wetlands, alpine areas, and tropical
forests) [8] and has evolved at least ten times independently, with 800 species in 19
genera, 12 families, and 5 orders having been identified to date [9].
In addition to the predator–prey interactions between carnivorous plants and
insects, many carnivorous plants have entomophilous flowers and rely on insects
for pollination to facilitate sexual reproduction and outcrossing. In such a situation,
carnivorous plants face conflicting pressures, as there is the possibility of capturing
mutualistic pollinators in their trap leaves and consuming them. Thus, carnivorous
plants face a trade-off between the pollination service and nutrient uptake. This issue
was raised as the “prey/pollinator paradox” by Juniper et al. [10] and discussed as the
“pollinator–prey conflict (PPC)” by Zamora [11], and comprehensive reviews of the
PPC have since been written by Jürgens et al. [12] and Cross et al. [13].
When carnivorous plants rely on insects for their pollination and pollinator/pollen
limitation exists, pollinator trapping will reduce the fitness of the plants, leading to a
PPC occurring. By contrast, those plants that do not rely on insects for their
pollination and are not pollinator limited will not experience a PPC. Furthermore,
when nutrient limitation rather than pollinator limitation is the fitness bottleneck,
trapping pollinators will increase the fitness of carnivorous plants [12]. Therefore,
the consequences of trapping pollinators will vary depending on the breeding system
and the factors that limit the fitness of carnivorous plants, which has led to the
evolution of diverse characteristics of the trap leaves and flowers.
Two major characteristics of carnivorous plants will affect the efficiency (or risk)
of trapping pollinators. The first is the degree of spatial or temporal separation
between the flowers and trap leaves. If trapping pollinators reduces the fitness of
carnivorous plants, it will be adaptive for the flowers and trap leaves to be separated
spatially or temporally to reduce the risk that pollinators are captured by chance, for
example, by producing a long flower scape to spatially separate the flowers from the
rosette-shaped trap leaves (e.g., Drosera spp. and Pinguicula spp.) [8] or by producing the flowers and active trap leaves in different seasons (e.g., Sarracenia spp.)
776
K. Tagawa
Keywords
Carnivorous plants · Pollinator · Pollinator–prey conflict · Anthocyanin ·
Predator–prey interactions
1
Introduction
Carnivorous plants are an intriguing group of angiosperms that reverse the usual
trophic interaction between plants and animals, with the plant acting as the predator
and the animal becoming the prey [1], and consequently have attracted the attention
of scientists since Darwin’s time [2]. Carnivorous plants mainly use their trap leaves
to capture and digest small invertebrates and absorb nutrients such as N and P from
them [3], which increase plant growth [4] and seed and fruit set [5–7]. This trait
allows them to live in nutrient-poor habitats (e.g., wetlands, alpine areas, and tropical
forests) [8] and has evolved at least ten times independently, with 800 species in 19
genera, 12 families, and 5 orders having been identified to date [9].
In addition to the predator–prey interactions between carnivorous plants and
insects, many carnivorous plants have entomophilous flowers and rely on insects
for pollination to facilitate sexual reproduction and outcrossing. In such a situation,
carnivorous plants face conflicting pressures, as there is the possibility of capturing
mutualistic pollinators in their trap leaves and consuming them. Thus, carnivorous
plants face a trade-off between the pollination service and nutrient uptake. This issue
was raised as the “prey/pollinator paradox” by Juniper et al. [10] and discussed as the
“pollinator–prey conflict (PPC)” by Zamora [11], and comprehensive reviews of the
PPC have since been written by Jürgens et al. [12] and Cross et al. [13].
When carnivorous plants rely on insects for their pollination and pollinator/pollen
limitation exists, pollinator trapping will reduce the fitness of the plants, leading to a
PPC occurring. By contrast, those plants that do not rely on insects for their
pollination and are not pollinator limited will not experience a PPC. Furthermore,
when nutrient limitation rather than pollinator limitation is the fitness bottleneck,
trapping pollinators will increase the fitness of carnivorous plants [12]. Therefore,
the consequences of trapping pollinators will vary depending on the breeding system
and the factors that limit the fitness of carnivorous plants, which has led to the
evolution of diverse characteristics of the trap leaves and flowers.
Two major characteristics of carnivorous plants will affect the efficiency (or risk)
of trapping pollinators. The first is the degree of spatial or temporal separation
between the flowers and trap leaves. If trapping pollinators reduces the fitness of
carnivorous plants, it will be adaptive for the flowers and trap leaves to be separated
spatially or temporally to reduce the risk that pollinators are captured by chance, for
example, by producing a long flower scape to spatially separate the flowers from the
rosette-shaped trap leaves (e.g., Drosera spp. and Pinguicula spp.) [8] or by producing the flowers and active trap leaves in different seasons (e.g., Sarracenia spp.)
776
K. Tagawa