Lobelia (also known as blue-flowered bellflower), Lobelia sessilifolia, and Lobelia sessilifolia are all members of the Campanulaceae family, and are characterized by their blue flowers and bilaterally symmetrical blooms. They are commonly cultivated in gardens, especially in horticulture. However, these species are often confused in image searches. In reality, they are completely different species with distinct flower shapes, growth patterns, and leaf characteristics. This article will explain the classification and morphology of the Lobelia genus.

What are Lobelia (Lobelia chinensis), Lobelia chinensis, and Lobelia sessilifolia?

Lobelia erinus, also known as blue-flowered lobelia, is native to central and southern Africa and is cultivated as an ornamental plant worldwide, including in Japan (RBG Kew, 2024).

Lobelia chinensis, also known as Mizokakushi (furrow cover), is a perennial herb that grows in damp places such as rice paddy ditches and ditches. It is distributed in Hokkaido, Honshu, Shikoku, Kyushu, and the Ryukyu Islands in Japan; as well as in Korea, China (south of central China), Taiwan, India, and Malaysia (Kanagawa Prefecture Flora Survey Association, 2018). Its Japanese name comes from the fact that it grows in a way that hides ditches.

Lobelia sessilifolia, also known as marsh bellflower, is a perennial herb that grows in wetlands in hilly to mountainous areas and is distributed in Hokkaido, Honshu, Shikoku, and Kyushu in Japan; as well as in Korea, China, Sakhalin, the Kuril Islands, eastern Siberia, and Kamchatka.

All of these species belong to the genus Lobelia in the family Campanulaceae. In addition to having blue flowers typical of the Campanulaceae family, they share the common characteristics of the genus Lobelia, such as bilaterally symmetrical flowers and fused anthers that form a tube.

In horticulture, Lobelia sessilifolia and Lobelia sessilifolia are commonly cultivated. Lobelia sessilifolia is hybridized with Lobelia cardinalis and sold under names such as "perennial lobelia."

However, a Google image search for "perennial lobelia" clearly shows that Lobelia japonica is mixed in, suggesting a confusion between the two species.

Also, while "Lobelia" is actually a general term for species belonging to the genus Lobelia, the name "Lobelia" is sometimes used to refer to *Lobelia japonica*, which may lead to confusion.

What are the differences between Lobelia sessilifolia, Lobelia sessilifolia, and Lobelia sessilifolia?

The clear difference between these three species lies in their flowers. All members of the genus Lobelia belong to the family Campanulaceae, so they have "sympetalous flowers," and what appear to be petals are actually "corolla lobes."

In Lobelia sessilifolia, the corolla is pale reddish-purple and the upper pair of the five lobes points diagonally downwards, whereas in Lobelia sessilifolia and Lobelia sessilifolia, although there are exceptions, the corolla is usually bluish-purple and the upper pair of the five lobes points upwards or diagonally upwards.

Regarding Lobelia sessilifolia and Lobelia sessilifolia, in Lobelia sessilifolia, the lower three of the five corolla lobes are obovate, and the upper pair protrudes upward, while in Lobelia sessilifolia, the lower three of the five corolla lobes are lanceolate, and the upper pair protrudes diagonally upward.

This involves a bit of technical jargon, but essentially, the corolla lobes of Lobelia sessilifolia are more elongated than those of Lobelia sessilifolia.

Furthermore, their growth patterns differ; the stems of Lobelia sessilifolia and Lobelia laciniata grow in a creeping manner, while the stems of Lobelia sessilifolia grow upright (Kanagawa Prefecture Flora Survey Association, 2018).

Only the leaves of Lobelia sessilifolia are covered with hairs, while only the leaves of Lobelia sessilifolia have clearly visible lateral veins.

The above explains how to distinguish them. However, I am not aware of the difference between Lobelia sessilifolia and perennial lobelia, which is a hybrid of Lobelia sessilifolia and Lobelia sessilifolia. As the name suggests, Lobelia sessilifolia itself has red corollas.

What are the varieties of Lobelia sessilifolia and Lobelia sessilifolia?

Lophophora williamsii has undergone extensive breeding, resulting in countless cultivated varieties. While it's impossible to introduce them all, in terms of flower color, some have entirely white corollas, while others have white only in the center.

There is a variety of Lobelia sessilifolia called white-flowered Lobelia sessilifolia f. leucantha.

References

Kanagawa Prefecture Flora Survey Association. 2018. Kanagawa Prefecture Flora 2018 (Electronic Edition). Kanagawa Prefecture Flora Survey Association, Odawara. 1803pp. ISBN: 9784991053726

RBG Kew. 2024. The International Plant Names Index and World Checklist of Vascular Plants. Plants of the World Online. http://www.ipni.org and https://powo.science.kew.org/

Both Campanula punctata and Campanula punctata are annual plants native to North America, belonging to the Campanulaceae family and Campanula genus. In Japan today, they are naturalized species and are frequently seen in urban areas. Since they grow in almost the same places and both have purple flowers with five deep lobes at the top, it may be difficult to distinguish them in the wild. However, there are differences in their leaves, flowers, and fruits, and the leaves in particular can be distinguished regardless of the season. The size of the flowers differs from that of Campanula punctata. There are two types of flowers: open flowers and cleistogamous flowers. Open flowers are purple flowers with five deep lobes in a star shape. Cleistogamous flowers do not have a corolla. Cleistogamous flowers do not open their interiors to the outside and are self-pollinating, while open flowers are cross-pollinating by bees, etc. These two types of pollination methods are probably the secret to their ability to grow even in urban areas of foreign countries. The fruit is a capsule, and the seeds are dispersed by the wind through a hole in the ovary. This article will explain the classification, morphology, pollination ecology, and seed dispersal of the genus Campanula.

What are Campanula punctata and Campanula punctata?

Triodanis perfoliata, also known as bellflower, is native to North America and in Japan it is an annual plant that grows in sunny locations such as hedges and plantings in parks and along roadsides (Kanagawa Prefecture Flora Survey Association, 2018). It has also become naturalized in China.

Triodanis biflora, also known as dwarf bellflower, is native to North America and is an annual plant that grows in Japan in dry, bare areas such as roadsides and construction sites. The first recorded instance of its presence in Japan was in Yokohama in 1931. It has also become naturalized in China.

Both are annual plants native to North America, belonging to the genus Campanula in the family Campanulaceae. In present-day Japan, they are frequently seen in urban areas, and they grow in almost the same locations. They both have purple flowers with five deeply lobed corollas at the top. They also both produce cleistogamous flowers from the stems and leaves below the middle section, so it may be difficult to distinguish them in the wild.

What is the difference between bellflower and balloon flower?

Some people may not even know the difference between this plant and the bellflower (kikyo), from which it gets its name.

Balloon flower (Platycodon grandiflorus) is a perennial herb that grows in bright grasslands in mountainous areas and fields, distributed throughout Japan (Hokkaido, Honshu, Shikoku, Kyushu, and Ryukyu Islands), as well as Korea, China, and Ussuri.

However, wild specimens are now extremely rare, and most are cultivated for ornamental purposes. Therefore, unlike other types of bellflowers, you'll likely only see bellflowers in towns in gardens or flowerbeds.

There are many differences between bellflowers and balloon flowers, but the most notable is their size.

In the Campanula genus, the upright stems are 20-80 cm tall, while in the balloon flower (Platycodon grandiflorus), the stems are 40-100 cm tall, although balloon flowers are generally larger.

The flower sizes are completely different; the corolla of Campanula species is only 1-1.8 cm in diameter, while that of balloon flowers is 3-5 cm in diameter.

From a taxonomic perspective, the presence or absence of cleistogamous flowers is important. While the genus Campanula has flowers called "cleistogamous flowers" that do not have a corolla above the leaf, this is not the case with balloon flowers (Platycodon grandiflorus).

What is the difference between Campanula punctata and Campanula punctata?

There are many differences between Campanula punctata and Campanula japonica, but I think the leaves are the easiest way to distinguish them regardless of the season or individual variation. The leaves on the middle and upper parts of the stems of both Campanula punctata and Campanula japonica are sessile, but they differ considerably in shape.

In Campanula punctata, the leaves above the middle of the stem are elliptical with heart-shaped stems, their length is equal to or shorter than their width, their serrations are prominent, and their base clasps the stem. In contrast, in Campanula punctata, the leaves above the middle of the stem are ovate, their length is clearly longer than their width, their serrations are shallow, and they do not clasp the stem.

The next easy way to distinguish them is by their flowers. In Campanula punctata, open flowers grow in groups of 1-2 (or up to 3) in the leaf axils, with a corolla diameter of 1.5-1.8 cm, whereas in Campanula punctata, open flowers usually grow only 1 (or up to 2) at the top, with a corolla diameter of only 1-1.3 cm.

There are also differences in the fruits: in Campanula punctata, the pore of the capsule is located 1-1.5 mm from the top (excluding the calyx lobes) (in the center of the capsule), whereas in Campanula punctata, the pore is located about 0.5 mm from the top (excluding the calyx lobes) (at the top of the capsule). Many publications mention this difference, but it may be difficult to observe it conveniently in the field.

What is the structure of a flower?

The genus Campanula produces two types of flowers: open flowers and closed flowers.

The open flowers of the Campanula genus are common to all plants in the Campanulaceae family, with purple corollas that are deeply five-lobed and star-shaped, and they bloom facing upwards. However, there are also species in the Campanulaceae family, such as Campanula and Adenophora, whose flowers face downwards.

On the other hand, cleistogamous flowers do not have a corolla and their interiors do not open. They grow singly on each stem and leaf.

Campanula punctata flowers from May to July. The flowers are sessile or have short stalks and grow in clusters of 1-2 (up to 3) in the leaf axils. As the plant elongates, it produces cleistogamous flowers in the lower to middle sections and open flowers at the top. Open flowers have 5 sepals and a 5-lobed corolla, are purple, and 1.5-1.8 cm in diameter. Cleistogamous flowers have 3-4 sepals and a nearly vestigial corolla.

Campanula punctata flowers from April to July. It typically produces only one (or two) flowers at the top of the stem. The open flowers are purple and star-shaped, with a corolla 1-1.3 cm in diameter. Most flowers other than the one at the top are cleistogamous. The calyx usually has five lobes, but cleistogamous flowers often have three or four.

How is pollination done?

Cleistogamous flowers do not open their interiors to the outside, and self-pollination occurs through contact between the stamens and pistils within the flower. This is called cleistogamous fertilization. As a result, a certain number of seeds can be produced without relying on insects, and since the corolla does not need to be formed, the plant can allocate more energy to seed production.

However, self-pollination alone may result in insufficient genetic diversity to cope with changes in the natural environment and parasites. Furthermore, research has shown that seeds produced from open flowers develop more easily and grow stronger after germination (Gara & Muenchow, 1990). Therefore, cross-pollination by pollinating insects is likely essential.

According to research in the United States, Campanula plants are visited by bees of the families Sphecidae, Sphecidae, and Cantharidae, with occasional visits from the families Halictidae and Bumblebees (Gara & Muenchow, 1990; Stewart, 2013).

However, these species are relatively large among pollinating insects, and it is questionable whether individuals of the Campanula genus found in urban areas of Japan are pollinated by these insects. It is possible that there are differences, such as a higher proportion of self-pollination or a higher proportion of bee species, but there is insufficient research on this in Japan.

The ability to utilize both cleistogamous and open flowers is a major factor in its survival as a naturalized species that can grow even in urban areas.

The fact that Campanula punctata has fewer flowers than Campanula punctata suggests that it has more cleistogamous flowers and relies on self-pollination. This might be advantageous in urban areas where there are fewer insects and the environment is stable, but it is unclear whether this difference is significant. The insects that visit Campanula punctata are unknown, and the differences in the ecology of these two species are not understood.

What is the structure of the fruit?

The fruit is a capsule, common to all species in the genus Campanula (Wu et al., 2011). A capsule is a type of dry fruit, consisting of multiple fused sac-like pericarps. Capsules can develop from both open and closed flowers.

The capsules of Campanula are 4-6 mm long, cylindrical, and when mature, the ovary wall curls back in a tongue-like manner, opening a hole. The hole in the capsule is located 1-1.5 mm from the top (excluding the calyx lobes) (in the center of the capsule). Seeds fall out from the hole. The seeds are about 0.5 mm long, brown, lenticular, and flattened oval.

The capsule of Campanula punctata is 6-10 mm long, oblong-cylindrical in shape, and divided into three chambers. When mature, the ovary wall curls up in a tongue-like manner, opening a pore. The pore is located about 0.5 mm from the top (excluding the calyx lobes) of the capsule. Seeds fall out through the pore. The seeds are glossy brown, flattened oval in shape, and about 0.5 mm long.

What are the seed dispersal methods?

While most capsules dry out and release their seeds when ripe, the Campanula genus is unique in that the entire capsule does not open; instead, a part of the ovary wall curls up, creating a pore from which the seeds spill out.

This is thought to facilitate both gravity and wind dispersal (Tackett, 2021). While the advantages of this method, where part of the ovary wall flips up to release the seeds, haven't been specifically considered, it seems that wind would pass through the opening more efficiently than if the top were open, thus dispersing the seeds. The flattened elliptical shape would also be ideal for catching the wind.

There is a difference in the height of the holes between Campanula punctata and Campanula punctata, but it is unclear whether this difference is ecologically significant.

References

Gara, B., & Muenchow, G. 1990. Chasmogamy/cleistogamy in Triodanis perfoliata (Campanulaceae): some CH/CL comparisons in fitness parameters. American Journal of Botany 77(1): 1-6. https://doi.org/10.1002/j.1537-2197.1990.tb13521.x

Kanagawa Prefecture Flora Survey Association. 2018. Kanagawa Prefecture Flora 2018 (Electronic Edition). Kanagawa Prefecture Flora Survey Association, Odawara. 1803pp. ISBN: 9784991053726

Stewart, ER 2013. Hybridization in two subspecies of Triodanis perfoliata, a cleistogamous annual plant (Campanulaceae) [Master's thesis, East Carolina University]. http://hdl.handle.net/10342/4196

Tackett, M. 2021. Understanding Dispersal Corridors and Population Structure in a Widespread Annual Plant [Master's thesis, Southeast Missouri State University]. https://www.proquest.com/openview/5a9449a97a8f42d7c5d400a5422fc0d0/

Wu, ZY, Raven, PH, & Hong, DY (Eds.). 2011. Flora of China (Vol. 19 Cucurbitaceae through Valerianaceae, with Annonaceae and Berberidaceae). Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. ISBN: 9781935641049

Both Campanula punctata and Campanula punctata are perennial herbs belonging to the genus Campanula in the family Campanulaceae, and are very familiar plants in Japan, both as wildflowers and cultivated species. They are classified as the same species, differing only at the variety level. Their flower shapes are identical, with a urn-shaped corolla ranging from white to reddish-purple, making them difficult to distinguish. However, they can be reliably differentiated by examining the reflexed appendages between the sepals. They are completely different in flower orientation and shape from Campanula punctata, also known as "bellflower" or "bellflower." The urn-shaped flowers are not visited by fireflies, but almost exclusively by one species of bee, the bumblebee (Bombus ignitus). The inside of the flower is lined with hairs, which the bee uses as a foothold to enter, and pollination occurs when pollen gets on its back or touches the stigma of the pistil. The fruit is a capsule that, when ripe, scatters tiny seeds like dust, which are dispersed by the wind. Some even cross the ocean. This article will explain the classification, morphology, pollination ecology, and seed dispersal of Campanula punctata and Campanula punctata.

What are Campanula punctata and Campanula punctata?

Campanula punctata var. punctata, also known as the bellflower (or bellflower), is a perennial herb distributed in Hokkaido (southwestern part), Honshu, Shikoku, and Kyushu in Japan; as well as in Korea and China. It grows in grasslands, forest edges, bright forest floors, collapsed bare ground, and stone walls from lowlands to mountainous areas (Kanagawa Prefecture Flora Survey Association, 2018). It prefers relatively lowlands. It also grows in urban areas and is cultivated for ornamental purposes.

Campanula punctata var. hondoensis, also known as mountain bellflower, is a perennial herb distributed in Honshu, Japan (southern Tohoku region to Kinki region), growing in hilly and mountainous areas. It prefers relatively high altitudes.

There are two theories regarding the origin of the Japanese name: one suggests it comes from the fact that children used to play by putting fireflies inside the bag-like flowers of this plant, and the other suggests it means "firefly bag," referring to a paper lantern.

Both are perennial plants belonging to the genus Campanula in the family Campanulaceae, and are very common plants in Japan. In addition to growing as wildflowers, Campanula punctata in particular is cultivated for ornamental purposes, so it is often seen even in urban areas. However, distinguishing it from Campanula punctata var. japonica can be difficult. Campanula punctata and Campanula punctata var. japonica are classified as the same species, with only differences at the variety level. The characteristics of their corollas, which are urn-shaped and white to reddish-purple in color, are exactly the same, and no differences have been found in the shape of their leaves.

What is the difference between Campanula punctata and Campanula punctata?

The difference between Campanula punctata and Campanula punctata is slight, but they can be clearly distinguished when they are in bloom.

Specifically, the difference is that Campanula punctata has reflexed appendages between the calyx lobes, while Campanula punctata does not.

The expression "curved appendages" is used in various botanical guides, but it may be difficult to understand. In other words, it means that there is a curved part between each of the sepals (each individual sepal).

It's obvious from the photo, so please take a good look at the shape of the calyx.

Furthermore, while the seeds of Campanula punctata have almost no wings, those of Campanula punctata have narrow wings.

This point might be difficult to observe, but it would be interesting to take a look if you have the time.

Regarding habitat, while Campanula punctata is more common in lower elevations and Campanula punctata is more common in higher elevations, their distributions often overlap, so this should only be considered as a general guideline. It is safe to assume that most plants cultivated in urban areas are Campanula punctata, but it is best to confirm their morphology for certainty.

What is the variety of bellflower?

Several varieties of Campanula are known.

There are several varieties of Campanula punctata, including Campanula inpunctata f. inpunctata, which has flowers without spots; Campanula lucida f. lucida, which has glossy leaves; and Campanula rubriflora f. rubriflora, which has purple flowers.

There is a variety of Campanula punctata called f. albiflora, which has white flowers.

While both Campanula punctata and Campanula punctata have flower colors that vary from white to reddish-purple, the wild species of Campanula punctata is said to have white flowers, while the wild species of Campanula punctata is said to have purple flowers, which can be a bit confusing. This is related to the order in which they were scientifically described.

Other species, such as Campanula microdonta (a different species) found in the Izu Islands and Campanula takeshimana (a different species) found on Takeshima Island, are also known.

What is the difference between this and Campanula bellflower?

In horticulture, various introduced species such as Campanula medium are cultivated under the name "Campanula," and while we won't introduce all of them here, their corollas are usually not long enough to form a pouch like those of the Campanula genus, and most of them face sideways or upwards, so they can usually be easily distinguished.

What is the structure of a flower?

Flowers of the Campanula genus generally have bell-shaped corollas. However, Campanula punctata is distinctive in that its flowers face downwards, are elongated, and have a shape that is close to a vase.

Campanula punctata bears several downward-facing flowers in a spike-like inflorescence at the top of the stem (Wu et al., 2011). The corolla is 3-6.5 cm long, large and bell-shaped, shallowly 5-lobed at the tip, reddish-purple or white, with spots on the inner surface and densely covered with long hairs. There are 5 stamens. The stamens mature protogynously, releasing pollen while still in the bud. The pistil's style receives pollen, causing the flower to open, and the stigma opens after flowering. The calyx is 5-lobed, with narrow, elongated triangular sepals, and reflexed appendages in the indentations between the sepals, with many hairs along the edges.

The corolla of the Japanese bellflower (Campanula punctata) is 4-5 cm long, and otherwise it is almost the same as the common bellflower (Campanula punctata), but it does not have the reflexed appendages between the sepals.

How is pollination done?

Most of the Campanula punctata populations distributed on Honshu Island are self-incompatible. Therefore, cross-pollination by insects is essential. However, as the Japanese name suggests, fireflies do not naturally enter the area.

It is known that only the bumblebee Bombus diversus diversus visits Campanula punctata in the lowlands of Honshu (Inoue & Amano, 1986; Kobayashi et al., 1999; Tanaka, 2001; Nagano et al., 2014).

The flowers of the Campanula punctata undergo a type of sex change called "protandry," in which the sexual role changes from male to female over time (Tanaka, 2001). While in the bud stage, the stamens mature, but once the flower opens, the pollen from the stamens is transferred to the pollen-collecting hairs on the pistil's style. In this way, the pollen is concentrated in the pistil, preparing to be handed over to the bees (male phase). Flowers that move pollen in this manner are rare.

The arriving bee, seeking nectar, uses the hairs growing inside the corolla as a foothold to penetrate deep into the flower. At this time, the style of the pistil, which is covered in pollen, comes into contact with the bee's back, allowing it to pollinate the flower.

After about three days, the pollen is gone and the male phase ends, and the tip of the pistil (stigma) splits into three parts, transitioning to the female phase.

Similarly, bees penetrate deep into the corolla in search of nectar glands, but this time, as they penetrate, their backs come into contact with the curved stigma, receiving pollen from another individual and thus pollinating the flower.

In Honshu, the only pollinating insect is the bumblebee *Bombus spp.*, but interestingly, in the mountainous areas of central Honshu where *Bombus spp.* is scarce or absent, the small bumblebee *Bombus beaticola* is present (Nagano et al., 2014).

Furthermore, it has been found that on Oshima Island in the Izu Islands, where the species Campanula microdonta, which evolved from the common bellflower, is distributed, Bombus ardens ardens and members of the family Halictidae are found, while on Niijima, Shodoshima, and Hachijojima, only members of the family Halictidae are found (Inoue & Amano, 1986).

Consequently, the size of the flowers has also changed to adapt to the size of these bees. Furthermore, self-incompatibility has decreased in Campanula punctata, making self-pollination possible. This is thought to be a way to mitigate the risk of pollinating insects not visiting the flowers. This microevolution of flowers in response to pollinating insects, which has been observed in various plants, has now been confirmed in Campanula punctata. It can be said that this demonstrates the resilience of Campanula species, which enables pollination even in remote areas.

What is the structure of the fruit?

The fruits of the Campanula genus are all capsules. A capsule is a type of dry fruit, and a single fruit consists of multiple fused, sac-like pericarps.

The capsules of the Campanula punctata are bell-shaped or inverted cone-shaped, and the seeds are grayish-brown, smooth, and oval-shaped, about 1 mm in length.

The capsules of Campanula punctata are almost identical to those of Campanula punctata, but the seeds have narrow wings.

What are the seed dispersal methods?

When the capsule dries, it releases its seeds from the inside, and it is thought that at least gravity dispersal occurs.

However, the fact that the Japanese bellflower (Campanula punctata) has wings is interesting. Perhaps the Japanese bellflower is adapted to wind dispersal. However, both are dust-like and very small, so they are easily affected by wind in the first place, and the difference may be negligible.

While there are no records of this in *Campanula punctata*, it has been suggested that wind or water flow dispersal is the cause for *Campanula punctata* and *Campanula punctata var. japonica* (Oiki et al., 2001; Cheong et al., 2020). It appears that the ancestors of *Campanula punctata var. japonica* underwent long-distance seed dispersal across the sea by being carried by the wind.

References

Cheong, WY, Kim, SH, Yang, J., Lee, W., Pak, JH, & Kim, SC 2020. Insights from chloroplast DNA into the progenitor-derivative relationship between Campanula punctata and C. takesimana (Campanulaceae) in Korea. Journal of Plant Biology 63: 431-444. https://doi.org/10.1007/s12374-020-09281-3

Inoue, K., & Amano, M. 1986. Evolution of Campanula punctata Lam. in the Izu Islands: changes of pollinators and evolution of breeding systems. Plant Species Biology 1(1): 89-97. https://doi.org/10.1111/j.1442-1984.1986.tb00018.x

Kanagawa Prefecture Flora Survey Association. 2018. Kanagawa Prefecture Flora 2018 (Electronic Edition). Kanagawa Prefecture Flora Survey Association, Odawara. 1803pp. ISBN: 9784991053726

Kobayashi, S., Inoue, K., & Kato, M. 1999. Mechanism of selection favoring a wide tubular corolla in Campanula punctata. Evolution 53(3): 752-757. https://doi.org/10.1111/j.1558-5646.1999.tb05369.x

Nagano, Y., Abe, K., Kitazawa, T., Hattori, M., Hirao, AS, & Itino, T. 2014. Changes in pollinator fauna affect altitudinal variation of floral size in a bumblebee-pollinated herb. Ecology and Evolution 4(17): 3395-3407. https://doi.org/10.1002/ece3.1191

Oiki, S., Kawahara, T., Inoue, K., Ohara, M., & Maki, M. 2001. Random amplified polymorphic DNA (RAPD) variation among populations of the insular endemic plant Campanula microdonta (Campanulaceae). Annals of Botany 87(5): 661-667. https://doi.org/10.1006/anbo.2001.1389

Tanaka, Hajime. 2001. Flowers and Insects: A Collection of Discoveries of Mysterious Deception. Kodansha, Tokyo. 262pp. ISBN: 9784062691437

Wu, ZY, Raven, PH, & Hong, DY (Eds.). 2011. Flora of China (Vol. 19 Cucurbitaceae through Valerianaceae, with Annonaceae and Berberidaceae). Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. ISBN: 9781935641049

Adenophora triphylla, Adenophora fukushimaensis, and Campanula punctata are representative Japanese herbaceous plants that grow in forest edges and other areas, bearing numerous purple flowers. All belong to the Campanulaceae family and Adenophora genus, and are similar in that they grow in forests and bear downward-facing purple flowers, which can sometimes make them difficult to distinguish. However, if the flowers are in bloom, the shape of the flowers and the inflorescence can clearly distinguish the three species. The way the leaves are attached can also be a clue. The insects that visit and pollinate Adenophora triphylla flowers have been relatively well studied, and it has long been thought that the downward-facing purple flowers are attracted to bees, which are adept at hanging down, and that the same applies to Adenophora triphylla. However, further detailed research has revealed that it is not diurnal bees, but nocturnal moths that are directly involved in pollination. This has been revealed by studies on fruit set rates. It has also been found that Adenophora triphylla has adapted to be pollinated at night by opening its flowers and secreting nectar at night. However, other studies have shown that bees do contribute to pollination on some remote islands, which may explain regional differences and the large variations in flowers. The fruit is a capsule and the seeds are dispersed by wind. This article will explain the classification, pollination ecology, and seed dispersal of the Adenophora genus.

A herbaceous plant that grows in forest edges and other similar areas, bearing numerous purple flowers.

Adenophora triphylla (broad sense) is a perennial herb distributed in Hokkaido and the Southwest Islands of Japan, as well as Sakhalin, the Kuril Islands, Korea, China, and Taiwan. Adenophora triphylla var. japonica (narrow sense) is distributed in Sakhalin, the Kuril Islands, Hokkaido, Honshu, Shikoku, and Kyushu in Japan, and grows in mountainous areas, grasslands, forest edges, and managed riverbanks where grass is mowed (Kaizu, 1995; Baba and Onuki, 1996). It is also known for its edible and medicinal uses. Adenophora japonica is distributed in Honshu and the Izu Islands, and grows in grasslands near the coast. Adenophora hakusanensis var. hakusanensis is distributed in Hokkaido and Honshu (north of the Chubu region), and grows in high mountains. Adenophora triphylla var. triphylla is distributed in Honshu (west of the Chugoku region), Kyushu, Okinawa, and China, growing in mountainous areas and plateaus. Its Japanese name comes from the fact that its bell-shaped flowers resemble the thick roots of Panax ginseng, a traditional Chinese medicine.

Fukushima Adenophora divaricata, also known as Fukushima bellflower, is a perennial herb distributed in Honshu (north of the Chubu region) and Shikoku, as well as Korea and China (northern and northeastern regions), growing in bright woodlands and grasslands from hilly to mountainous areas. Its Japanese name comes from the fact that it was based on a specimen from Fukushima Prefecture. "Shajin" is the name of a crude drug made from the roots of Adenophora triphylla.

Adenophora remotiflora, also known as sobana, is a perennial herb distributed in Honshu, Shikoku, Kyushu, Korea, and China, growing in the forest floor, forest edges, and grasslands of hilly areas and fir forest zones. There are several theories about its Japanese name, but the most likely origin is that it was originally "soba-na" (buckwheat vegetable), and that the vegetable was steamed and then cut in the same way as buckwheat to make porridge (kon-gayu).

Both belong to the Campanulaceae family, genus Adenophora, and are similar in that they grow in forests and bear downward-facing purple flowers. Therefore, it may be difficult to distinguish between them.

What are the differences between Adenophora triphylla, Adenophora fukushimaensis, and Campanula punctata?

However, the three species Adenophora triphylla, Adenophora fukushimaensis, and Campanula punctata can be clearly distinguished when they are in bloom (Ohashi et al., 2017; Kanagawa Prefectural Flora Survey Association, 2018).

First, while the corollas of Adenophora triphylla and Adenophora fukushimaensis are bell-shaped, the corolla of Adenophora umbellata is funnel-shaped.

Regarding the two species, Adenophora triphylla and Adenophora fukushimaensis, Adenophora triphylla has linear calyx lobes with sparsely spaced serrations that end in glands, while Adenophora fukushimaensis has lanceolate calyx lobes with entire margins. In short, Adenophora triphylla has narrower calyxes.

Another difference is that the inflorescence branches of Adenophora triphylla are usually arranged in whorls, while those of Adenophora fukushimaensis are usually arranged alternately.

There may also be differences in the shape and arrangement of the leaves.

In Campanula punctata, the upper leaves are sessile, but the middle stem leaves are stalked, alternate, ovate or lanceolate, with coarse serrations along the edges. In contrast, in Adenophora triphylla and Adenophora fukushimaensis, the middle stem leaves are almost sessile, opposite or alternate, but usually whorled, ovate-elliptic, with fine serrations.

It can be difficult to distinguish between Adenophora triphylla and Adenophora fukushimaensis by their leaves alone, but Adenophora fukushimaensis is said to have slightly lighter leaves.

While the three species listed above are generally considered to be the genus Adenophora, there are actually 12 known species in Japan, including those mentioned above, and this list alone is insufficient to distinguish them all. Many have speciated due to adaptation to specific environments.

To give a few examples, Adenophora takedae is distributed in Honshu (southeastern Chubu region and western Kanto region), growing on slightly damp rocky areas and cliffs in mountainous regions, with slender stems that hang down from rocks and steep cliffs.

Adenophora nikoensis is distributed in Honshu (southern Tohoku region to central region), growing in rocky areas of subalpine and alpine regions. It resembles Adenophora fukushimaensis but is smaller, and its leaves are usually alternate.

Adenophora pereskiifolia, also known as Moiwa bellflower, is distributed in Hokkaido and Honshu (Tohoku region), growing on rocky areas in mountainous regions. It resembles Adenophora fukushimaensis, but is smaller in size.

Adenophora maximowicziana is distributed in Shikoku, grows in limestone areas, is quite small, and has linear-lanceolate leaves.

What are the differences between Adenophora triphylla and Adenophora triphylla? What are the other varieties?

The above gives you a general idea of the species, but several varieties of Adenophora triphylla (in the broad sense) are known (Ohashi et al., 2017; Kanagawa Prefectural Flora Survey Association, 2018). There are also many cultivars, but we will omit them here.

Adenophora triphylla var. triphylla is distinguished from Adenophora triphylla (in the narrow sense) by its slightly narrower, urn-shaped corolla and its long, protruding style. However, there doesn't seem to be a specific indicator of how long the style needs to be to be considered Adenophora triphylla. Judging from the photographs by Ohashi et al. (2017), the style appears to be about twice the length of the corolla.

Adenophora triphylla var. glabra is distributed in Honshu and the Izu Islands, growing in grasslands near the coast. Unlike Adenophora triphylla (in the narrow sense), its leaves are leathery and glossy on the upper surface.

Campanula hakusanensis is distributed in central and northern Japan, as well as Hokkaido. It grows in high-altitude areas and is smaller in size, but some argue that it should not be distinguished from Campanula hakusanensis because similar individuals can be found in lowlands (Ohashi et al., 2017).

Adenophora triphylla var. puellaris is distributed in Shikoku (Higashiakaishi Mountain, Ehime Prefecture) and grows on serpentine rock. Unlike Adenophora triphylla (in the narrow sense), its leaves are remarkably narrow and linear.

Adenophora triphylla var. insularis is distributed in the Southwest Islands of Japan and appears to be a type with a bell-shaped corolla and a pistil that does not protrude much, but the distinguishing features from Adenophora triphylla (in the narrow sense) are unclear.

Other species such as *Campanula japonica* var. *sasamotoi * and *Campanula fragrans* var. *verticillata* are not found in Japan.

What is the structure of a flower?

Adenophora triphylla blooms from August to October, producing conical inflorescences at the top of the stems, with one to several flowers arranged in whorls and slightly downward-facing (Kadota et al., 2013). The bell-shaped corolla is pale purple or white, 1.5–2 cm long, with five lobes that spread slightly at the tip. The style protrudes slightly beyond the corolla and is shallowly three-lobed at the tip. The calyx lobes are linear, 3–5 mm long, with one to four small serrations along the edges.

Fukushima Campanula flowers from August to September, with the lateral branches of the inflorescence extending horizontally and forming a sparse conical shape. The bell-shaped corolla is pale purple to white, 1.5-2 cm in diameter, and shallowly 5-lobed at the tip, slightly spreading out. The style is the same length as the corolla or slightly protruding. The calyx lobes are lanceolate, 4-8 mm long, and have entire margins.

Campanula punctata flowers from August to October, bearing sparse flowers in a conical inflorescence at the top of the plant. The flowers droop downwards. The bell-shaped corolla is pale purple, 2-3 cm long, and has five lobes that widen at the tip. There are five stamens. The style usually does not protrude beyond the corolla, but it can. The stigma is three-lobed. The calyx lobes are lanceolate and entire.

The purple color is a common characteristic of the Campanulaceae family, and although the shape of the corolla and the way the flowers are arranged differ slightly, they are basically very similar.

Adenophora triphylla is known to exhibit "protandry," meaning it is male first. In protandry, the stamens wither after releasing pollen during the male phase, then transition to the female phase, during which the club-shaped tip of the pistil develops and splits into three lobes.

It's been said that flowers are pollinated by bees, but is that actually not true?!

Among these species of Adenophora, the question of which insects visit the flowers of Adenophora triphylla and pollinate them has long been studied in Japan.

Generally, downward-facing purple flowers are well known to attract bees, which are adept at hanging from them. For this reason, it was long believed that the same was true for Adenophora triphylla (Tanaka and Hirano, 2000; Utsumi, 2003).

However, recent research suggests that different insects also engage in pollination at completely different times, and that these insects may be the ones making a significant contribution to pollination.

A study conducted over 24 years in southwestern Japan, investigating which moths visited the flowers of various plants (Ikenoue & Kanai, 2010), and a study examining daytime and nighttime pollinating insects in Ibaraki and Nagano prefectures (Funamoto & Ohashi, 2016; Funamoto & Ohashi, 2017; Funamoto, 2021), concluded that the insects contributing most to pollination are "nocturnal moths."

In particular, studies in Ibaraki and Nagano prefectures have not only meticulously observed and recorded pollinating insects for sufficient time both day and night, but have also investigated whether diurnal or nocturnal pollinating insects contribute more to fruit setting by attaching bags to flowers to prevent insects from approaching them only during the day and night.

The results showed that while insects were observed both day and night, with butterflies, bees, and syrphidae making up the majority during the day and moths at night, experiments with bags attached showed that only nocturnal pollinating insects contributed significantly to the increase in fruit set. The fruit set rate of flowers visited only by diurnal pollinating insects was almost the same as that of flowers where bags were attached all day to eliminate insect influence, indicating an extremely low fruit set rate.

Therefore, it is natural to conclude that the presence of moths at night, rather than insects during the day, is very important for the pollination of Adenophora triphylla.

This has been found to be the same for Campanula punctata (Funamoto, 2019).

Why do only certain nocturnal moths contribute to pollination?

However, it seems that not all moths visit the flowers of Adenophora triphylla. Specifically, two groups of nocturnal moths have been identified that visit: Noctuidae and Pyraloidea.

Why don't these daytime insects and moths other than the two groups mentioned above contribute to the pollination of Adenophora triphylla?

In the case of moths of the Noctuidae and Pyraloidea superfamilies, pollination occurs when the moth first firmly places its legs on the tip of the corolla or the style (the part slightly below the tip of the pistil) and then extends its proboscis inside, causing the moth's thorax or abdomen to come into contact with the anthers (the tips of the stamens) or stigma (the tip of the pistil) of the flower (Ikenoue and Kanai, 2010).

This behavior requires the insect to burrow deep into the flower, so even if moths or hoverflies with short proboscises come, they cannot properly contribute to pollination. Conversely, butterflies have proboscises that are too long, so they become nectar robberies that steal nectar without touching the stamens or pistils, and thus do not properly contribute to pollination.

There is another possible reason for this in the case of bees. Bees are known to have a high "pollen discounting" rate. This is a phenomenon in which the behavior of insects produces wasted pollen that does not contribute to pollination. Bees consume pollen as food or drop it during grooming, behaviors not seen in other insects, thus lowering their pollination rate.

Furthermore, although not mentioned in the paper, it is well known that some bees have the characteristic of visiting all the flowers on the same inflorescence in succession. When this behavior occurs, the pistil of the flower becomes covered with its own pollen, promoting self-pollination (stigma cover by neighboring flower pollination).

It is known that self-pollination of Adenophora triphylla results in a low fruit set rate. Furthermore, the inflorescence is densely covered with flowers, and neighboring flower pollination by bees may be inefficient for Adenophora triphylla in terms of seed production.

Why do moths come to downward-facing blue flowers?

By the way, you might find it strange that moths visit bellflower blossoms. As mentioned above, downward-facing purple flowers are well known to attract bees, which are adept at hanging down. In addition, moths are known to prefer upward-facing, white, and fragrant flowers.

What characteristics attract nocturnal moths to blue flowers?

First of all, the characteristic of hawk moths preferring white, strongly scented flowers applies to them, but ordinary nocturnal moths sometimes prefer blue-ish colors. Therefore, it's not that unusual for a moth to be attracted to a blue flower.

In addition to this, it is thought that three other characteristics of the Adenophora triphylla flower, besides its shape, are also involved.

These are the "timing of flowering," the "timing of the start of the female phase," and the "timing of nectar production."

Experiments have shown that Adenophora triphylla rapidly opens its flowers in the inflorescence starting around 6 PM.

Furthermore, while Adenophora triphylla changes the sex of its flowers from male to female over time, experiments have shown that this change occurs between 6 PM and 5 AM, with the sex change occurring gradually each time night falls.

Furthermore, experiments have shown that the best time to produce honey is between 6 PM and 5 AM.

These characteristics suggest that Adenophora triphylla flowers are more actively attracting insects at night than during the day, preparing for pollination. This is likely a factor that allows nocturnal moths to actively visit the flowers.

The characteristics of flowers on Miyakejima Island have evolved even further!?

However, some islands in Japan have shown results that differ from these studies.

A study conducted on Miyakejima Island revealed that, contrary to reports from the mainland, diurnal bees were observed visiting flowers, and their flower-visiting efficiency was remarkably high compared to nocturnal lepidopterans (Okazaki et al., 2019).

Since this study hasn't been formally published in a paper yet, we don't know the details such as the fruiting rate, but it points out that "the nectar-secreting disc is morphologically differentiated." If that's the case, it's quite possible that the nectar secretion time has also changed.

This can be considered an adaptation to the surrounding insect habitat.

Considering this, it's possible that Adenophora triphylla, originally designed to appeal to nocturnal insects, has adapted to appeal to diurnal insects, or vice versa, with its characteristics shifting depending on the region. This could also explain the significant variation in flower color and shape within the species or between species of the same genus.

It is well known that the characteristics of different species are not necessarily fixed but can change subtly depending on the environment. When looking at Adenophora triphylla, if you look at its physiological aspects from this perspective, rather than just its shape, you might discover something different.

The fruit is a capsule and the seeds are dispersed by wind.

As is common with the genus Adenophora, the fruit is a capsule.

The capsules of Adenophora triphylla turn straw-colored in winter, hang down, and split open at the top. The seeds are about 1.5 mm long and have a narrow wing on one side.

The capsule of Adenophora umbellata dehisces through the intercostal spaces on the lateral wall.

Campanula punctata has a capsule that is flattened and spherical in shape, with distinct longitudinal veins and a persistent calyx.

The capsules of the Adenophora genus split open at the top, and when they are turned upside down by wind, the seeds fall out little by little. The seeds are quite small, and at least in Adenophora species, they have narrow wings, making it highly likely that they are dispersed by wind. Their distribution throughout Japan suggests that they have a reasonable capacity for dispersal, but the details are not well understood.

References

Baba, Atsushi & Onuki, Shigeru. 1996. 500 Medicinal Herbs: From Cultivation to Uses. Seibundo Shinkosha, Tokyo. 167pp. ISBN: 9784416496183

Funamoto, D. 2019. Precise sternotribic pollination by settling moths in Adenophora maximowicziana (Campanulaceae). International Journal of Plant Sciences 180(3): 200-208. https://doi.org/10.1086/701734

Funamoto, Daichi. 2021. Exploring the Co-evolution of Flowers and Animals: New Flower Forms Hidden in Familiar Wild Plants, Chapter 4: Moths that Carry Pollen from Adenophora triphylla. *Journal of Species Biology* 40/41: 81-92. ISSN: 0913-5561, ISBN: 9784829962084

Funamoto, Daichi & Ohashi, Kazuharu. 2016. Pollination mode mismatched with appearance: Pollination of Adenophora triphylla relies on nocturnal moths. Tsukuba Journal of Biology 15: 60. ISSN: 1347-7048, http://gradtex.biol.tsukuba.ac.jp/2015/tjb201601/201210593.pdf

Funamoto, D., & Ohashi, K. 2017. Hidden floral adaptation to nocturnal moths in an apparently bee-pollinated flower, Adenophora triphylla var. japonica (Campanulaceae). Plant Biology 19(5): 767-774. https://doi.org/10.1111/plb.12579

Ikenoue, Toshiyuki & Kanai, Hiroo. 2010. Nocturnal moth flower-visiting activity. Journal of the Botanical Society of Japan 85(4): 246-260. ISSN: 0022-2062, https://doi.org/10.51033/jjapbot.85_4_10230

Kadota, Y., Nagata, Y., & Azegami, N. 2013. Flowers Blooming in the Mountains (Revised and Expanded New Edition). Yama-kei Publishers, Tokyo. 616pp. ISBN: 9784635070218

Kaizu, Yoshitaka. 1995. Medicinal Herbs of Japan. Shogakukan, Tokyo. 279pp. ISBN: 9784092080164

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Okazaki, Junko; Minamiguchi, Kosuke; Hasegawa, Masahiro; Abe, Harue; and Suzuki, Koji. 2019. Morphological variation and pollinating insect fauna of Adenophora triphylla, a Campanulaceae family species exhibiting protandry, in the Izu Islands. Abstracts of the Annual Meeting of the Ecological Society of Japan 66: P2-164. https://www.esj.ne.jp/meeting/abst/66/P2-164.html

Ohashi, Hiroyoshi; Kadota, Yuichi; Murata, Hitoshi; Yonekura, Koji; and Kihara, Hiroshi. 2017. Wild Plants of Japan (Revised New Edition, Vol. 5: Convolvulaceae to Caprifoliaceae). Heibonsha, Tokyo. 760pp. ISBN: 9784582535358

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Source

This article is a significantly expanded version of a piece originally published in the following book.