The enigmatic fast leaflet rotation in Desmodium motorium

Abstract

I propose that the enigmatic leaflet movements in elliptical circles every few minutes of the Indian telegraph (semaphore) plant Desmodium motorium ( = D. gyrans = Hedysarum gyrans = Codariocalyx motorius), which has intrigued scientists for centuries, is a new type of butterfly or general winged arthropod mimicry by this plant. Such leaflet movement may deceive a passing butterfly searching for an un-occupied site suitable to deposit its eggs, that the plant is already occupied. It may also attract insectivorous birds, reptiles or arthropods to the plant because it looks as if it is harboring a potential prey and while they patrol there, they can find insects or other invertebrates that indeed attack the plant. The possibility that diurnal mammalian herbivores may also be deterred by these movements should not be dismissed.

Keywords: :

• butterfly mimicry
• deception
• defence
• Desmodium
• herbivory
• leaf movement

Adaptive plant organ movement has attracted considerable scientific attention since Darwin’s time.¹ The best known examples are sun tracking,² prey-driven movements, i.e., of Dionaea³ and movements during self seed dispersal (autochory).² Quick anti-herbivory plant movements are best known in Mimosa pudica and several other related taxa that down-fold their leaflets to reduce visibility when mechanically perturbed.³ Braam⁴ proposed that Mimosa leaflet movement may also deter herbivores. Leaflets of Schrankia micropylla down-fold when touched, and by doing this expose their thorns,⁵a type of induced visual aposematism.⁶ In Cardamine scutata, silique bursting expels and even kills chewing caterpillars, thus defending its seeds.⁷ In addition, Yamazaki,⁸ in a broad and intriguing theoretical treatment of potentially defensive plant movements, advocated the hypothesis of considering the possible roles of passive leaf movement in wind and rain as a common anti-herbivory defense. Interestingly, all plant taxa expressing quick active leaf movements (Dionaea, Mimosa pudica, Schrankia micropylla and Desmodium motorium) are found in warm parts of the globe, probably because high temperatures allow quick movements in ectothermal plants.

One of the most dramatic and enigmatic quick plant movements, for which there is no proposed adaptive hypothesis, is that of the Indian telegraph plant Desmodium motorium, also known as D. gyrans. The plant has large leaves that perform typical slow sleep (nyctinastic movement) movements at night as well as smaller stipules that move during the day in conspicuous quick elliptical circles every few minutes, and under high temperatures (35°C) may execute a round in 90 sec.³ The structural-physiological mechanism allowing this quick leaflet rotation is based on pulvinar motor cells that induce movement by volume change mediated via plasma membrane depolarization.^9,10 The enigmatic function of this conspicuous movement has intrigued scientists for centuries. Darwin¹ (page 364) wrote: “No one supposes that the rapid movements of the lateral leaflets of D. gyrans are of any use to the plant; and why they should behave in this manner is quite unknown,” a statement that is still valid today. The fact that this leaflet movement is similar in timing, size and duration to slow butterfly rest wing movements was never considered.

I propose a probable function for this unique fast leaflet movement, that it mimics a butterfly, butterflies, or any winged arthropod (herbivorous or predaceous) that occupies the plant. Resting butterflies commonly move their wings to control exposure to the sun.¹¹ Since the plant has many stipules, and each pair moves once in a few minutes (see Desmodium in youtube.com), to a passing butterfly searching for an unoccupied site suitable to deposit its eggs, the plant may look as if it is already occupied. This principle (deceptive mimicry of being occupied) was found by experiments to operate in several Passiflora species that express butterfly egg mimicry by producing small yellow bulges on their leaves, which has been suggested to reduce egg-laying by Heliconius butterflies, and seems to operate also for other plant and butterfly taxa.^12-16 The second type of defensive butterfly mimicry in this genus was proposed by Rothschild¹⁷ for the stipules along the branches of Passiflora caerulae, which resemble caterpillars crawling along the stems. Potential defensive visual butterfly mimicry in the shape of caterpillar mimicry was also proposed to exist in the pods of various legumes.¹⁸ Moreover, stipule movement in D. gyrans may attract predacious birds, lizards or arthropods, deceived by the movements concerning the existence of a potential winged arthropod prey, and while carefully examining the plant at close range, may catch and consume or parasitize insects and other invertebrates that occupy it. The defensive role for plants of insect predators is well documented.^{19, 20} The visual predator attraction hypothesis was proposed previously irrespective of plant movement for the lobed shape of various leaves.^21,22 Predator attraction to leaves was found to increase plant fitness in many cases, i.e., by producing extrafloral nectaries that feed bodyguards,²³ by emitting volatiles^24-26and by sticking small insects to leaves by sticky trichomes.²⁷

The visual aspect of plant movement as a way of communication with (and deception of) animals has already been studied in two cases of pollinator attraction. In the first, some orchid species belonging to the genus Oncidium induce attacks by territorial male Centris bees when the inflorescences move in the wind, because the male bees mistake them for rival male bees. During the attacks of the moving pseudo rivals, the male bees transfer the pollen.²⁸ In the other case, Warren and James (2008)²⁹ showed that movements (“waving”) of the inflorescences of Silene maritima increase pollination success. Thus, following such functional examples from pollination biology, there is no theoretical reason to dismiss the possibility that actual and relative plant movements may take part in visual defense from herbivory. As for the defensive potential of plant movement combined with arthropod mimicry, Lev-Yadun and Inbar¹⁸ proposed that black anthers of Paspalum that move with a light wind may look like swivelling aphids. Later, Lev-Yadun⁶ proposed that the swaying of leaves, stems or branches in the wind may help in visual ant mimicry by plants by creating the illusion that the pigmentation patterns proposed to mimic “ants” (e.g., Ref. 18) actually move, thus providing a better visual illusion.

Concerning experimentation, the best experiment is to compare herbivore attacks and attraction of predators to mutants of D. motorium that do not move their leaflets (such mutants have not been described yet) as compared with the wild-type. The alternative is to do so with mechanical models in which it is possible to control “leaflet” movements, or to block leaflet movements in D. motorium by various inhibitors.

I conclude by proposing that the enigmatic quick diurnal leaflet movements of the Indian telegraph plant D. motorium (D. gyrans), which has intrigued scientists including Charles Darwin for centuries, is a type of defensive butterfly or other winged arthropod mimicry by plants.

Acknowledgments

I thank Moshik Inbar for his comments.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.