Proc. NatL Acad. Sci. USAVol. 78, No. 1, pp. 402-404, January 1981Evolution

Leaffolding in a sensitive plant: A defensive thorn-exposuremechanism?

(adaptation/plant movement/defense)

THOMAS EISNERSection ofNeurobiology and Behavior, Division of Biological Sciences, Cornell University, Ithaca, New York 14853

Contributed by Thomas Eisner, October 15, 1980

ABSTRACT Quantitative photographic evidence is presentedindicating that in the sensitive plant Schrankia microphyila theleaf-folding response that. accompanies the sensitive reaction re-sults in a pronounced increase in thorn exposure. It is argued thatin sensitive plants that are thorny, including other species ofSchrankia, as well as Mimosa pudica, the plant in which the sensi-tive reaction is traditionally demonstrated, leaf folding may be adefensive adaptation.

To my knowledge, no adaptive function has been demonstratedfor the peculiar leaf-folding reaction of sensitive plants. Typi-cally, such plants respond to mechanical disturbance such asprodding or pinching oftheir leaves or shaking oftheir branchesby folding their leaflets inward, rotating these in such fashionthat those of opposing rows become facially appressed (1). Thephenomenon is well known to naturalists and is often demon-strated as a curiosity to students in introductory biology courses.The sensitive reaction is quick and graded. It is initiated withinthe second following disturbance (2) and at first involves onlythe leaflets closest to the site stimulated. However, with contin-uing stimulation, it spreads to adjacent leaves and eventuallyover the entire plant. The reaction is reversible. Slowly, over aperiod of minutes following stimulation, the leaflets unfoldagain (2). The most obvious visual consequence of the sensitiveresponse is a sudden and pronounced reduction in the apparentleaf surface. Mimosa pudica is the leguminous plant classicallychosen to exemplify the phenomenon, but the sensitive reactionalso occurs in other plants (1).

I have obtained evidence suggesting that in Schrankia micro-phylla (Leguminosae), a sensitive plant indigenous to the south-ern United States, leaf folding could play a defensive role. Theplant is a sprawling vine-like shrub. Its leaves are bipinnatelycompound, with leaflets arranged in opposite rows along thesecondary branchings (rachillae) of the primary shaft (rachis) ofthe leaf (Fig. LA). The entire plant is thorny. The thorns arehard, recurved, extremely sharp, and firmly attached. They aredensest and largest along stems and branches. Even the smallestthorns, on the rachillae, can pierce human skin and be felt.Stumbling into a Schrankia plant can- be a painful experience.The sensitive reaction involves the quick propagated folding ofthe leaflets (Figs. 1 and 2 A-C). In an extensively stimulatedplant, the leaves literally appear to disappear from view (Fig. 2D and E).

Leaves in a thorny plant, to the extent that they may obstructthe thorns, can interfere with the plant's defenses. Only-in suchplants as cacti, on which the thorns project outward unimpededand are essentially permanently deployed, is the problem non-existent. Visual examination alone had indicated that increasedthorn exposure is the invariable consequence ofleaffolding in S.

FIG. 1. Portion of leaf of S. microphylla (severed about midwaythrough the rachis) before (A) and after (B) induction of the sensitivereaction. Note.that as a consequence of leaflet folding, there is in-creased exposure of thorns on the rachillae and rachis.

microphylla. The quantitative evidence was provided by pho-tography. Paired photographs were taken ofportions ofSchran-kia plants before and after elicitation ofthe sensitive reaction bymanual stimulation. Constancy of photographic viewing anglefor each pair ofpictures was assured by placing the camera on atripod. A total of37 pairs ofphotographs were taken (18 Schran-kia plants) of viewing fields (35-mm photographic film format)approximately 10-30 cm wide. Counts of visible thorns weremade from enlarged. prints of the photographs, providing thebasis for calculation, for each pair of pictures, of the percent in-crease in thorn exposure following leaf folding. The number ofthorns visible before and after stimulation were in the range of5-145 and 9-218, respectively. As is -evident from the results(Fig. 3), the, percent increase in thorn exposure is substantial,with a peak in the range of 100% and a recorded maximum ofover 300%. Portions of representative photographs from whichcounts-were made are shown in Fig. 2 F-I.

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Proc. Natl. Acad. Sci. USA 78 (1981) 403

FIG. 2. (A-C) Sensitive reaction in a leaf ofS. microphylla. A terminal rachis has been pinched by hand, causing the leaflet-folding response tospread from the site stimulated to the base of the leaf. Photographs were taken over a period of a few seconds. (D and E) Portion of S. microphyllaplant before (D) and after (E) induction of the sensitive response by sweeping a hand across the plant. (F and G, H and I) Portions of two pairs ofphotographs from which the number of thorns was determined to measure the percent increase in thorn exposure that accompanies the sensitiveresponse. F andH show portions of plants before stimulation; G and I show the same regions after stimulation. The white circles have been placedbeside thorns newly exposed as a result of leaffolding. (Bars: A = 3 cm;D = 10 cm;F andH = 2 cm.)

A second potentially defensive feature of Schrankia is theseemingly hinged attachment of the rachillae to the leaf rachis.As is depicted in Fig. 4, if a rachilla is deflected mechanically(e.g., by pushing it from one side or the other with a finger), itrotates around and swings past the rachis without contacting thethorns of the latter. The mechanism appears designed to pre-vent thorn obstruction when disturbance is relatively gross andthe plant is in potential need of maintaining its deployed weap-onry unencumbered.

Nothing definitive appears to be known about natural ene-mies of Schrankia although one can easily envision how, by ac-tivated exposure of nonspecific traumatizing devices such asthorns, the plant might gain protection against herbivores.Mammalian browsers might be among the principal enemiesdiscouraged by thorn exposure, but molluscs and insects couldalso be affected. Thorn exposure could even protect the plantagainst being trampled ifroaming animals, upon contacting theplant and activating its defenses, are thereby deterred and re-routed.

Leaf folding, not as a sensitive reaction but as a recurringnight-long "sleeping" (or nyctinastic) movement, occurs in a di-versity of plants, including numerous Leguminosae (1). Littledefinitive is known about the adaptive role of such sleepingmovements, which have been said to serve for reduction of ra-diative heat loss (3, 4) and for other functions (1, 5). Whateverthe evolutionary ancestral role or roles of such sleeping move-

ments, I would propose that in thorny plants, when such move-ments occur, they could also serve for defense inasmuch as theycould provide for automatization ofthorn exposure during dark-ness when maximization of exposure of leaf surfaces for photo-synthetic purposes is unnecessary. The sensitive reaction in

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100 200% increase thorn exposure

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FIG. 3. Percent increase of thorn exposure plotted as a function ofincidence (n = 37). See text for details.

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Proc. Natl. Acad. Sci. USA 78 (1981)

FIG. 4. Portion of leaf (leaflets folded; comparable to Fig. 1A) in which one rachilla is being deflected (e.g., by pushing with a finger) in thedirection of the arrows shown. Note that the trajectory of rotation of the rachilla is such that it sweeps past the rachis without touching the latter.Thorn interference, such as might otherwise occur under conditions ofgross disturbance ofthe plant, is thus prevented.

Leguminosae might perhaps best be viewed as an evolutionarilyspecialized sleeping movement, specialized in the sense that itis inducible in the daytime and by mechanical stimulation. Insensitive plants that are thorny, I would suggest that the spe-cialization occurred without shift in the defensive function. In-terestingly, thorniness appears to be the rule in the genusSchrankia (pressed specimens of S. nuttallii, S. uncinata, S. acu-leata, S. leptocarpa, and S. distrachya that I examined at theBailey Hortorium, Cornell University, are all thorny), and also,of course, in M. pudica. Although I cannot be certain that allthorny sensitive plants also show conventional sleeping move-ments, some certainly do. Both S. microphylla and M. pudicaspend the night with their leaflets folded, in what I would argueto be a state ofimproved defensive readiness.

This study was carried out at the Archbold Biological Station, LakePlacid, Highlands County, Florida. I thank the staff of the Station forhelp and hospitality, Dr. Ruth L. Satter, Yale University, for helpful dis-cussion, and my daughter Vivian Eisner for making the drawings.

1. Satter, R. L. (1979) in Encyclopedia of Plant Physiology: PlantMovements, eds. Haupt, W. & Feinleib, M. E. (Springer, NewYork), Vol. 7, pp. 442-483.

2. Oda, K. & Abe, T. (1972) Bot. Mag. 85, 135-145.3. Darwin, C. R. (1896) The Power ofMovement in Plants (Appleton,

New York).4. Smith, A. P. (1974) Biotropica 6, 263-266.5. Bunning, E. & Moser, I. (1969) Proc. NatL Acad. Sci. USA 62,

1018-1022.

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