Partly transparent young legume pods: Do they mimic caterpillars for defense and simultaneously enable better photosynthesis?

Abstract

Being partly or fully transparent as a defense from predation is mostly known in various groups of aquatic animals and various terrestrial arthropods. Plants, being photosynthetic and having cell walls made of various polymers, cannot be wholly transparent. In spite of these inherent limitations, some succulent plant species of arid zones have partially transparent “windows” in order to perform photosynthesis in their below-ground leaves, as defense from herbivores as well as for protection from harsh environmental conditions. Similarly, transparent “windows” or even wholly transparent leaves are found in certain thick or thin, above-ground organs irrespective of aridity. The young pods of various wild annual Mediterranean legume species belonging to the genera Lathyrus, Pisum and Vicia are partly transparent and may therefore look like caterpillars when viewed with back illumination. I propose that this character serves 2 functions: (1) being a type of defensive caterpillar mimicry that may reduce their consumption by various herbivores in that very sensitive stage, and (2) simultaneously allowing better photosynthesis in the rapidly growing seeds and pods. Unlike animals that are transparent for either defensive or aggressive crypsis, in the case of young legume pods it allows them to visually mimic caterpillars for defense.

Introduction

Being transparent as defense from predation or as crypsis toward prey is mostly known in various groups of aquatic animals.^1-4 Theoretically, all transparent organisms can be seen, although not at all parts of the spectrum and not under all lighted conditions. Therefore, in spite of being imperfect, being transparent is a practical solution for crypsis in many animals. In terrestrial habitats and even in shallow aquatic habitats being transparent for defense from predation or as crypsis from prey increases the risks of UV damage.⁴ The number of terrestrial animals that use transparency for crypsis is low, and this character is found mostly in arthropod wings. The great differences in reflection of transparent organisms in very different media such as air versus water, as well as the generally much lower visibility in water, may also explain why transparency for crypsis is common in aquatic animals but is a much less common defensive solution in terrestrial animals.^3,4 The use of transparency for crypsis from prey in combination with animal mimicry is found in some transparent pelagic siphonophores that perform aggressive mimicry of copepods or fish larva in order to lure prey that does not fear them and approaches a deadly predator because most of their body is transparent.¹

Defense from herbivory by plants via transparency for crypsis has never been proposed, to the best of my knowledge. The reason for this is simple: plants, being photosynthetic, cannot be highly transparent in general.⁵ Moreover, the fact that plant cells have cell walls made of various polymers^6,7 further reduces the ability of plants to be highly transparent. In spite of these inherent limitations, many succulent plant species of hot arid zones have partially transparent “windows” to allow below-ground photosynthesis as defense from both herbivores and from harsh environmental conditions, or have such “windows” in thick, aerial organs.^5,8-10 Recently, Lev-Yadun¹¹ proposed that similarly to the succulent leaves of window-plants, in many unripe fleshy fruits there are partly transparent whitish spots that among their several proposed defensive functions serve as windows that enable light to penetrate deeper into the photosynthetic layers in the developing fruit, this being a solution to overcome the limitations of light harvest because of the high volume-to-surface ratio of developing fleshy fruits.

One of the proposed functions of fruits being green when immature is to add to the photosynthetic pool.^12,13 The contribution of the photosynthesis of the immature green fruit of non-tropical trees ranges from 2.3% in Quercus macrocarpa to 64.5% in Acer platanoides, but the common values range between ca. 10–35%.¹⁴ Janzen¹² proposed that for tropical species this value might be even higher than 64.5%. Thus, in many cases, fruit photosynthesis contributes considerably to fruit development and maintenance not only by net CO₂ fixation, but probably also by refixation of CO₂ from mitochondrial respiration.^15,16

During my 20 y of field work with Eastern Mediterranean wild legumes, it was obvious that the young pods of many of them are temporarily partially transparent.

Results and Discussion

With back illumination, it is obvious that the young pods of various annual Mediterranean legume species belonging to the genera Lathyrus, Pisum and Vicia are partly transparent. Of the genus Lathyrus, the species L. ochrus and several other un-identified Lathyrus species have transparent young pods. In all 3 wild Pisum species of Israel, P. elatius, P. fulvum and P. humile, the young pods are transparent. The young pods of several unidentified Vicia species are transparent. With their elongated shape and showing their row of dark developing seeds that are conspicuous at that transparent stage when back-illuminated, they look like caterpillars (Fig. 1), very different from their classic pod look when they are not transparent (Fig. 2). I propose that being partly transparent probably simultaneously serves 2 functions: (1) acting as defensive caterpillar mimicry to reduce their consumption by various herbivores, and (2) allowing better photosynthesis in the rapidly growing seeds and pods.

Figure 1.

(1) A pair of back-illuminated transparent pods of Lathyrus ochrus that look like 2 caterpillars; (2) The same pair of pods of Lathyrus ochrus with frontal illumination; (3) Mature pods of Lathyrus ochrus with dark spots that make them look like aposematic caterpillars.

Figure 2.

The same pair of pods of Lathyrus ochrus with frontal illumination.

Annuals and perennial herbaceous Near-Eastern plants differ a lot from woody species in their allocation for defense. When defense by sharp organs (spines, thorns, prickles) was compared in the about 300 wild spiny species that belong to the flora of Israel, annuals and perennial herbs mostly defended their reproductive organs (95.7% and 83.0% respectively), dwarf-shrubs defended mostly their leaves (54.2%), and shrubs and trees mostly their branches (89.7% and 76.2% respectively). Trees in the flora of Israel do not defend their reproductive organs by associated sharp appendages.¹⁷ Ronel and Lev-Yadun¹⁷ proposed that there seems to be a simple evolutionary reason for these dramatic differences in allocation for defense and that the level of importance of seeds in survival selected the level of their defense. Annuals have no other means of genotype continuation, which is the reason for the fact that practically all spiny annual species defend their reproductive structures with spines or prickles. Perennial herbs may reproduce more than once, so the selection pressure on the defense of their reproductive structures seems to be somewhat lower. In woody plants that reproduce repeatedly (iteroparous), and where the reproductive organs of the larger plants, especially trees, may be out of reach of most grazers, less is invested in physical defense of their reproductive organs. For the annual legume species discussed here, any strengthening of the defense on their precious seeds (produced only once in their life) has a significant contribution to the survival of their genotype. Since being partly transparent also goes hand in hand with improved photosynthesis, the selection for partly transparent young pods seems to be twofold.

Letting light pass through several layers of plant tissues performing photosynthesis is a common adaptation in plants at the cellular, organ and whole plant level and this can be achieved by various mechanisms. For instance, Horn¹⁸ demonstrated that lobed leaves in dense temperate forests allow the illumination of lower leaf layers, allowing better overall tree photosynthesis. A well-known case of translucent leaves in order to improve photosynthesis, to allow warming of the tissues and even to improve reproduction is that of the glasshouse plants of several Rheum species of the Himalayas.^19-22 While improving their survival and sexual reproduction by being translucent, these glasshouse plants decrease the danger of UV-B radiation damage by expressing high levels of flavonoids that absorb it.^21,22 Improving photosynthesis also seems to operate when the fast-growing young and partly transparent pods discussed here can perform photosynthesis in both external and internal layers.

Caterpillar mimicry as defense from herbivory was proposed to exist in several plant taxa. Rothschild²³ proposed that modified stipules of Passiflora, which resemble horned caterpillars, defend these plants from insect attacks because they are considered by insects to be occupied. Lev-Yadun and Inbar²⁴ proposed that the pods of various Near-Eastern wild legume species mimic toxic aposematic caterpillars and by this defend them from herbivores. A detailed analysis of defensive pod and seed coloration in the 3 Mediterranean Pisum species showed that many individuals of 2 of them (Pisum elatius and P. humile) visually mimic aposematic caterpillars.²⁵ Interestingly, aposematic caterpillar mimicry is also performed by nestlings of the Amazonian birds Laniocera hypopyrra and Laniisoma elegans in order to reduce predation.^26,27 Caterpillar mimicry as defense from herbivory is part of a larger phenomenon of visual, e.g.,^24,25,28-32 and chemical³³ animal mimicry as defense from herbivory. It is interesting that while the young partly transparent pods of Lathyrus ochrus, Pisum elatius and P. humile seem to mimic caterpillars because they are partly transparent (e.g., Fig. 1), when these pods are more mature and no longer transparent, they mimic aposematic caterpillars by expressing a line of very conspicuous red spots (see^24,25; and Fig. 3). Since caterpillars do not interest various herbivores, when pods look like caterpillars because of back illumination as demonstrated here, it may serve as a type of masquerade sensu Lev-Yadun.³⁴ Contrary to the use of being transparent in animals for crypsis, in the case of young legume pods it is used for enhancing apparency and by this they visually mimic caterpillars for defense. Because flowering and the formation of pods in legumes is indeterminate,³⁵ in the beginning the plants will have only transparent pods that will look like caterpillars when back lighted. Some weeks later, the plants will simultaneously have pods that mimic aposematic caterpillars.^24,25 Toward the end of the season, only pods that mimic aposematic caterpillars are found on the plants. Since real aposematic caterpillars are found in the fields where these plants grow, e.g., Figure 10 in²⁴, such aposematic caterpillars seem to be the models for the mimicry. The lesser resemblance of the partly transparent pods to aposematic caterpillars seems to be compensated by the principle introduced by Miriam Rothschild³⁶ “aide mémoire mimicry,” according to which the herbivore is made to recall previous unpleasant experiences or risks and so there is no need for very good mimicry.

Figure 3.

Mature pods of Lathyrus ochrus with dark spots that make them look like aposematic caterpillars.

Plant-animal communication via transparent tissues was considered in 2 plant types: (1) For pitcher carnivorous plants,^37,38 although via 2 different mechanisms, demonstrating that illumination through transparent plant tissues can be used in more than one way. Moran et al.³⁷ found that in the pitcher plant species Nepenthes aristolochioides, the light coming through the translucent pitcher windows causes a visual illusion of false exits, helping to keep the prey inside the trap. However, Schaefer and Ruxton³⁸ found that the windows in the species Sarracenia minor do not serve as false exits but rather function in long-range visual attraction of prey. (2) “Windows in traps aimed for pollination that cause pollinating trapped insects to stay longer within the trap.^39,40 There is therefore no theoretical reason to dismiss the possibility that partly transparent young legume pods may visually defend themselves by mimicking caterpillars in order to deter herbivores, possibly by using their perceptual exploitation sensu Schaefer and Ruxton⁴¹ concerning fear of various animals. The animal mimicry by the partly transparent young legume pods shown here is also a kind of aposematism for herbivores that do not like to consume caterpillars; in addition, it may give the impression that the plant is already occupied to insects that search for unoccupied plants to lay their eggs on, or else it can serve as a type of masquerade sensu Lev-Yadun³⁴, by looking like a uninteresting food item to herbivores searching for pods. At the same time, looking like a caterpillar may attract predaceous birds and invertebrates (see⁴²) and they may attack invertebrate herbivores that have already occupied these plants.

Conclusions and Further Research

1. Being partly transparent may be used by young legume pods of several species and genera to establish a visual illusion that the pods are caterpillars. This may decrease their consumption by large mammalian herbivores, and in turn may attract predaceous birds or arthropods to the plants, which might hunt real herbivorous insects infesting them. This may also cause butterflies to refrain from laying eggs, as occurs in Passiflora plants that mimic butterfly eggs.²⁸

2. Being transparent may simultaneously allow fast-growing young legume pods to perform higher levels of photosynthesis.

3. It seems that while in animals being transparent serves both defense and attack via crypsis, in plants it serves photosynthesis, heating and defensive mimicry/aposematism and masquerade.

4. Of the thousands of legume species worldwide there are probably many that express it but were not described. The possibility that it may also be expressed in various other taxa should also be considered and studied. Such a database is essential for evaluating the physiological, ecological and evolutionary aspects of this phenomenon.

5. Experiments to examine if this defensive hypothesis operates under controlled conditions as well as in the wild are certainly needed.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.