Object-based learning is an approach that aims to foster observational skills and sensory awareness. Paradoxical plant objects that do not lend themselves to all-too-easy explanations and interpretations can be used to practice the search for ecological explanations and the formation of evolutionary hypotheses. They can be the basis of particularly fruitful and rewarding learning experiences. Gleditsia triacanthos, the honey locust, is a commonly planted ornamental tree. It exhibits striking structures of defense against – and fruit that point to a mutualism with – large animals. These structures, possibly developed in coevolution with Pleistocene faunas, invite a discussion of the complex, neither fully antagonistic nor fully mutualistic, relationships between plants and animals.
Ecological Thinking in Plant Object-Based Learning
Object-based learning is a powerful learner-centered and inquiry-based method to spark students' curiosity and inquisitiveness and to foster skills of observation, interpretation, and critical analysis (Corbishley, 2015; Kador et al., 2017). Students across many disciplines, including biology, have characterized object-based learning as more efficient than traditional lectures. Learners described object-based work as, in general, more enjoyable, inspiring, and engaging than other forms of learning (Hannan et al., 2013).
In biology, and especially in the study of plants, it is valuable to handle living objects and to establish links between form and function from firsthand observations, as done in object-based learning with artifacts (Corbishley, 2015). Encounters with plants that can be touched and smelled (and even heard – see below) and that have an aesthetic appeal also help train sensory awareness and observation skills and offer an “immersive learning experience” (Andrews, 1977; Kador et al., 2017). A plant's body is the physical manifestation of adaptations to myriad individual and interacting environmental factors. It shows structures that fend off, buffer, or modify environmental impacts. Plants, therefore, provide a rich repertoire of living illustrative examples and study objects to exercise biological systems-thinking habits.
For teaching purposes, it appears fruitful to introduce learners not only to straightforward and obvious models. Often it is the more challenging biological objects – in which the function of a certain structure is not instantly obvious and which at first may seem nonsensical or even contradictory – that trigger creative, sometimes speculative thinking processes. In the example outlined here, a plant with seemingly nonsensical features is put at the center of an object-based learning exercise that aims to improve understanding of evolutionary processes and timescales and overall “ecosystems thinking.” To make use of the motivating effect of novelty, a plant was chosen that was likely to be new to most students. Trees offer certain advantages as study objects: important structures are often sufficiently large to be easily seen, touched, and smelled, and an entire group can study one tree at the same time. Trees also attract interest through their multiple uses and, often, their cultural significance.
A Large-Thorned & Large-Fruited Tree
Gleditsia triacanthos (Fabaceae, subfamily Caesalpinioideae) is a deciduous leguminous tree native to eastern and central North America. Its distribution reaches from the Gulf coast along the lower Mississippi Valley as far as southern Canada. It is hardy to USDA Zone 4 or 5 and has been introduced to many parts of the world. It grows to a height of up to 45 m (Lance, 2004, p. 154) and an age of about 125 years (USDAFS, 1990, p. 358), and it may resprout from the rootstock. Its leaves turn a brilliant autumn yellow (Figure 1D). In bloom, it bears tassels of greenish-yellow to cream-colored, fragrant flower catkins. Sometimes flowers emerge directly on the trunk, rather than from younger shoots (Figure 1A). The bark is grayish-brown and appears rather smooth, yet is somewhat sandpapery to the touch. It tears laterally, in long, narrow plates forming around the trunk in several vertical fissures, furrows, and slab-like ridges with projecting, outcurving edges (Fergus, 2002, p. 184; Figure 1A, B).
The fruit is a spectacular sight: the flat, maroon pod reaches up to 45 cm in length (Allen & Allen, 1981, p. 299) and warps, when ripe, into an almost helical shape (Figure 1C, D). When the pod has dried, the seeds come loose inside it, turning it into a natural rattle. This botanical sound effect has been used in teaching young children (Moomaw, 2013, p. 107), but it certainly can catch adults' attention too. The limitations of dispersal without a mobile agent are evident from pods piling up near the trunk in urban spaces. Names like “honey locust,” “sweet locust,” and “honey shuck” apparently refer to the fruit pulp's sweetish taste. The pulp can contain up to 14% sugars (Allen & Allen, 1981, p. 299) and was used by Native American peoples as a basis for fermentation and brewing of a beer-like beverage (Austin, 2004, p. 324). Conveniently for teaching purposes, many of the pods remain on the tree through winter and into spring. Unless the site is cleaned regularly, some that have dropped late can still be found on the ground when the next season's flowers emerge (Figure 1C).
Apart from the pods, the tree's most striking feature is certainly its enormous thorns (Figure 1A, B). They normally measure, in a typical “wild-type” specimen, between 10 and 20 cm in length but may reach a staggering 40 cm (Lance, 2004, p. 154). Not surprisingly, the tree is blamed for flat tires (Logsdon, 2012, p. 111), human injuries, and even casualties (Walker, 1917). There is also the story – probably purely fictional – of alleged gangster David McCanles forcing victims of his displeasure to climb up a honey locust stem as a cruel and unusual punishment (Connelley, 1928). Another perfidious, though less ostentatious and probably rather ineffective, method to inflict harm on others by means of Gleditsia thorns is reported from the Deep South, where the thorns were apparently used for voodoo ceremonies (Brown & Hand, 1977, p. 103).
The honey locust, however, has several other, more benign uses. Its flowers are a nectar source for honeybees, and the stem provides a durable timber for furniture making. It is also planted for shade and shelterbelts and has proven a valuable urban street tree for its tolerance of drought, compacted soil, and pollutants (Gilman, 1997, p. 288). A popular choice is the “unarmed” G. triacanthos var. inermis and its cultivars “Shademaster” and “Sunburst,” the latter being a “golden” selection with yellowish foliage, and both being not only thornless but also mostly podless (Stoecklein, 2001, pp. 7, 15). These are forms that students may frequently see in urban spaces, but unfortunately they lack the very features at the center of the learning activity described here.
Both large fruits and large thorns are believed to be adaptations to the former presence of large herbivores, namely of the late Pleistocene. The species is therefore thought to be shaped by past evolutionary forces and fit for a biological environment that no longer exists (Barlow, 2001, 2002; Bronaugh, 2010).
Several Old World Gleditsia species – such as Southeast Asian G. australis, or G. fera – are equipped with equally impressive thorns that may have protected them (until recently) against browsing and debarking by extant large herbivores. However, no literature was found as to whether any of these species is browsed upon, or avoided, or their fruit eaten and seed dispersed by Asian elephants.
Channeling the Mastodon
The exercise described here was carried out with students from senior high schools (grades 10, 11, and 12; ages 16–18), students of a school for mature students, and university students in teacher's training (M.Ed.) in biology and horticultural sciences, on a day visit at the International Garden Exhibition (IGA) Berlin in summer 2017.
The IGA Park harbors a particularly striking specimen of G. triacanthos. Students were guided to the tree without any comments. I initiated discussion with an open question like “What's going on here?” – asking only for observations, not background knowledge. Following Corbishley (2015), participants familiar with the object were asked not to reveal any details to the rest of the group. Only one student – who, prior to entering university, had completed vocational training as a landscape gardener – was aware of Gleditsia, but was not familiar with any botanical detail. Several students felt reminded of acacias and were told that the first botanical description of G. triacanthos indeed called the species Acacia americana (Austin, 2004, p. 323). One student remembered having played with such pods as a child and mentioned the rattling of the seeds.
Typically, students immediately interpreted the thorns as a defensive structure. To induce “facilitated interaction” (Kador et al., 2017) with the object, several guiding questions were asked, like “What can you imagine, when looking at this tree and its thorns, that this defense might work against?” Answers across groups summed up to a colorful pan-global bestiary including “raccoons,” “giraffes,” “moose,” “deer,” “roe deer,” “camels,” “birds,” “woodpeckers,” “bears,” “panda bears,” “squirrels,” “rabbits,” “koalas,” “monkeys,” and “dinosaurs.”
Given that the tree's North American origin had been mentioned, this revealed that general biogeographic knowledge was rather mixed. Several students suggested that the thorns were a defense against a climbing animal – until I argued that for smaller animals the large thorns may, in fact, be more like the rungs of a ladder. Thus, among the “climbing animals,” probably only raccoons or bear cubs might be deterred (though Garber  claims that “squirrels never climb these thorned trees”). However, mere climbing by those animals would not cause an evolutionary pressure strong enough to translate into the evolution of such structures.
To narrow the discussion to large herbivores, students were asked which animal might open its mouth wide enough that the thorns would deter a bite, and which animal might want to come so close to the tree trunk that the thorns might be an effective deterrent. Typically, I had to draw attention to the location of the thorns and ask which part of the plant these are protecting and what animals might harm bark and cambium, before students said “elephants.” In one case, though, a student suggested that the thorns might be useful for elephants to scratch their itchy back, which does not quite follow a line of evolutionary thinking. Once the discussion had taken a proboscidean turn, I first drew a comparison to the defense systems of plants like umbrella thorn acacia (Vachellia tortilis) of the African savannas that show similarly large thorns. But then I pointed out that there was a lamentable dearth of elephants in the wild in America, which may make such an adaptation appear rather pointless.
I reminded students that the emergence of a “useless” feature, such as a defense structure against elephants where there are none, would be incongruous with Darwinian evolutionary theory. Typically, at least one student per group eventually came up with “mammoth,” which (corrected to “mastodon”) was established in the discussion as a hypothesis that could not be rejected on the basis of students' observations and our current background knowledge in the group. If no student suggested that loss of this defense structure may only be a matter of time, I pointed to the fact that the megafaunal extinctions (and thus the loss of the “evolutionary pressure” for being thorned) in North America date back only a comparatively short time, equaling relatively few tree generations. I also informed them that thornless specimens indeed appear at times in the wild, from which the unarmed “inermis” form was selected – a thornless mutation that would surely struggle to form stem old enough to form fruit in the presence of browsing and debarking megaherbivores.
In evolutionary terms, the tracks left in the coevolved plant's morphology are still fresh and have not yet been blurred by a more recent evolutionary history. Similarly, in other regions of the world morphologies of plants have been interpreted as defense mechanisms against browsing by past faunas (e.g., New Zealand's moas or Madagascar's elephant birds; Bond & Silander, 2007; Dempewolf & Rieseberg, 2007).
The fruit was discussed as the second central element. Asked what it reminded them of, students typically referred to the fruits of other Fabaceae (beans, mange tout, pea pods, etc.), and there were a few “joke” answers such as “worms.” Pointing out the pods' large size and how they pile up at the foot of the stem, I asked how the seed might be dispersed. Pleistocene megafauna having already appeared in our discussion, the suggestion that this fruit might be eaten and the seed dispersed by an extinct large animal came forward readily. The conjecture that this trait was not lost yet because of the relatively recent extinction of the Pleistocene megafauna was easily established. Several other leguminous species of the New World are believed to have been dispersed by now-extinct large herbivores (Janzen & Martin, 1982). Also, the question of why the loss of the dispersal agent did not lead to extinction of the plant was answered easily with reference to the short time that has passed since.
A final question put the focus on what looks at first like a contradiction: the tree, on the one hand, attracts large herbivores; on the other hand, it defends itself against them. Suggestions included, among others, that the tree may show adaptations to different animals, that the fruit may be available only once fallen off the tree, and that the animal disperser may be forced to carefully angle with its trunk for the fruit dangling at the branches, avoiding the thorns and thus causing no damage to either the bark or its own skin.
In Gleditsia, the thorny adaptation may be understood as a mechanism that channels the movement of the mastodon attracted by the fruit, keeping the animal at bay while getting it to disperse the seed and not allowing it to destroy vital structures of the plant's body. The tree thus lures, restrains, and ushers the energetically browsing, branch-breaking and debarking animal on its way, directing the mastodon's energy into channels favorable to the preservation of its own species.
“Strange Trees All Over…”
Gleditsia triacanthos combines in its morphology – namely that of flowers, fruit, and armature – several unusual features that may help attract student interest and improve retention. Indeed, students showed a sound interest in the tree, and natural history and cultural dendrology facts and “stories” were well remembered in the group: one student referred to the species when encountering another specimen elsewhere (on an excursion weeks later) as “that tree of the mammoth,” while another dubbed it “the voodoo tree.” One student later reported he had now seen the tree in another part of town, upon which his classmate added that he was now often reencountering this and other “strange trees” covered in this class now “all the time, all over.”
The student interest I observed is noteworthy and can be considered a learning success in view of the waning of natural history from curricula (Cheesman & Key, 2007; Leather & Quicke, 2010) and the dwindling of plant knowledge in the Western world (Hershey, 1992; Wandersee & Schussler, 2001; Bebbington, 2005). Working with “storied” plants that provide unusual models for ecological and biological principles not only may offer a rich resource of illustrative case studies but also may help to bring natural history back into biological and environmental education.
This exercise is not predominantly about the acquisition of factual knowledge, but is more about exercising basic scientific reasoning in an ecology-and-evolution context based on easily observable morphologies. My students exhibited innovative thinking and engagement with the living object in the various explanations they brought forward. Once the potential role of a large herbivorous animal was touched upon, students were able to develop the ecological context.
The discussion of the ambiguous role of the animal, as “destructive” browser or “helpful” disperser, typically brought the groups to the point of considering that there was no simple answer and acknowledging the complexity of the interaction. In the grander picture of evolutionary biology, work with this living object was thus a first step toward challenging a habit of thought based on the “gladiatorial” view of Huxleyan Darwinism. In Gleditsia, the complexity and multidimensionality of the plant–animal relation becomes visible in striking structures that allow the interpretation that plants do not simply defend themselves against a “damaging” herbivore, but redirect and channel the energy of the browsing animal from being destructive of its tissue to being a useful disperser of its seed. Discussing such cases as the “liaison dangereuse” of a thorned plant with a toothed herbivore can be expected to help students move away from all-too-simplified “friend” and “foe” imagery in ecology and evolution and toward complex systems thinking.