Hanging Gardens

           A translucent white butterfly patterned in black drifts above the foliage – ticking against the leaves beneath it – tasting them with its feet. Bold red chevrons on its wings come into view when it pauses to touch down. The animal is looking for the right plants to lay its eggs upon.
          Finally it settles motionless in a bunch of epiphytes strung across a branch a hundred feet above the jungle floor. After a moment the butterfly inverts her abdomen and affixes a single egg beneath the margin of a leaf.
          She moves to another site a few feet away and touches down again. But there her entrance draws the attention of an aggressive brown ant. The soldier lifts its head, antennae wide apart, then jumps at the visitor. Broad wings flick into the air at the first brush with the assailant, and the butterfly is gone.
          Later in the afternoon a smaller, more retiring ant wanderers out of sight under the leaf. It discovers the egg stuck upside down, grips it in its mandibles, and works it back and forth. Finally it comes free, the ant drops it away into space, and walks on.
          These two different species of ants, the brown aggressor and the smaller worker, come from the same nest. They work as a team to protect this patch of green – it is their shared garden. If they succeed in their efforts, the plants there will ripen their purple fruit, and the ants will tear into it and harvest the seeds inside.
          The ants patrol the foliage day and night, but their challenge is greater after dark. Raiders come out of the blackness, announced by the slightest puff of breeze, or the brush of weightless whiskers. The night patrol then comes alive when one of the ants emits a burst of alarm pheromone into the air. All the other ants raise gaping mandibles and race blindly in every direction. But when their search patterns take them off of the fruits and down the stem for a moment, they feel the branch recoil beneath them as the weight is removed from its end. When they pass back up again they find only empty, moist pedestals remaining – bats have stolen the fruit they were guarding, along with all the seeds inside. Now the ants will have to go find those seeds and bring them back.
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          These are gardening ants. They live together underground, up in the trees, where it never floods. Their association forms the most successful social society in the seasonally flooded lowland tropical forest. They nest in the dirt in the root-balls of the epiphytic plants they cultivate high up in the branches – plants they grow from seed.
          The two species of arboreal ants that tend this garden work together on the same root-ball. The “small garden ant” protects the plants that sprout from those roots against insect herbivores. The “large garden ant” defends the garden against larger intruders, and collects seeds. Both of the ant species collect bits of bark and dead leaf, as well as animal droppings to fold in between the roots to fertilize the plants in their living nest. In so doing, they create the earth into which their plants send the roots that hold them fast to their trees.
          The two species live together, maintaining separate brood chambers beneath the same garden plot. The larger ants may occasionally bully the smaller ones – chasing them off of the best food sources – but the two never actually fight. Their mutualism is permanent. And the plants depend on both species of ants to secure their place in the sun – as the ants depend on those plants for the shelter they provide.
          The larger ants prize the live seeds of the epiphytic plants they cultivate. The living seed attracts them through its unique aroma. Even though they are hard and dry, these seeds emit a steady fragrance. The larger ants descend from the trees to spend their days scouring the forest floor, searching for that aroma – the most enticing scent they know.
          A handful of thousands of those seeds would smell faintly of sweet vanilla. The seeds are spread far and wide across the forest in the droppings of fruit bats. And even though they will have passed through the digestive system of a bat, the fragrance is still produced – enabling the ants to find them wherever they chanced to land.
          The ants carry the seeds one at a time back up the tall trunks then out along the branches to their garden, and then down through their tunnels into the dark. They place their harvest in the brood chambers next to their next generations – the helpless, white immature stages in the nursery. Perhaps the seed scent reminds them of their young, and they are following the same behavior they would in replacing a mislaid pupa or larva.
          There the seeds germinate. The seedlings send their white shoots straight up through the earth to break into the light; and they send out their roots in every direction through the soil. Those fibrous sinews will anchor the garden to the branches, and knit the fabric of the root-ball firm. And they also keep the soil there from growing too heavy with rain.
          The suspended sphere of earth and ants is drenched in the afternoon by thunder showers. The root-ball absorbs water and swells beyond twice its morning weight – bending its branch downward. The sodden soil between the roots threatens to liquefy and return to its natural level – to the forest floor below. But the roots within the earthen sphere soak up water like a sponge. They draw it up into the main stem and distribute it out to the scores of leaves above.
          The leaves are solar evaporators. The plant holds them up in the air where the sunshine and the breeze can draw the water off into the sky. The net effect is to take water that weighs down the aerial garden and spread it out to dry over the thin, flat layer of several square meters of leaf surface.
          It is their plants that allow these ants to live in an earthen nest high above tropical wet forest. Moisture never penetrates to the hive center – the residents there remain dry inside, even in torrential downpours that wash workers caught outside down out of the trees.
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          Still, the gardening ants are not rooted forever to a particular aerial plot of ground. They are ready to move their nests when times change. They follow the sun through the forest to maintain homes in the most productive parts of the realm – such as on the walls of foliage exposed to the light along the open corridors beside river-ways.
           The contours of the forest over which sunlight stimulates the most growth are along the walls of tree-fall gaps – beneath skylights torn in the canopy where old trees have fallen, leaving the light to cascade down through the breach. In such gaps, a guild of early-maturing vines and understory trees is adapted to seize the advantage where bonanzas of brightness bloom.
          Sessile sap-sucking insects are drawn to the profusion of new growth in tree-fall gaps, and the gardening ants in turn are attracted to those sap-tappers. The ants move into the area to farm honeydew produced by scale insects and aphids that colonize the fastest growing shoot tips – and when they come, those ants bring their garden with them.
          The ants notice the diminishing sunlight at their established nests when the sessile insects emigrate. That departure is complete when the light gaps close over and total shade returns the forest to its default climax state. When the local plant growth slows, the ant colonies split. Half of their members march away, guided by scouts that have found more insects to shepherd – somewhere off through the jungle where the light is brighter and the new growth vigorous.
          Ants arriving at new sun-sites find temporary bivouac among the creepers and moss, and then they set about planting the seeds of their favored epiphytic plants. Their hanging gardens will grow over the years along with the other plants that eventually come to fill the hole in the canopy, and the migratory cycle continues.
          The sedentary sucking insects grow as quickly as the shoots they colonize. The sap they tap is high in nitrogenous nutrients, which the insects need to maintain their rapid reproduction rate. They absorb all the nitrogen they can get from the sweet sap; in the process, they imbibe more sugar than they need. Their stationary life does not demand much carbohydrate to provide them energy. They excrete the excess in droplets of honeydew.
          Sweeter than nectar, the ants are quick to harvest this. They divide their labor. The smaller ants patronize young aphid colonies, where the insects – and their offerings of honeydew – are smaller. When the colony of sessile insects expands, the larger ants move in.
          Their high energy diet enables the gardening ants to pursue a high energy lifestyle. They are alert and aggressive – they defend their trails, and their sources of honeydew against other ants – which are scarce where the gardening ants are most active.
          A monkey inspecting the hanging garden will find his skin crawling; the ants rip exposed skin with their mandibles and spray formic acid over the wound. They lift up the scales of reptiles that tarry too long in their domain, and insert their stingers underneath. Frugivorous grazers usually choose to pass up the fruits that adorn these gardens hanging in the sunshine. Leaf-eating lizards likewise soon leave.
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          Now another small dusky butterfly drifts through shafts of sun above the foliage – looking to lay her eggs. She is drawn to the tip of a shoot colonized by scale insects, under the guard of a patrol of gardening ants. The butterfly comes to a hover just above the colony; she bends her antennae down and probes the backs of the two closest ants. The sentries sense the faint sensation above them – the puff of a sudden breeze at their back, the brush of weightless feelers.
          They respond by emitting alarm pheromone; all the other ants lift gaping mandibles into the air and race in every direction. But when their search patterns take them off of one part of the colony for a moment, the butterfly descends – and in only seconds she places an egg on the stem among the sessile scales. Then she lifts off again just before the ants pass back.
          The ants won’t notice this alien presence in their flock – it is cloaked in pheromone-mimetic camouflage scent. By this subterfuge, they will also accept the tiny larva that emerges and grows into a caterpillar that exudes sweet offertory droplets just as do the scales. But this larval butterfly is no herbivore – it is a predator that prospers by eating the insects the ants shepherd; it is a parasite on the efforts of the ants – surviving and growing as a result of the work they expend to protect the residents of this shoot.
          The success of the gardening ants has created resources that are exploited by a menagerie of parasites and predators. Some of these interlopers use their chemical mimicry to avoid notice in the hanging gardens. Others prey on the ants directly.
          The ants are unable to defend their nests from swarms of army ants that file up the branches in endless columns. The invaders specialize in attacking arboreal social insects. The army kills the gardening ants below ground in their tunnels, and carries off the broods. The remaining garden ant workers stand aside in the foliage, and repopulate their homes when the invaders move on.
           Other plants may take advantage of the hanging gardens as well. Some anthuriums and bromiliads that get a foot-hold in the garden may grow to out-compete the principle epiphytes. They can fill the rootball with thick roots, and displace the ants from their own space.
           But when the gardens prosper, the entire epiphytic overstory benefits from the work of the gardening ants. The air plants avail themselves of the soil hauled up into the trees bit by bit, and stabilized in ant gardens. Fields of airborne flowers bloom in profusion high above the less productive, deeply shaded forest floor. Ant gardens abandoned to the shade are eventually populated by other arboreal arthropods, and overgrown by shade-tolerant orchids, lianas, figs and ferns – the emblematic decor of the aerial scaffolds in the tropics.
          Nonetheless, among all the airborne growth, the particular plants cultured by the gardening ants make up more than half of the total epiphytic biomass in areas where their ants are active. The ants continually find places to cache the few seeds that will grow new gardens for them, to replace the old.
          The two species of ants, and the select few species of hanging plants they cultivate, should all be able to survive and prosper independently – each on its own. Advantageous trade-offs that would commit them to a symbiotic life style are not obvious. But the gardening ants and their chosen plants are almost never found growing apart and alone. The success of their joint effort is reflected in their populations. Where their gardens flourish, the aggressive gardeners are the most prevalent animals in the forest – as anyone who chances to disturb their plants or their trails will soon discover.
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           In North American temperate forests, we see a scaled down version of the tropical gardening ant mutualism in the Trillium. This plant spikes out of shaded ground and unfurls a platter of three flat leaves a foot above the soil. Trilia produce a white bud at the central apex of their leaves. The bud may fade to pink with age.
           These trefoil plants are dispersed through their range by ants that inhabit the humid coolness under the trees at the bottoms of north-facing canyons. They climb the stems in search of the hard black seeds, which are crowned with a cap made of the ant’s favorite food. The ants take the seeds back to their queens, eat away the tasty crown, and dispose of the seed in the bottom of the nest.
           Trillium seeds lay dormant for many years. They are “double dormant” – they pass two winters before germinating. Then they send down one slender root but send up no leaf the year they first germinate. They finally send up a fine, slender primary leaf that sustains the enlargement of their underground roots. Each fall the above ground parts die off, sending their nutrients back underground. Each spring, they send up a larger shoot, until finally they send up the three-fold symmetrical leaves that will host the central flower. A decade of growth may have passed before that.
           From a site above an abandoned ant nest, the Trillium will produce about fifteen seeds. Their surviving percentage will be small – deer are fond of trillium. But the few that do survive stand as reminders of the more extensive ant-plant mutualisms that flourish beyond the horizon, in forests far away to the south in the tropics.

Hanging Gardens notes. Gardening ants are found in the New World tropics (Vantaux et al, 2007). The large garden ant Camponothus femoratus and the small garden ant Crematogaster levoir (aka C. limata parabiotica) maintain separate brood chambers in their communal rootballs in the tropical lowlands. They share foraging trails, the two species reminiscent of the large and small leaf-cutter ants marching in files through the upland forest. The gardeners feed on honeydew from sap sucking insects, and on the extra-floral nectaries and pearl bodies produced by gap-filling trees (Davidson, 1988). Leaves growing from the gardens suck up moisture from the rootball and evaporate it off into the breeze at a rate that may average 10 micrograms of water per square centimeter of leaf surface area per second. For a plant supporting a hundred leaves, each of which has a surface area of a hundred square centimeters, this amounts to the removal of ten ounces of water per hour from the earth around its roots. In the process, the plant absorbs carbon dioxide into its leaves from the air, and moves dissolved nutrients up into its leaves from the base – driving its growth. It also prevents the accumulation of sodden weight in its rootball (Yu, 1994). The earthen tangle maintains a consistency of cardboard, and the ants in the brood chambers within stay dry. Peperomia is a common gardening ant-associated epiphytic plant, along with certain anthuriums; other gardening ants live in bromiliad rootballs (Cereghino et al, 2010); the garden usually contains several species of plants.
          Ant garden plant seed is attractive to gardening ants – perhaps mimicking the scent of the brood. Some of those seeds are toxic to other non-gardening ants. Ant garden-associated epiphytes make up more than half of the aerial plants in ant garden habitat (Nieder et al, 2000). They are rarely found growing in the ab¬sence of the ants that tend them (but see Morales & Vesconcelos, 2009). One butterfly in the metalmark family lays its eggs only on colonies of sessile insects guarded by the gardening ants (DeVries & Penz, 2000). The Metalmarks as a family are often associated with ants.
          Trillium plants are found in the circum-arctic forests of North America and Asia.

Cereghino, R. et al (2010) Ants mediate the structure of phytotelm communities in an ant-garden bromiliad. Ecology 91,1549-56

Davidson, D. W. (1988) Ecological study of neotropical ant gardens. Ecology 69:1138-52

DeVries, P. J. & Penz, C. M. (2000) Entomophagy, behavior, and elongated thoracic legs in the myrmecophilous neotropical butterfly Alesa amesis (Riodinidae). Biotropica 32:712-21

Morales, S. C. & Vesconcelos, H. L. (2009) Long-term persistence of a neotropical ant-plant population in the absence of the obligate plant-ants. Ecology 90:2375-83

Neider, J. et al (2000) Spatial distribution of vascular epiphytes (including hemi-ephiphytes) in a lowland Amazonian rain forest (Surumoni crane plot) of southern Venezuela. Biotropica 32:385-96

Vantaux, A. et al (2007) Parasitism versus mutualism in the ant-garden parabiosis between Camponotes fermoratus and Crematogasater levoir. Insectes Sociaux 54:95-99

Yu, D. W. (1994) The structural role of epiphytes in ant gardens. Biotropica 26:222-6

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