Mini garden

Some arboreal ants grow useful plants

A Squamellaria major plant on macaranga, grown by ants

Gardening is an art – and there are ants that master this art. On the branches of trees they cultivate plants to live in or to strengthen their nests, as research teams of Guillaume Chomicki and Jonas Morales-Linares report.

Many ants and plants are partners in a mutualism: the plants provide the ants with a place to live or with nectar, and the ants deposit their droppings as fertilizer or protect the plants from herbivorous insects. Some tropical arboreal ants go a step further and cultivate the plants they live with. As these plants grow upon tree branches (they are epiphytes), it is more difficult for them to obtain nutrients than it is for plants that root in the soil, so the ant-plant mutualism is a good strategy. Many of the ant-grown plants are completely domesticated and would perish without the ants.

Seed collection

Philidris nagasau, native to Fiji, inhabits the hollow stems of Squamellaria species, bulb-shaped plants that grow on trees. The ants live nowhere else, and six Squamellaria species are always inhabited by these residents. The ant fertilizes the plants, as Guillaume Chomicki and colleagues had previously shown.

workers of Philidris nagasau inspect seedlings of SquamellariaNow, they discovered that the ant makes sure that plants are available by farming them. The researchers observed ant workers collecting exclusively the seeds of these six Squamellaria-species, and not those of any other species. They take them out of the unripe fruits, insert them in fissures and cracks in the bark of a tree and patrol the planting sites. Soon after, the seeds germinate and seedlings appear on the tree, and as soon as they form a cavity, a few ants will enter it, likely to leave their droppings. By doing so, they grow the plants they need to live in.

So, this ant-plant mutualism is more intimate than previously thought. The plants need the ant partner not only for nutrition, but also for seed dispersal.

Beautiful flowers

A different kind of plant nurseries can be found in Central and South America: conspicuous little gardens that hang from some trees. They are the overgrown carton nests of certain ant species. The ants collect seeds of epiphytes and insert them in the walls of their nest, where of the seeds germinate and grow up. The plant roots strengthen the nest and take up water when it rains, so that the nests don’t disintegrate. In return, the ants fertilize the plants and protect them against herbivorous insects. Some plants are exclusively dispersed by the ants and only germinate in an ant nest.

Hanging garden of Azreca gnavaAzteca gnava from southern Mexico and Panama is such a gardening ant. His gardens are frequently found in plantations, as Jonas Morales-Linares and colleagues report, mostly on cocoa, mango, sapote and orange trees. The gardens contain twelve plants on average, typically of two or three different species. Two plant species that cannot live outside these gardens are the bromeliad Aechmea tillandsioides and the orchid Coryanthes picturata. Apparently, the gardening ants have a good taste, for these plants have beautiful flowers.

Three million years

The ant Camponotus femoratus of the Amazonian lowland forest plants similar gardens. Mutualism is obligate for the plant Peperomia macrostachya, that only lives in the nests of this ant. Elsa Youngsteadt and colleagues showed that Camponotus femoratus is the only ant species to collect the seeds of this plant. The ant takes them from the plant, from the soil or from the feces of birds and mammals that have eaten the fruits. Probably, the seeds emit volatiles that only only Camponotus femoratus appreciates. The ant inserts many Peperomia seeds in the walls of its nest. Each seed has only a small chance to germinate there, but the seeds that are not brought into the ant’s nests have no chance to sprout at all.

According to Chomicki, Philidris nagasau in Fiji descends from ancestors that, just like their American colleagues, made carton nests in trees and planted seeds in the wall. But at some time, Philidris nagasau stopped making nests and planted the seeds in the bark instead; at roughly the same time Squamellaria species developed the hollow, bulbous stems that can house the ants. So, ant and plants co-evolved; their co-evolution started about three million years ago.

Willy van Strien

Large: a Squamellaria major plant, grown by ants on macaranga. © Guillaume Chomicki
Small 1: workers of Philidris nagasau inspecting seedlings. © Guillaume Chomicki
Small 2: hanging garden of Azteca gnava. © Jonas Morales-Linares

Chomicki, G. & S.S. Renner, 2016. Obligate plant farming by a specialized ant. Nature Plants 2: 16181. Doi: 10.1038/nplants.2016.181
Chomicki, G., Y.M. Staedler, J. Schönenberger & S.S. Renner, 2016. Partner choice through concealed floral sugar rewards evolved with the specialization of ant-plant mutualisms. New Phytologist, online May 9. Doi: 10.1111/nph.13990
Morales-Linares, J., J.G. García-Franco, A. Flores-Palacios, J.E. Valenzuela-González, M. Mata-Rosas & C. Díaz-Castelazo, 2016. Vascular epiphytes and host trees of ant-gardens in an anthropic landscape in southeastern Mexico. The Science of Nature 103: 96. Doi: 10.1007/s00114-016-1421-9
Youngsteadt, E., J. Alvarez Baca, J. Osborne & C. Schal, 2009. Species-specific seed dispersal in an obligate ant-plant mutualism. PLoS ONE 4: e4335. Doi: 10.1371/journal.pone.0004335

Too busy to care

A successful daddy longlegs is a bad dad

Serracutisoma proximum, two males fighting

In Serracutisoma proximum, a species belonging to the harvestmen, the mother guards her eggs until the young have hatched. A male can do the job as well, but he does so only when he has nothing better to do, as Louise Alissa and colleagues report.

Many species of harvestmen (or daddy longlegs) exhibit a form of parental care: they protect their eggs. This is also true for Serracutisoma proximum, a species that inhabits the Atlantic forests of Brazil.

At the start of the breeding season, males try to establish a territory. They perform ritualised fights for the possession of an attractive area: two males face each other, extend their strongly elongated second pair of legs and try to hit each other. If one of them gives up and leaves, the other is the owner of the territory.


This male then has to wait for a female to arrive. When this happens, he copulates with her and she lays her eggs after fertilising them internally with his sperm. For a month, she will then stay and guard the clutch. That improves the survival, as conspecifics and other predators will eat many of the eggs when unattended.

Serracutisoma proximum, male tending eggsOn rare occasions, a female deserts or dies. The owner of the territory can take her place and tend the eggs, but there may be more important things for him to do, Louise Alissa and colleagues realised. A second female may visit the territory, and maybe still another. Around a successful male, a harem forms. The territorial male will copulate which each newcomer female as to increase his number of offspring, and he cannot tend a clutch and court newcomer females at the same time.

And that’s not all. There is also a need to guard a female after copulation until she has laid her eggs because of sneaker males, a second type of males (minors) that exist in addition to the territorial males (majors). Sneakers don’t fight for territories (and their second pair of legs is not strongly elongated), but they invade the territories of other males, especially when there are several females present, and try to furtively copulate with one of them to fertilise some of her eggs. The females lay almost all their eggs on the first day after mating with the territorial male, so continuous vigilance during this period is most important. Thereafter, sneaker males still have a chance to sire some young because a few late eggs appear during the next two weeks.

Deserted eggs

Because a successful male must pay attention to newcomer females, he will have less time to guard deserted eggs than a less successful male, the researchers hypothesized. To prove, they removed a egg-tending female from a number of territories that they had been observing for ten days. They then inspected these territories regularly to see whether the owners cared for the orphaned eggs.

As expected, males with only one or two females in their territory guarded the deserted eggs pretty well, while more successful males typically spent less time with the clutch. Males can do only one thing at a time.

Willy van Strien

Photos: ©Bruno A. Buzatto.
Large: two territorial males fighting
Small: caring male

Alissa, L.M., D.G. Muniz & G. Machado, 2016. Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem-defending arachnid. Journal of Evolutionary Biology, online November 7. Doi: 10.1111/jeb.12998
Munguía-Steyer, R., B.A. Buzatto & G. Machado, 2012. Male dimorphism of a neotropical arachnid: harem size, sneaker opportunities, and gonadal investment. Behavioral Ecology 23: 827-835. Doi:10.1093/beheco/ars037
Buzatto, B.A., G.S. Requena, R.S. Lourenço, R. Munguía-Steyer & G. Machado, 2011. Conditional male dimorphism and alternative reproductive tactics in a Neotropical arachnid (Opiliones). Evolutionary Ecology 25: 331-349. Doi: 10.1007/s10682-010-9431-0
Buzatto, B.A. & & G. Machado, 2008. Resource defense polygyny shifts to female defense polygyny over the course of the reproductive season of a Neotropical harvestman. Behavioral Ecology and Sociobiology 63: 85-94. Doi: 10.1007/s00265-008-0638-9

Gravid frog

Mother transfers nutrients to the young in her dorsal pouch

female Gastrotheca excubitor has a brood pouch on her back

Young of the live-bearing frog Gastrotheca excubitor are well taken care of. The mother carries them in a brood pouch on her back and provides them with nutrients, as Robin Warne and Alessandro Catenazzi show.

In many frog species, females lay their eggs in the water and then leave them alone. After hatching, the tadpoles take care of themselves. Parents of other species look after their young to some extent: the father or mother sees to it that the eggs, which are deposited above a water body, remain moist, or the parents carry the tadpoles to a suitable pool to grow up and bring them some food.

Brood pouch

A few species go even further: parents retain the young in or on their body until they have developed into froglets. One of them is Gastrotheca excubitor, a terrestrial marsupial frog of Central and South America. A mother carries the young in a brood pouch on her back and she transfers nutrients to them, Robin Warne and Alessandro Catenazzi report.

A male clasps a female that is about to lay eggs (amplexus) and fertilizes them when they come out. He then leads them into her dorsal brood pouch, a skin fold with an entrance at the rear. It accommodates more than ten eggs.

During pregnancy the brood pouch is sealed, so the eggs and, later, the hatchlings cannot take up oxygen from their environment. Respiratory gas is exchanged with the mother, as was already known, through the numerous blood vessels in the brood pouch membrane which folds over each egg. The eggs absorb oxygen through the egg membrane and hatchlings breathe through their large external and well vascularised gills that have fused to a ‘bell’. All nutrients the embryo needs are contained in the yolk, the idea was, as they are in other frog species.


Larva of Gastrotheca excubitorBut Warne and Catenazzi hypothesized that a mother provides her young also with nutrients, using the extensive network of blood vessels. Because she retains them for a long period – until they have fully developed into froglets – the amount of yolk may be insufficient, they reasoned. And experiments showed that this is true. The researchers fed pregnant frogs with insects that were chemically labeled (with rare isotopes of carbon and nitrogen, 15N and 13C), and found that the amounts of isotopes increased in the embryos. In addition, the developing froglets gained weight. So, nutrients must be transferred from mother to young.

More species of live-bearing frogs exist. In some species, the males swallow fertilised eggs and brood them in their vocal sac. There are also species in which the females ingest the eggs, which develop in their stomachs, and species in which froglets develop in the oviducts. Transfer of nutrients, however, is rare.

Willy van Strien

Photos © Alessandro Catenazzi
Large: mother with one of her emerged young
Small: larva

Warne, R.W. & A. Catenazzi, 2016. Pouch brooding marsupial frogs transfer nutrients to developing embryos. Biology Letters 12: 20160673. Doi: 10.1098/rsbl.2016.0673
Wake, M.H., 2015. Fetal adaptations for viviparity in amphibians. Journal of Morphology 276: 941-960. Doi: 10.1002/jmor.20271

Who is the prey?

Assassin bug sneaks in the web to eat the deadly spider


Thanks to a stealthy hunting tactic, the giraffe assassin bug is able to prey on web building spiders. Fernando Soley unravelled how the bug manages to approach a spider unnoticed.

With their sticky webs and their venom, web building spiders are formidable predators of insects and other small animals. Webs and venom also make a powerful defence and it is nearly impossible for small animals to prey on spiders. Still, some critters feed on these predators, risking their lives.

One of the most remarkable spider eating species is the giraffe assassin bug, Stenolemus giraffa, an inhabitant of the northern, tropical part of Australia. It has a weird appearance, as a long ‘giraffe’s neck’ (pronotum) extends between the head with part of the thorax and the rest of the thorax with the thin abdomen. Antennae and front legs are placed at one end of the neck, middle legs and hind legs at the other end. The bug lives on rock escarpments and is often found associated with spider webs because it is araneophagic: it preys on web building spiders. After grasping one, it inserts the tip of its rostrum (piercing mouthparts) into the spider’s abdomen to feed on the contents. Feeding takes an hour or longer.


How is this delicate looking bug able to approach and attack a dangerous spider in her web? To find out, Fernando Soley observed the bugs under natural conditions and conducted experiments in the lab.

The giraffe bug spends nearly half his time on stalking resting spiders, as Soley noticed. If he perceives one, he first tries to access it without touching the web, for the spider will perceive any vibration of the threads. Hanging from the rock on middle and hind legs the enemy cautiously progresses. If he is close enough, he bends to his prey and stretches his forelegs to grab it. The long legs and giraffe neck facilitate this way of hunting.

But often, he cannot reach the spider without invading the web. Soley made artificial webs of spider’s silk and placed them in front of a laser vibrometer in order to measure the vibrations produced when a bug steps on a thread. It turned out that those vibrations are very soft and hardly detectable. Because of the long body and the long legs, the bug’s weight is distributed over a large surface area. Besides, it moves slowly, pausing after each step.


Great difficulties arise when the spider rests at the opposite side of the web. Then the assassin bug has to break some threads next to the spider with its forelegs to be able to capture it. He does so very carefully. To prevent the ends from snapping back after the break and alerting the spider, the bug holds on to the loose ends for a while, causes them to sag and then releases them carefully. After releasing the first loose end, he waits several seconds or even minutes before he releases the second one to space out the vibrations in time. In this way, Soley reports, the bug strongly attenuates the vibrations produced, making them often indistinguishable from background noise.

If a wind blows, things are easier, as vibrations are less conspicuous and the bug can move faster. So, it prefers to breaks threads in the presence of wind.

Long rest

In spite of this stealthy behaviour, there is a risk that the spider notices the steps of the giraffe assassin bug or the breaking of threads and either escapes or attacks. Occasionally, the hunting bug becomes prey himself. The success rate of his attacks is only 20 per cent, but if he succeeds, rewards for his patience and careful behaviour are high. After having overpowered and eaten a spider, the bug can rest for days, digesting this meal.

Willy van Strien
This is an update of an earlier version in Dutch

Photo: Giraffe assassin bug Stenolemus giraffa. © Fernando Soley

Soley, F.G., 2016. Fine-scale analysis of an assassin bug’s behaviour: predatory strategies to bypass the sensory systems of prey. Royal Society Open Science 3: 160573. Doi: 10.1098/rsos.160573
Soley, F.G. & P.W. Taylor, 2012. Araneophagic assassin bugs choose routes that minimize risk of detection by web-building spiders. Animal Behaviour 84: 315-321. Doi:10.1016/j.anbehav.2012.04.016
Soley, F.G., R.R. Jackson & P.W. Taylor, 2011. Biology of Stenolemus giraffa (Hemiptera: Reduviidae), a web invading, araneophagic assassin bug from Australia. New Zealand Journal of Zoology 38: 297-316. Doi: 10.1080/03014223.2011.604092

An uninvited guest

Frog breeds safely and undisturbed among leafcutter ants

Lithodytes lineatus breeds among leafcutter ants

Leafcutter ants ignore the frog Lithodytes lineatus when it breeds in their nests. They simply do not notice him, André Lima Barros and colleagues show, because the frog is chemically camouflaged.

Ants behave aggressively against intruders in their nests, but the South American Leptodactylid frog Lithodytes lineatus isn’t molested. In fact, he is at home in the huge colonies of leafcutter ants. Years ago, Andreas Schlüter reported that he had heard frog males calling from the interior of a leafcutter ant nest to attract females. Upon inspection of a nest, he found an adult frog within and numerous tadpoles swimming in a little pool. Obviously, the frogs breed in leafcutter nests.


It is clear why they willingly live there. Adult frogs, eggs and larvae are safe from predators, for the ants prevent these from entering the nest. Moreover, the nest has an agreeable humid microclimate.

But the question is why the ants, eager to evict all intruders from their nests, do tolerate these animals.

Now, André de Lima Barros and colleagues show that the frogs are chemically camouflaged. In their skin, they synthesize compounds which apparently imitate the odours with which the ants communicate. Since the ants rely on odour perception, the frogs go unnoticed: a good example of mimicry.

Not a burden

The researchers placed frogs of different species close to a nest entrance. When the experimental frog was a Lithodytes lineatus, the ants never attacked, but when it belonged to another species – either a species that is closely related to Lithodytes lineatus or a species that looks exactly the same as this frog – the ants became aggressive and bit the unwanted guest, that tried to escape quickly.

Next, the biologists prepared an extract from the skin of Lithodytes lineatus and coated a frog with it that normally would be chased away by the ants. Impregnated with skin extract of Lithodytes lineatus, the frog elicited no response.

So, Lithodytes lineatus can enter a leafcutter nest unharmed thanks to chemical camouflage. The uninvited guest is not a burden to the ants whatsoever, as he doesn’t touch the ants nor their brood. As he eats all sorts of other critters, such as assassin bugs and crickets, he may help the ants to keep the nest free of such enemies, in return for a safe place to breed.

Willy van Strien

Photo: Lithodytes lineatus, outside ant nest. Andrew Kay (via Flickr, Creative Commons CC BY-NC-SA 2.0)

De Lima Barros, A., J. L. López-Lozano & A. P. Lima, 2016. The frog Lithodytes lineatus (Anura: Leptodactylidae) uses chemical recognition to live in colonies of leaf-cutting ants of the genus Atta (Hymenoptera: Formicidae). Behavioral Ecology and Sociobiolology, October 20 online. Doi: 10.1007 / s00265-016-2223-y
Schlüter, A., P. & K. Löttker Mebert, 2009. Use of an active nest of the leaf cutter ant Atta cephalotes (Hymenoptera: Formicidae) as a breeding site of Lithodytes lineatus (Anura: Leptodactylidae). Herpetology Notes 2: 101-105.

Surprising and familiar

The pied butcherbird and the art of composing

pied butcherbird, male. V. Nunn

A clever composer is able to grip the audience with variations, but without presenting music that is a confusing chaos. The pied butcherbird masters that art too, as Eathan Janney and colleagues report.

A piece of music with more variety in it is more pleasing to listen to. But it should not be too surprising: the piece must remain recognizable as a unit. In order to maintain consistency, a composer will repeat parts of the music and take care that themes can be heard several times.

In this respect, the beautiful singing pied butcherbird can compete with a good composer, according to research done by Eathan Janney and colleagues.

The black and white bird, slightly smaller than a magpie, lives in Australia where it is the most accomplished song bird with a very complex song. The bird may sound like a flute, a cornet or organ; hence the name. Males can sing continuously for hours at night. Their song consists of hundreds of clear phrases which take about two and a half second. After each phrase they wait a few seconds before they proceed.


Janney wondered if they, just as composers, keep a balance between novelty and repetition. That would be important to prevent habituation in female listeners while at the same time the bird remains identifiable as an individual. He studied the nocturnal solo songs of 17 birds. He divided the phrases of each bird in types and investigated how often and in what order he sang each type. Also, he discerned motifs; a motif is a single tone or a group of a few tones (syllable) that often recurs. Several types of phrases may share a same motif. Finally, for each bird he investigated how he arranged his phrases and motifs. Was there any structure in the temporal patterning?

The singing of the birds is well organized, the analysis shows. Types of phrases and particularly motifs were regularly spaced in time. That regularity arises, as the researchers show, because a performing bird orders the different types of phrases in such a way, that each motif is heard at constant time intervals.

Large repertoire

The birds differ greatly in the amount of variation in their song. Some birds have more types of phrases and more different motifs in their repertoire than others. The more variety, the greater the risk that the song as a whole will be incoherent. But, as it turns out, the birds with the most different phrases and motifs organized their song more strictly. The larger the repertoire is, the stronger the temporal regularity with which the motifs are repeated. The birds seem to actively maintain the balance between variety and regularity – just like a good composer.

Willy van Strien

Photograph: Pied butcherbird male. Vicki Nunn (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

An accomplished performer can be heard on this video of the researchers
Hear another record of the song

Janney, E., H. Taylor, C. Scharff, D. Rothenberg, L.C. Parra & O. Tchernichovski, 2016. Temporal regularity increases with repertoire complexity in the Australian pied butcherbird’s song. Royal Society Open Science 3: 160357. Doi: 10.1098/rsos.160357

Fly trap

Parachute flower smells like a tasty bee in distress


Flowers of the African parachute plant are deceivers, as Annemarie Heiduk and colleagues show. The flowers mimic the smell of honeybees that are caught in the jaws of a spider. Their volatiles attract flies that feed on the fluids that such unhappy bees excrete. These flies pollinate the flowers.

Many plants have their flowers pollinated by insects. The insects take up pollen from one flower they visit and leave some of it on the pistil of the next flower, that can then grow seeds. And in return, most plants offer their pollinators nectar as a reward.

Clumps of pollen

But not all plants are honest plants. Some lure their pollinators with false promises of a reward.

A sophisticated deceptive plant is the African parachute plant Ceropegia sandersonii, a climbing herb from southern Africa, as Annemarie Heiduk and colleagues reveal.
Its pollinators are Desmometopa-flies. They visit the flowers and disperse the pollen, but not voluntarily. The flower is a trap where they go into. Downward pointing hairs on the flower wall make it impossible for them to get out. Clumps of pollen (pollinaria) within the flower dislodge and stick to their mouthparts.

Only the next day, when the flower withers, the flies are able to escape, packed with pollen. In the flower that they enter next, they will deposit the pollinaria unwittingly on the right place.

The question arises: how is it that the flies can be tricked time and again? Now, Heiduk answered that question: the flower smells like their food.


The flies, especially the females, need protein and they derive it from honeybees. They can’t overpower a honeybee by themselves, as they are much smaller. But when a spider has caught one, they come and feed on the fluids that leak from the dying bee. They find such a bee as they detect compounds that are released from its mandible glands and sting glands when it tries to defend itself by biting or stabbing. Also, they detect the pheromones that the bee releases to alert conspecifics.

Heiduk analysed the blend of volatiles dispersed by the flowers of the parachute plant, and found that many components are identical to the compounds that are released by bees in agony. This blend of volatiles is unique among flowering plants, and clearly adapted to lure the flies. Upon detection, they approach the flower, expecting to find a helpless bee. They find nothing of the kind, however, but are imprisoned for a time and meanwhile serve the plant. For free.

Willy van Strien

Photograph: Ceropegia sandersonii. Alzheimer1 (via Flickr. Creative Commons BY-NC-SA 2.0)

Nasty video: a honeybee is hold by a spider and licked by Desmometopa-flies

Heiduk, A., I. Brake, M. von Tschirnhaus, M. Göhl, A. Jürgens, S.D. Johnson, U. Meve & S. Dötterl, 2016. Ceropegia sandersonii mimics attacked honeybees to attract kleptoparasitic bees for pollination. Current Biology, online October 6. Doi: 10.1016/j.cub.2016.07.085