Cycad Pollinators

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When it comes to insect pollination, flowering plants get all of the attention. However, flowers aren't the only game in town. More and more we are beginning to appreciate the role insects play in the pollination of some gymnosperm lineages. For instance, did you know that many cycad species utilize insects as pollen vectors? The ways in which these charismatic gymnosperms entice insects is absolutely fascinating and well worth understanding in more detail.

Cycads or cycad-like plants were some of the earliest gymnosperm lineages to arise on this planet. They did so long before familiar insects like bees, wasps, and butterflies came onto the scene. It had long been assumed that, like a vast majority of extant gymnosperms, cycads relied on the wind to get pollen from male cones to female cones. Indeed, many species certainly utilize to wind to one degree or another. However, subsequent work on a few cycad genera revealed that wind might not cut it in most cases.

White-haired cycad ( Encephalartos friderici-guilielm i)

White-haired cycad (Encephalartos friderici-guilielmi)

It took placing living cycads into wind tunnels to obtain the first evidence that something strange might be going on with cycad pollination. The small gaps on the female cones were simply too tight for wind-blown pollen to make it to the ovules. Around the same time, researchers began noting the production of volatile odors and heat in cycad cones, providing further incentives for closer examination.

Subsequent research into cycad pollination has really started to pay off. By excluding insects from the cones, researchers have been able to demonstrate that insects are an essential factor in the pollination of many cycad species. What's more, often these relationships appear to be rather species specific.

Cycadophila yunnanensis ,  C. nigra , and other beetles on a cone of  Cycas  sp.

Cycadophila yunnanensis, C. nigra, and other beetles on a cone of Cycas sp.

By far, the bulk of cycad pollination services are being performed by beetles. This makes a lot of sense because, like cycads, beetles evolved long before bees or butterflies. Most of these belong to the superfamily Cucujoidea as well as the true weevils (Curculionidae). In some cases, beetles utilize cycad cones as places to mate and lay eggs. For instance, male and female cones of the South African cycad Encephalartos friderici-guilielmi were found to be quite attractive to at least two beetle genera. 

Beetles and their larvae were found on male cones only after they had opened and pollen was available. Researchers were even able to observe adult beetles emerging from pupae within the cones, suggesting that male cones of E. friderici-guilielmi function as brood sites. Adult beetles carrying pollen were seen leaving the male cones and visiting the female cones. The beetles would crawl all over the fuzzy outer surface of the female cones until they became receptive. At that point, the beetles wriggle inside and deposit pollen. Seed set was significantly lower when beetles were excluded.

Male cone of  Zamia furfuracea  with a mating (lek) assembly of  Rhopalotria mollis  weevils.

Male cone of Zamia furfuracea with a mating (lek) assembly of Rhopalotria mollis weevils.

For the Mexican cycad Zamia furfuracea, weevils also utilize cones as brood sites, however, the female cones go to great lengths to protect themselves from failed reproductive efforts. The adult weevils are attracted to male cones by volatile odors where they pick up pollen. The female cones are thought to also emit similar odors, however, larvae are not able to develop within the female cones. Researchers attribute this to higher levels of toxins found in female cone tissues. This kills off the beetle larvae before they can do too much damage with their feeding. This way, the cycad gets pollinated and potentially harmful herbivores are eliminated. 

Beetles also share the cycad pollination spotlight with another surprising group of insects - thrips. Thrips belong to an ancient order of insects whose origin dates back to the Permian, some 298 million years ago. Because they are plant feeders, thrips are often considered pests. However, for Australian cycads in the genus Macrozamia, they are important pollinators.

Macrozamia macleayi  female cone.

Macrozamia macleayi female cone.

Thrip pollination was studied in detail in at least two Macrozamia species, M. lucida and M. macleayi. It was noted that the male cones of these species are thermogenic, reaching peak temperatures of around   104 °F (40 °C). They also produce volatile compounds like monoterpenes as well as lots of CO2 and water vapor during this time. This spike in male cone activity also coincides with a mass exodus of thrips living within the cones.

Thrips ( Cycadothrips chadwicki ) leaving a thermogenic pollen cone of  Macrozamia lucida.

Thrips (Cycadothrips chadwicki) leaving a thermogenic pollen cone of Macrozamia lucida.

Thrips apparently enjoy cool, dry, and dark places to feed and breed. That is why they love male Macrozamia cones. However, if the thrips were to remain in the male cones only, pollination wouldn't occur. This is where all of that male cone metabolic activity comes in handy. Researchers found that the combination of rising heat and humidity, and the production of monoterpenes aggravated thrips living within the male cones, causing them to leave the cones in search of another home.

Inevitably many of these pollen-covered thrips find themselves on female Macrozamia cones. They crawl inside and find things much more to their liking. It turns out that female Macrozamia cones do not produce heat or volatile compounds. In this way, Macrozamia are insuring pollen transfer between male and female plants.

Thrips up close.

Thrips up close.

Pollination in cycads is a fascinating subject. It is a reminder that flowering plants aren't the only game in town and that insects have been providing such services for eons. Additionally, with cycads facing extinction threats on a global scale, understanding pollination is vital to preserving them into the future. Without reproduction, species will inevitably fail. Many cycads have yet to have their pollinators identified. Some cycad pollinators may even be extinct. Without boots on the ground, we may never know the full story. In truth, we have only begun to scratch the surface of cycads and their pollinators.

Photo Credits: [1] [2] [3] [4] [5] [6] [7]

Further Reading: [1] [2] [3] [4] [5] [6]

Growing Camouflage

A garden on the back of a weevil living a humid Chilean rainforest.

A garden on the back of a weevil living a humid Chilean rainforest.

Lots of us will be familiar with organisms like decorator crabs that utilize bits and pieces of their environment, especially living sea anemones, as a form of camouflage and protection. Examples of terrestrial insects attaching bits and pieces of lichens to their body are not unheard of either. However, there are at least two groups of arthropods that take their camouflage to a whole new level by actively growing miniature gardens on their bodies.

Little is known about these garden-growing arthropods. To date, these miniature gardens have only been reported on a few species of weevil in the genus Gymnopholus as well as a species of millipede called Psammodesmus bryophorus. Coined epizoic symbiosis, it is thought that these gardens serve as a form of protection by camouflaging the gardeners against the backdrop of their environment.

Bryophytes on a  Psammodesmus bryophorus  male.

Bryophytes on a Psammodesmus bryophorus male.

Indeed, both groups of arthropods frequent exposed areas. What is most remarkable about this relationship is that these plants were not placed on the carapace from elsewhere in the environment. Instead, they have been actively growing there from the beginning. Closer inspection of the cuticle of these arthropods reveals unique structural adaptations like pits and hairs that provide favorable microclimates for spores to germinate and grow.

The plant communities largely consist of mosses and liverworts. At least 5 different liverwort families are represented and at least one family of moss. Even more remarkable is the fact that even these small botanical communities are enough to support a miniature ecosystem of their own. Researchers have found numerous algae such as diatoms, lichens, and a variety of fungi growing amidst the mosses and liverworts. These in turn support small communities of mites. It appears that an entire unknown ecosystem lives on the backs of these mysterious arthropods.

FIGURE 39. Elytral base of Gymnopholus (Niphetoscapha) nitidus with exudates. FIGURES 40a–b. Gymnopholus (Niphetoscapha) inexspectatus sp. n., live specimen with incrustrations of algae and lichens; photographs M. Wild, Mokndoma.  [SOURCE]

FIGURE 39. Elytral base of Gymnopholus (Niphetoscapha) nitidus with exudates. FIGURES 40a–b. Gymnopholus (Niphetoscapha) inexspectatus sp. n., live specimen with incrustrations of algae and lichens; photographs M. Wild, Mokndoma. [SOURCE]

There is still much to be learned about this symbiotic relationship. Although camouflage is the leading hypothesis, no work has been done to actually investigate the benefits these arthropods receive from actively growing these miniature gardens on their backs. Mysteries still abound. For instance, in the case of the millipede, gardens are found more frequently on the backs of males than on the backs of females. Could it be that males spend more time searching their environment and thus benefit from the added camouflage? Only further research will tell.

Photo Credits: [1] [2] [3]

Further Reading: [1] [2] [3]

From Herbivore to Pollinator Thanks to a Parasitoid

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In the Atlantic forests of Brazil resides a small orchid known scientifically as Dichaea cogniauxiana. Like most plant species, this orchid experiences plenty of pressure from herbivores. It faces rather intense pressures from two species of weevil in the genus Montella. These weevils are new to science and have yet been given full species status. What's more, they don't appear to eat the leaves of D. cogniauxiana. Instead, female weevils lay eggs in the developing fruits and the larvae hatch out and consume the seeds within. In other words, they treat the fruits like a nursery chamber.

This is where this relationship gets interesting. You see, the weevils themselves appear to take matters into their own hands. Instead of waiting to find already pollinated orchids, an event that can be exceedingly rare in the dense Amazonian forests, these weevils go about pollinating the orchids themselves. Females have been observed picking up orchid pollinia and depositing the pollen onto the stigmas. In this way, they ensure that there will be developing fruits in which they can raise their young.

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Left unchecked, the weevil larvae readily consume all of the developing seeds within the pod, an unfortunate blow to the reproductive efforts of this tiny orchid. However, the situation changes when parasitoid wasps enter the mix. The wasps are also looking for a place to rear their young but the wasp larvae do not eat orchid seeds. Instead, the wasps must find juicy weevil larvae in which to lay their eggs. When the wasp larvae hatch out, they eat the weevil larvae from the inside out and this is where things get really interesting.

The wasp larvae develop at a much faster rate than do the weevil larvae. As such, they kill the weevil long before it has a chance to eat all of the orchid seeds. By doing so, the wasp has effectively rescued the orchids reproductive effort. Over a five year period, researchers based out of the University of Campinas found that orchid fruits in which wasp larvae have killed off the weevil larvae produced nearly as many seeds as uninfected fruits. As such, the parasitoid wasps have made effective pollinators out of otherwise destructive herbivorous weevils.

The fact that a third party (in this case a parasitic wasp) can change a herbivore into an effective pollinator is quite remarkable to say the least. It reminds us just how little we know about the intricate ways in which species interact and form communities. The authors note that even though pollination in this case represents selfing and thus reduced genetic diversity, it nonetheless increases the reproductive success of an orchid that naturally experiences low pollination rates to begin with. In the hyper diverse and competitive world of Brazilian rainforests, even self-pollination cab be a boost for this orchid.

Photo Credits: [1] [2]

Further Reading: [1]