'Tis the Season for Symbiosis

Science Sushi
By Christie Wilcox
Dec 21, 2015 4:16 PMNov 20, 2019 4:56 AM

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The whooping calls of howler monkeys were an effective alarm. I rolled up my mosquito net and hastily yanked on the pair of skinny jeans I had draped over the chair next to my bed. Ugh. They were still wet from yesterday's rain. My luggage had gotten caught in LAX on my way to Lima, and even though I'd waited an extra day before heading to Puerto Maldonado, it hadn't caught up with me. I'd just have to grin and bear it for now.

Aaron and Jeff examine the mysterious yellow bulbs. Photo by Christie Wilcox Soon, we set out on the trail — we being Jeff Cremer (an award-winning photographer), Aaron Pomerantz (entomologist for the center), our guide from the Tambopata Research Center, Frank Pichardo, and myself. "There's something you've gotta see," Aaron said. As we rounded the bend in the trail, it was obvious what he was referring to — in front of us stood a tall tree covered in strange, raised yellow spots. "What are those?" I asked him. He didn't know. But while colorful bulbs had caught Aaron's eye, what really intrigued him was what he found living amongst the canary protrusions: a caterpillar he'd never seen before, tended to by ants. Jeff zoomed with his macro lens while Aaron collected some of the larvae to hopefully raise into adults.

The caterpillar spotted by Aaron and its hymenopteran protective detail. Gif by Aaron Pomerantz, filmed with the help of Chris Johns I picked at one of the bulbs. The yellowish dome seemed to erupt from the bark, sometimes with a brownish cup at the base. The bulb itself was firm, but not that tough — my fingernail easily penetrated and split it in half. No visible spores, nothing to suggest they were the fruiting bodies of some fungus. The bulbs seemed plant-like, though unlike any plant parts I'd ever seen. There are trees that have fruits which burst from the trunk and branches, but those fruits are much larger, and this tree had dark, larger fruits on higher limbs. The yellow bulbs just seemed out of place, like they didn't belong. It turns out they didn't.

The mysterious yellow bulbs sprouting from the tree's bark. Photo by Christie Wilcox Aaron spent months talking to plant scientists around the globe to finally learn that the bulbs were the flowers of a rare parasitic plant belonging to the Apodanthaceae (possibly Apodanthes caseariae). The Apodanthaceae are a small family consisting entirely of endoparasitic plants — plants that live inside other plants — which only become visible when flowering. In retrospect, the caterpillar and its defending ants make a lot more sense knowing that the bulbs are freeloading flowers; parasitic plants around the world are hosts to similar symbionts.

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The romantic Christmas plant is actually a brutal parasite. Photo by Marilyn Barbone A year later, I carefully stretch my arms to pin a sprig of mistletoe above my doorway. Even standing on the step stool, it's difficult for me to reach, and I struggle to get the angle with my fingers to press with enough force (I hate being short). My boyfriend, Jake Buehler

, turns the corner and laughs. "Let me help you with that," he says, easily pressing the pin into the hard wood. His hand traces my arm down until his fingers cup my cheek, and he grins just before leaning in for a quick, gentle kiss. Mistletoe is my favorite Christmas tradition. When I was younger, I would buy dozens of sprigs and place them all over the place — above entranceways, hidden on ceiling fan blades, even under table edges — anywhere I might be able to sneakily line up to smooch whomever I was sweet on. I would spend hours brainstorming creative places to convince my man of the moment to place his head, so I could flash a sly smile and point to the leaves and berries above his crown and present my cheek for a kiss. I have always found it hilarious that we imbue such romantic power into a parasite. Mistletoes are parasitic plants found all over the globe. All pierce their host plants with a structure called a haustorium, which then steals water and nutrients for the mistletoe. Most are technically 'hemi-parasites', as their evergreen leaves are able to photosynthesize and thus produce some of the mistletoe's energetic supply (but I'm sure that's a distinction lost on the plants that these yuletide moochers penetrate and plunder).

Wild mistletoe stays green year round in part because it steals nutrients from its host. Photo by Matteo Sani People have been fascinated with mistletoes for centuries. Amongst the early inhabitants of the British Isles, it was considered a holy plant with magical curative powers, but it was the Norse that imbued romantic flare. Myths say that mistletoe was involved in the death of Baldur, the son of Frigga, the goddess of love and marriage. Somehow this led to the plant serving as a symbol of friendship and love and the tradition of kissing below it... though how isn't entirely clear. In ancient Greece, mistletoe was common during the festival of Saturnalia and marriage ceremonies because the plant's evergreen nature was associated with fertility. And in Roman culture, peacemaking was done beneath the parasite. By the 18th century, the association between mistletoe and Christmas emerged. Good fortune smiled upon those who locked lips beneath its boughs, while bad luck followed those who did not. According to etiquette, men could only give as many kisses as there were berries, as they were to pluck one for each smooch. We've been using mistletoe as an excuse to makeout during the holidays ever since. We're not the only species with a special relationship to mistletoe. While the trees it infects might not be too keen on its presence, lots of species rely on the parasitic plant. Artificial removal of Australian mistletoe species, for example, led to the loss of others

, especially birds, and a similar connection was made for birds and Mexican mistletoes

. The Australian Azure butterflies (genus Ogyris) are often associated with mistletoe

, which seems to be the preferred meal of their larvae. The caterpillars, in turn, rely on ants which protect them from harm, shepherding them between their nest and a feast of mistletoe leaves. The ants are so important to some species that female butterflies will selectively lay their eggs where the ants already are

, even if the plant itself isn't otherwise suitable. The ants, of course, aren't offering their services out of the goodness of their hearts — they are rewarded for their loyalty with a sweet secretion that the caterpillar produces.

An Ogyris genoveva caterpillar under the protection of a sugar ant (Camponotus consobrinus). Photo by Ross Field

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It's Christmastime again in the Amazon, which means that hidden in the vast, dense forest are more trees decorated with tiny yellow bulbs. Dutiful ants stand ever watchful over the small, fuzzy caterpillars like an insect nativity scene. As the people nearby revel in merry delight, the forest is alive with the yuletide spirit, brimming with ecological interactions that only occur during this very special time of year. The caterpillar Aaron found munching away on the parasitic yellow bulbs was the young of the butterfly 

Terenthina terentia.

 Like plant it was eating, little is known about these pretty little butterflies. They were described over a century ago, yet until Aaron stumbled across a strange tree in the Peruvian Amazon, no one knew anything about their larval stages, host plant, or ant-associated behaviors. Interestingly, the adult butterfly has a notable yellow spot on its wings — perhaps an adaptation to blend in when it perches amongst the bulbs where it lays its eggs.

An adult Terenthina terentia, with its notable yellow spot. Photo by Aaron Pomerantz No one knows how the butterflies find the rare yellow bulbs, which erupt only once a year from October to January. No one knows if its caterpillars can survive without them, or if there are other species which rely on the parasitic plant. No one knows how the parasites' flowers are pollinated, or how the plant spreads to infect new trees. After Aaron's discovery, we know more about these interconnected species than we ever have, but we still have a lot to learn. If these parasitic plants are anything like the ones we deck our halls with, then it's possible there are entire communities of species reliant upon the saffron nodules, an entire web of ecological interactions we've been completely oblivious to for centuries. While we have our Christmas traditions involving one parasitic plant, there may be dozens of Amazonian species celebrating the season with their favorite floral freeloader — perhaps even getting lucky amongst its bulbs.

A special thanks to the crew at Rainforest Expeditions for making my foray into the Amazon possible! (And for hauling my giant suitcase two days upriver when it finally did arrive, an entire week later. Especially thanks to Jeff for getting me a couple extra shirts so my stench wasn't too noticeable!)

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