The Unexpected Pollinator Of The Cocoa Tree

The following is an excerpt from The Secret Life of Flies by Erica McAlister.

Hate chocolate? Well, I do. I simply detest the stuff—have done for years. I dislike the texture and the way it slimes down your throat, but most of all I don’t like the smell—just thinking about it turns my stomach. Even I have to admit this is not the most normal of dislikes. It is ironic considering my love of flies. Confused? Flies, you see, are the only pollinators of chocolate, or more specifically Theobroma cacao, the cacao or cocoa tree. This plant species has a complex reproductive structure, so complex in fact that only one group of very small flies, amusingly known as No See Ums, can pollinate it. This group, from the Forcipomyia genus of the family Ceratopogonidae, are, along with the rest of the family, known as the biting midges. Biting midges are cursed across the globe for ruining many a day in the countryside, especially the infamous Highland midge swarms in Scotland. According to her diary, Queen Victoria was half-devoured by these little ladies whilst at a picnic in Sutherland woodland in 1872.

The female adults of many biting midges have very painful and sometimes fatal bites due to some of the diseases they can transmit. They can also swarm in huge densities which can cause a large amount of blood loss.

But without these minute, often rage-inducing flies, many people would consider that life is no longer worth living. Cacao producers are very worried about the ongoing supply of their ‘miracle’ substance. Our (yours not mine) demand for the stuff is vast—it’s an $80 billion year industry with 3.5 million tonnes produced annually, a figure set to increase to 4.5 million tonnes by 2020. But it is a volatile time for this product—traditionally the tree has been grown on small-scale farms but these are affected by increased stochastic weather patterns, growth in the numbers of pests and diseases and by political instability in many of the countries where the cacao tree is grown. These factors are exacerbating the already naturally low pollination rate of the plant. Many of the small-scale cacao farms are now moving across to larger set ups to overcome some of the negatives and boost yields, but this has also had repercussions on production.

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The cacao plant has both male and female reproductive organs on the same plant but it cannot self-fertilize and so is entirely dependent on the midge to do this. It’s one of the many little known facts about flies and the benefits they bring us. Despite the efforts of the flies, few of the flowers go on to produce fruit; it’s a tricky business. No fruit means no bars of Galaxy or Curly Wurlies. Add poor pollination rates to the cultivation of these plants and your success rates drop further. The fact is, the pollinating flies are tree lovers—they like damp and shady conditions and many of the species require aquatic, semi-aquatic or moist soil conditions for their larvae to develop in. On these cultivated farms, trees are removed to create more space for the cacao but this removes most of the shade as well. So now there is very little shade and very limited leaf litter, and so nowhere for either the adult flies or their offspring to live.

In cultivated plots the average pollination rate is shockingly low at 0.3%. By cultivating forests for the production of the plant we are ironically destroying chocolate (and the midge!). Surely for chocoholics saving this fly ranks up there with saving the giant panda, which also has reproduction challenges.

Not only do flies from this family pollinate chocolate, some—again in the genus Forcipomyia—pollinate heather species within the genus Erica (I was destined to love flies). Why is this important? Well heather grows with abundance in the Scottish mountains, and the Picts—a group of people who lived in what is today eastern and northern Scotland during the Late Iron Age and Early Medieval periods—used to make heather ale as long ago as B.C. 325, and that they could was largely thanks to flies. The myth behind the birth of whisky was that some of this heather ale was being baled in a stone roof cottage, the steam condensed and into a cup, whisky dripped!

That story may not be totally true but there are many similar stories that reveal the close relationship between insects and flowering plants. Flowering plants evolved after insects had arrived on the planet and the success of plants is very much down to the symbiotic relationship they have with insects. Evidence of this relationship first appeared between 130 and 140 million years ago and the intervening years have seen many plants and insects, including the flies, evolve some exclusive relationships with each other. Two species of biting midge have been observed pollinating the long flowers of Erica species and are only able to do so as they have elongated mouthparts—so the nectar in these plants is only accessible to insects with long proboscises. Another fly, Rhynchoheterotricha stuckenbergae, a small dark-winged fungus gnat from the family Sciaridae with a true tongue-twister of a name, is another species with a very long proboscis, about three times the length of its head! Peringueyomyina barnardi, a primitive crane fly in the family Tanyderidae, has an equally long proboscis and another crazily long name— maybe there is a correlation between the length of names and the length of the proboscis? All of these species have only been found in the Cape region of South Africa where the climate and geography have led to the development of a highly endemic flora which includes many species with nectaries found deep within the long, tubular petals of the plants. These long-named flies and long-tubed plants have become co-dependent on each other.

The pollinating role of flies is hugely important for the general health of a range of ecosystems, including agricultural ones. Of the 150 families of flies, almost half, 71, have been shown to feed from flowers and therefore in principle transmit pollen from one plant to another. It’s not just the number of species that qualifies flies as important pollinators but also their distribution. As already mentioned flies are ubiquitous—they are everywhere. My colleagues and I have caught flies in the most unlikely places, the toughest of which was at more than 4,800 m (15,750 ft) altitude, up a mountain in Peru. This is not easy as the ‘pooters’ we use to catch them rely on manual suction. I don’t know how many of you have been to those altitudes but the oxygen is so thin I could barely crawl, let alone breathe. We had to try and suck up flies into a tube, often with limited success, with many a fly just sitting there on the plants unaffected by our ineffectual pootering. The point of this story is not to highlight my own inadequacies in failing to collect flies but to point out that flies are found at such high altitudes. A whole variety of them are found in these regions, including many hover flies from the family Syrphidae.

Hover flies are exceptionally common, distributed everywhere and very species-rich, with more than 6,000 species described globally to date. They are considered to be the most important of dipteran pollinators although this may change as our knowledge of fly biology increases. As their name suggests, they hover—when I was learning Latin family names I always found this group easy to remember as I would think of them ‘surfing’ (‘Syrphing’) on the wind.

In the USA this family is also called flower flies in acknowledgement of their associations with plants and their importance as pollinators. Many species in this group are distinctive and familiar in appearance—but not as typical flies. Rather, they are clever mimics of bees, wasps and hornets. It makes sense for a species to look like a more dangerous species to protect itself against potential predators, which at a glance will ignore them for a less risky morsel.

These pollinators have no venom like their dangerous doppelgangers, let alone a sting. But they do spend a lot of time out in the open, guarding their territories and trying to attract the opposite sex or feeding from plants. Most people have no idea that most of the little yellow-and-black insects zipping round their garden at speed—some can fly in short bursts at up to 25 mph (40 kph)—are not the helpful bees they think they are, but rather helpful flies. Among their many morphological adaptations to assist with pollen transfer is their covering of thick hairs which, while the fly is feeding on flowers, pick up pollen.

Hover flies are second only to solitary bees and bumblebees in their value as commercial pollinators. The economic worth of all insect pollinators of cultivated crops has been estimated at about £120 billion, which equates to 35% of global crop-based food production. Flies form a high component of that figure and they are key pollinators for many crops including mango, chilli pepper, black pepper, carrot, fennel and onion. I may not like chocolate, but I would be devastated not to have pepper in my life.

One of the most spectacular-looking groups of pollinating flies is the tangle-veined flies of the family Nemestrinidae. The adults are beautiful creatures, generally robust and chunky in shape and, more often than not, fluffy. As their name suggests, they have a distinct vein pattern on their wings which helps us to identify which flies belong to the family. And with this family, very unusually, it’s the female’s genitalia that grab the attention of dipterists. Male genitalia in flies are often ornate and vary considerably across species, even closely related ones, whereas with females there are generally few or no differences. Within Nemestrinidae however the female’s ovipositor varies considerably across species and so it is a very useful characteristic to aid identification. There are five subfamilies of tangle-veined flies: two of them (Hirmoneurinae and Nemestrininae) have telescope-shaped ovipositors that have retractile segments forming a pump-action, egg-laying machine. The other three subfamilies (Atriadopsinae, Trichopsideinae and Cyclopsideinae) have sabre-shaped ovipositors, with two very long and slender valvulae (a scientific term for diptera lady bits) from which the female shoots her eggs.

It is not just the shape and functionality of their genitalia that make the females so unusual, they can also lay several thousand eggs in their lifetime—compare this to a house fly, which only lays about 500 eggs in a lifetime. Several thousand may seem like a lot of eggs but there is a high attrition rate because the food source sought by the larvae is rather mobile, and includes locusts and grasshoppers. After about 10 days, the scattered eggs hatch into very active larvae called planidia. These readily disperse, often helped by the wind, into their surroundings to seek out their hosts, which vary across the family, with the Nemestrininae and Trichopsideinae subfamilies choosing grasshoppers, Atriadopsinae seeking bush crickets and Hirmoneurinae preferring scarab beetles. The fifth subfamily, Cyclopsideinae, is only known from a couple of specimens found in Australia and we know nothing of their host preference or anything else about them. This subfamily is solely represented by those few specimens and comprises just one species. What is depressing, but sadly a common state of affairs with many species, is that the holotype—the specimen that was used to formally describe the species—was destroyed. Not only do we know nothing about the biology of these flies but we also have hardly anything to work with in museum collections.

What we do know about the larvae of the other subfamilies is that they can survive for up to two weeks as an active mobile planidium, seeking out a host. Their hosts are also very active and most larvae perish during this stage. Successful individuals then undergo a second morphologyical change once they have found and penetrated their host. Not content with normal larval development, they alter the structure of the later stages hugely in comparison to the initial one, a process known as hypermetamorphosis. After being the sleek, active little host-seekers, they then behave like slobby teenagers by becoming sedentary parasites.

Although the larvae are interesting, it is not this stage that is important in pollination. Adult tangle-veined flies are special pollinators in that many are species specific and have co-evolved with their host plants to such a point that the flies often have the most spectacularly elongated mouthparts, necessary to penetrate the equally long tubes of the flowers in exclusive, mutually dependable, relationships. Most nemestrinids, of which there are approximately 330 species globally, have fairly long proboscises. Many of these are fairly rigid and can’t be curled up neatly out of the way when not in use as seen with butterflies and moths. Flies cope with what would seem to be an enormous inconvenience by loosely tucking the proboscis underneath their body as they fly, and a few species are able to partially retract them into their heads.

The idea of manoeuvring around with a proboscis 0.5 cm (¼ in) long for flies around 1 cm (½ in) in length sounds fairly cumbersome, but that is nothing in comparison to one species, Moegistrorhynchus longirostris, which has a proboscis that can reach eight times its body length (that’s up to 8 cm or 3¼ in). If humans had a tongue equal in ratio to this our tongues would be over six metres (19½ ft) long. This species has the longest proboscis in relation to body size of any insect. And why is it so long? Because they have co-evolved with the plants with long-tubed flowers, which include irises, orchids and geraniums, to feed and pollinate them exclusively. These groups of flowers are either pollinated exclusively (eight species) by M. longirostris or by it and a few other morphologically similar species. Moegistrorhynchus longirostris is therefore a keystone species, in that it is critical to the survival of these long-tubed plants—remove this and the flies die out. The Cape region of South Africa, where these flies are found, has an internationally recognized flora due to the diversity of plants that exists there and, when we get round to identifying all the fly species from this region, we’ll probably find they are equally diverse (and, may I add, equally if not more attractive).

Another dominant group of flies found in this region are horse flies in the family Tabanidae. Horse flies, when they are acknowledged, are generally considered evil, annoyances of impressive size and endeavour. But most of the females of these determined bloodfeeders also need nectar to provide energy for flight and the males feed exclusively on it. Within the subfamily Pangoninae, commonly called the long-tongued horse flies, there are many examples of important pollinators.

The Cape is also home to another fly with a long proboscis, Arthroteles cinerea, in the Rhagionidae family of snipe flies. This species has been observed clinging on to plants even in strong winds, yet it is quite useless at walking due to its poorly formed legs. All of these long-tongued flies (and there are more examples from different families) are crucial for the plants that grow there and nowhere else in the world can you find so many of them.

A species of fly that is less regionally specific is the fungus gnat Gnoriste megarrhina, which pollinates the pick-a-back plant, Tolmiea menziesii. This plant is a saxifrage, a common plant that was originally native to the North American woodlands. Its flowers dangle down loosely and have long tube-forming petals. The gnat has to reach deep into this flower’s corollas, or petals, to obtain nectar and as it does so it rubs pollen onto its body, ready to be transferred onto the next plant. This gnat is but 7 mm (¼ in) long but has a proboscis that is almost the same length again.

Flies are able to cope with such long proboscises because of suction pumps in their heads. Fluid enters the proboscis by capillary action, a process whereby the pressure of cohesion and adhesion causes the nectar (or blood) to flow up the tubes. This can however be very time-consuming, and flies have sped up this process by using suction pumps. Six different types of suction pumps within the head region have been identified, with the type and number varying in different groups. For example, the tangle-veined fly, Prosoeca sp., which has a very long proboscis, has two such pumps to assist with nectar uptake, whilst the horse fly, Philoliche sp. has just one. The hover flies in the Rhingia genus not only have several suction pumps, including a pump at the base of the labrum which generates the pressure to suck nectar into the food canal, but have also cleverly developed a way of protecting their elongated rostrums when not in use, with a very distinctive beak—they look like they have a spout coming out of their heads. Their mouthparts, when extended, are about nine times longer than the beak but are completely tucked away under the snout when they’re not feeding. At the tip of their proboscis they have a bristly pair of labella which they use to dab at or scrape the flower to remove the pollen.

Moving away from the warmth of southern Africa, some of the most hostile regions in the world are the Arctic and its polar opposite, the Antarctic, where survival is hard and flies have to cope with extreme fluctuations in temperature and daylight. In the Arctic the average yearly temperature is -40°C (-104°F) and the summer temperatures only reach the balmy heights of 10°C (50°F). On top of that there is very little shelter from the high winds as the landscape is dominated by very low vegetation and there is no tree cover. Only 4,000 or so species of insect have been described from these regions and roughly half of these hardy little critters are flies. And these are of critical importance to the environment through their pollination efforts—bees don’t cope well in such extreme habitats and so, thank goodness for the flies. Even though bumblebees have thicker coats they struggle with such low temperatures or high winds and the species numbers are greatly reduced. Flies on the other hand have adapted well to this environment and many of the plants have evolved alongside them.

Adult, non-biting midges from the family Chironomidae are some of the most important pollinators in the Arctic. These flies have had to survive arduous conditions to get to this stage of their lives. They undergo long periods of freezing as well as extremes of light or darkness. Smittia is a genus from this family that includes species found all over the world, with several important pollinators adapted to living in very cold conditions. Smittia velutina is one of the most dominant species found in the High Arctic and an important pollinator of plants including Saxifraga oppositifolia, the purple saxifrage, a dominant Arctic plant species. This plant has been found on Kaffeklubben Island in north Greenland, at 83°40’N, the most northerly plant locality in the world, and also in the Swiss Alps at over 4,500 m (14,760 ft)—this plant likes extremes! Its pollinating midge is an early emerging species and, interestingly, is thought to be parthenogenetic—a form of asexual reproduction where the offspring develop from unfertilized eggs—as no males have ever been found. Parthenogenesis is a particularly useful strategy if you want to produce vast numbers of eggs quickly to capitalize on an abundant, but possibly short-lived, food source. The flowering periods for plants such as purple saxifrage are very short and as such the flies have to develop rapidly to keep up. Why spend time fornicating when there is food to be harvested in a short space of time? An investigation into their ovary development found that the flies were able to mature in about three days, so vast numbers could be produced during favourable conditions. What is rather nice about these flies is that they are diaheliotropic, which means they are sun worshippers and rotate with the sun. Experiments have shown that they rotate around on the flowers to ensure they are exposed to the maximum amount of sunlight as possible. And, a fact that I find most amusing, these flies are what is termed ombrophobic—they don’t like the rain! So if it does start raining they use the flowers as umbrellas and hide underneath them.

It’s not just midges that are found in the Arctic; there are root maggot flies (Anthomyidae), dance flies (Empididae), frit flies (Chloropidae), dung flies (Scathophagidae), cheese skippers (Piophilidae), mosquitoes and house flies to name but a few. In 2016, researchers from Canada, Denmark, Finland and Sweden published their findings on Arctic pollinators across northeast Greenland. Not only were the flies shown to be so much better at pollinating than other insects but house flies were better than the rest. And within that family one species collected the gold medal as top pollinator, Spilogona sanctipauli. These drab little house flies are key pollinators so the recently observed decline in their numbers can only be cause for concern.

Male mosquitoes (and some females) are nectar feeders and we have known that they are important pollinators for more than 100 years. But we’ve only recently really been studying individual mosquito species, and there are still many assumptions and vague speculations as to their role and importance. We do know that the species Aedes communis is an important pollinator of the blunt-leaved bog orchid, Platanthera obtusata. It doesn’t carry the pollen on its legs or body like other pollinating flies. Instead the pollen balls become stuck to its eyeballs while the mosquito is head down in the plant trying to reach the nectar. The lengths they will go to.

Plants in inhospitable regions have developed little tricks to aid their beleaguered pollinators. As well as providing food, the plants offer warmth and protection. Some plants can raise their own temperature to 15-25°C (27-45°F) higher than the surrounding environment and so keep the snuggling flies cosy, enabling them to warm up enough to fly and so keep pollinating the community. This plant strategy is called thermogenesis and is found in at least 10 families of angiosperms. The skunk cabbage, Symplocarpus foetidus, a plant found across continental North America, can raise its temperature to 35°C (63°F) above the ambient environmental levels when conditions become too harsh. This enables the plant to flower while there is still snow on the ground (it melts the hard ground and then the snow) and so benefit from the early emerging pollinators. And the flies themselves have some ingenious coping strategies for the long, cold dark winters and short, only slightly less cold, summers. There may be summer as well as winter cocoons to protect the larvae. Some become tolerant to freezing, like the fly Heleomyza borealis, which has larvae that survive in temperatures down to -60°C (-76°F), and others, like the Arctic gall midges, super-cool themselves and so are able to remain unfrozen even in extreme temperatures of below -62°C (-79°F) .

The Antarctic is even more species-depauperate than its northern counterpart. There are very few insect species to be found there and most of the plants have subsequently evolved to be wind-pollinated. Back in 2010, Professor Peter Convey and his research colleagues published an article about two colonizing fly pollinators on South Georgia, a sub-antarctic island. The arrival of these pollinators was not a positive event though, as it is thought they will encourage other invasive insect species that previously couldn’t establish permanent populations there. The larvae of these species are able to consume and break down dead and decomposing material and as such release more nutrients into the soils, so affecting the balance between existing plant species and their environment. It is feared their influence may gradually alter the environment and many of the original, very environmentally specific species will disappear.

There are plants in other regions that are not considered to be insect-pollinated but rely on the wind to transfer pollen. For example, we typically think of grasses as being wind-pollinated as they lack the obvious bright flowers to attract insects. But in fact many types of grass are pollinated by insects. In places like forests, where there is little or no breeze, some species of grass have turned to flies to help them spread their seed. Some of these pollinators are found in the scuttle fly family Phoridae. This family has perhaps the most ecologically diverse collection of flies in comparison to all the other families of flies, and as such maybe of all the insects. Identification of these tiny flies, and I do mean tiny—a recently described species measured just 0.4 mm long—is very difficult though and several genera within the family are numerous, the genus Megaselia has over 1,500 species.

I call them horrid phorids for giving dipterists taxonomic-induced headaches whilst trying to identify them—most dipterists physically crumple at the thought. Luckily there are a few taxonomic experts out there who do work on this family as they are very important in many ecosystems, including forests. I can attest to the numbers that are found in these environments as a while ago I had a series of pitfall traps (plastic cups dug into the ground) laid out across a rainforest in Costa Rica. These traps when collected were dominated by beetles and these rather strange-looking creatures. They looked like insects in that they had the usual head, body and legs, but they were wingless. It turned out I was being hoodwinked by wingless females of this phorid family. Phorids are dominant in many ecosystems including forests and although information is limited, several species have been found to pollinate the rainforest grass species Pariana.

We are now discovering that more and more species of flies are either accidentally or purposefully acting as pollinators, including some unexpected ones. Many species of house fly possess pollen-retaining bristles and we are just beginning to study the impact these species have. House flies and flesh flies are also often tricked into pollinating plants. Many species of fly are not nectar feeders and like nothing better than a piece of meat, the older the better—a nice bit of rotting flesh is the perfect repast. And plants have cottoned on to this and are mimicking the smell and/or the appearance of decomposing flesh. Pollination by flies on rotten meat-smelling plants is called sapromyophily, which means flesh fly loving, and there are many plants that depend on this. In the Aristolochia genus of plants, more commonly called the Dutchman’s pipe, there are a large number of species that are rather pungent. To the flies their aroma of fresh carrion or dung is nothing less than exquisite. Once lured in, the flowers have long tubes internally covered in hairs which act at times to trap the fly and enable pollen transfer.

This process of kidnapping flies for pollination is at its most sophisticated with Aristolochia grandiflora, the pelican flower. The flower has a huge landing pad that acts to direct the flies down into its large reproductive chamber, within which the flies are held captive. On the way down to the chamber the flies brush past stiff hairs called trichomes that point into the chamber and act like barbs, preventing them from getting back out again. But fear not, it is not all over for the fly. This is just the first part of a three-stage reproduction process. Firstly the plant removes the pollen of other plants of the same species from the fly and fertilizes itself. Secondly, over a day or two, its own pollen-producing organs mature, and the fly rubs against this new source of pollen. Then finally whilst incarcerated, the fly munches on nectar produced in the walls of the flower. This stimulates the plants to destroy the thick (gaol) hairs and so enable the fly to escape. Free, but not unburdened, the fly heads off once more to find another sex-starved plant. Genius.

There are many other examples of plants that use so-called carrion flowers (or corpse flowers) to attract flies. One of these is the enormous Amorphophallum titanum (titan arum), the plant with the largest unbranched inflorescence in the world, reaching heights of three metres (9¾ ft). Imagine if you can an oddly coloured, enormous, half-peeled banana. Titan arum is an unpredictable flowerer, but when it does, it emits this incredibly powerful carrion odour! Some claim it has the foulest odour on the planet. And the flies, flesh flies to be exact, love it (though dung beetles also pollinate the plant). Not only do these flesh flies assist in pollination, their larvae are also parasites of snails—quite a gardener’s friend. These plants, and other similarly pollinated plants, have taken this method of attracting the pollinators a step further by heating up the flowers so they appeal even more to the insects—warm rotten flesh. I was recently able to collect flies from a flowering titan at the Royal Botanical Gardens, Kew, in London, and I can testify, quite emphatically, that they do indeed stink.

Flower deception like this has evolved in more than 7,500 species of flowering plants, and two-thirds of these sneaky species are orchids. Epipactus veratrifolia, the eastern or scarce marsh helleborine, is a type of orchid that mimics the alarm pheromones of aphids, and the flowers have aphid colouring so as to attract the aphidophagous larvae. The migrant hover fly, Eipeodes corollae, is one such species of hover fly that gets fooled by this rather sophisticated trick.

There is still so much to discover. A paper on pollinators published in 2015 by Katherine Orford and colleagues highlights that our knowledge of the pollinators is generally restricted to one or two very well-known families but there are masses more that we don’t have any information on at all. It’s also important to recognize that pollination isn’t the realm of bees alone. In fact, Alison Parker and colleagues at the University of Toronto, Canada, developed a computer model comparing the effectiveness of bee and fly pollinators. They determined that, because bees hoard the pollen they gather, flies, which don’t do this, increased pollination events with more visits. It really is time we really started to re-evaluate the role of pollinating flies, if not just for pepper and chocolate.

From The Secret Life of Flies by Erica McAlister. Copyright © 2017 by The Trustees of the Natural History Museum, London. Published by Firefly Books Ltd. 2017. Reprinted with permission.