Fungus farmers

Print edition : December 02, 2011

The largest known leaf hopper, Dorthula hardwickii. It is 28 mm long including the 12-mm long abdominal appendage. - PARAG GIRI

Insects began farming 40 to 60 million years before humans did.

"What sort of insects do you rejoice in, where you come from?" the Gnat inquired. "I don't rejoice in insects at all," Alice explained..

- Lewis Carroll, Through the Looking Glass

THE first revolution in the history of humankind, the agricultural revolution, began 10,000 years ago in certain parts of Asia, Africa and Central America. This comprehensively changed the patterns of human lifestyle. However, the revolution was neither unique nor exclusive to humans. Insects, which evolved 400 million years (MYA) ago, began farming 40 to 60 million years before humans started agriculture.

Three different groups of insects independently developed the ability to farm for their needs. About 330 species of termites, 220 species of ants and 3,400 species of weevils, referred to as ambrosia beetles, are farmers, and their cultivated crop is fungi1. Studies in evolution have revealed that in the case of ambrosia beetles, the habit of farming fungi rose independently seven times. This habit is not merely an absorbing story of weevil-fungi co-evolution but also evidence of the existence of the vast number of beetle species. There are, thus, nine lineages of insect farmers, each with different species, each of which has its own cultivars and style of cultivation.

Winged Termites seen soon after rains. They are a delicacy for many villagers in India.-

The entomologists Ulrich G. Mueller and Nicole Gerardo, authorities in this field, suggest that the termite-fungi association may have had its origins in a dead-wood feeding friendship. Both termites and fungi like to feed on dead wood. Did an accidental nibble excite the termites' palate and give them a taste for fungi? The process of actively cultivating fungi may have been a secondary ability developed by termites.

Plants have always enlisted the services of insects for pollination. Fungi may have similarly used insects for dispersal of their spores. Opportunists that insects are, they would have adapted to take advantage of such an offer. Entomologists believe this to be the genesis of beetle-fungal relationships.

The Jewel Bug, or Chrysocoris stolli, is a voracious feeder. It is a common plant pest.-

The picture of ant mycophagy is still far from clear. It is still uncertain what route ants took to establish their farming credentials.

Duur K. Aanen et al.2 have found that the termite-fungal symbiotic association had its beginnings in Africa about 24-34 MYA. Since its origin, this association has never lapsed: never has this species reverted from its farming state to a free-feeding one. Most termites import cultivars (in the form of fungal spores) from external sources during nest initiation. The spores acquired for a new nest are the product of sexual reproduction between fungi. However, as the nest expands, the fungal garden grows (on termite faeces) through asexual reproduction. In this manner, a fungal monoculture is maintained in the nest. At the same time, the termite workers adopt several strategies to prevent monoculture domination. Two interesting exceptions are seen in the genus Microtermes. The queen of this genus carries asexual spores in her gut to inoculate the gardens of her new nest3. In Macrotermes bellicosus, the male (or king) carries spores for the new nest initiated by the queen.

Insects are attacked by parasites too. Here, Borthogonia, a leafhopper, with phoretic mites.-PARAG GIRI

Fungus-farming ants belong to the genus Atta, commonly known as leafcutter ants. As in termites, agricultural practice evolved in attine ants only once and it did not lapse. However, ants do not import spores during nest initiation. Instead, they are carried by the winged female in a small pocket in her mouth specially designed for this purpose. When a suitable nest site is found, she first starts her fungal garden and begins laying eggs only when the fungal colony is established. The queen assists the first brood of workers in expanding the garden before retiring to the exclusive job of laying eggs. In South America, leafcutter ants are feared by farmers as they are known to devastate crops and vegetation in their search for suitable plant material for their fungal farms.

Ambrosia beetles are wood-dwellers. They too do not import fungal spores. The spores are either ingested or carried in special pockets called mycangia. When a beetle hibernates or migrates from its nest to a new location, it carries the fungal spores with it. Once it finds a suitable nesting site (a tree, for instance), it bores a tunnel into it. The tree will eventually have a gallery of tunnels where eggs hatch to form larvae. These tunnels are lined with a mixture of faeces and woodchips in which the fungal spores hatch and grow. The fungal farm provides the developing larvae with ample food but destroys trees. When beetles abandon their nest, other fungal species begin to grow on the ambrosia fungal gardens in the trees, causing large-scale damage.

The bright and beautiful Cantao ocellata, the only representative Scutellerid bug species in India.-

Farming entails a lot of work to keep farms and cultivars healthy. Insect farmers, too, need to work hard to maintain genetic purity in their fungal gardens and to remove pests and pathogens, such as mites, nematodes and the fungal spores of other species. Each ambrosia beetle cultivates a specific species of fungi. Scientists know how difficult it is to maintain a pure culture of fungi in the laboratory, but insects have managed to do this in the wild.

How they do it is yet to be understood completely. It is known, however, that they regularly weed their gardens to remove unwanted cultivars and constantly monitor them for mutant pathogens that may start an epidemic. They also isolate, maintain and propagate clones of favourable cultivars in large monocultures and introduce new cultivars and practise intercropping if needed.

The Nymph of the strange-looking hooded grasshopper.-

Attine ants use antibiotic treatment when required. These ants grow a species of Streptomyces bacteria on certain parts of their body from which they derive an anti-fungal concoction effective against fungal parasites. Bacterial strains, including Streptomyces, have also been isolated from the gut of termites and from ambrosia beetles. How well these antibiotics serve the two insect species is yet to be ascertained. But the successful insect farmer may have something to teach humans.

Insects... are not curiosities; they are creatures in common with ourselves bound by the laws of the physical universe, which laws decree that everything alive must live by observing the same elemental principles that make life possible. It is only in the ways and means by which we comply with the conditions laid down by physical nature that we differ, said R.E. Snodgrass in his book Insects: Their Ways and Means of Living4.

Neorthocris species, A wingless grasshopper. The male has a bright pink abdomen and the female is quite dull.-

Insect-plant interactions are evolutionary phenomena that are millions of years old. Plants and insects possess a love-hate relationship; insects pollinate them but many suck the sap out of a plant's life. There are insects that protect plants, and plants that feed on insects. It should, therefore, be no surprise that when humans decided to settle down and till the soil for food, they found insects that piggybacked on the plants. Early human communities dealt with insects in much the same way that insects dealt with pests in their farms. They found multiple strategies to limit the damage and also developed a palate for insects. The ancient adage seemed to be if you can't beat them, eat them. Termite queens, beetle grubs, locusts, grasshoppers and even mosquitoes figure on the food list of humans.

The short-horned grasshoppers (above and below) are masters of camouflage.-

Early human settlements practised integrated pest management without unduly poisoning themselves. They were perhaps aware that it was not necessary to eradicate insects; it was enough if their populations were kept under control. This, as researches seem to indicate, was the strategy of insect farmers too. Somewhere in the evolution of human agriculture, this strategy appears to have changed. Humans began to look at bugs as pests that had to be eradicated out of existence.

Bugs

Bugs is a term used to describe a wide variety of small animals that cause harm to humans. But in the scientific world, true bugs belong to the order Hemiptera, and they play a significant role in human agricultural systems. For this reason, hemipterans are a widely researched insect group. Phytophagous insects, as their name suggests, feed exclusively on plants. Sap-sucking and plant-chewing heteropterans, grasshoppers, several species of beetles and butterflies and moths are examples of insects that farmers recognise very well. Lesser-known and frequently missed out are insects that are farmers' friends. With mounting concerns over the use of poisonous pesticides, the chemical after-effects of fertilizers and increasing soil pollution, some of these lesser-known insects are beginning to receive attention.

A COFFEE LOCUST (Aularches sp.). Locusts represent the swarming phase of grasshoppers.-

The order Hemiptera includes a large variety of insects that show both morphological and physiological variations. For a layman, the easiest way to identify these insects would be to look for a small triangular chitinous part visible between the wings. A part of the forewings are hard and leathery in true bugs; hence, they are often mistaken for beetles. The hindwings are completely membranous. Heteropterans use chemicals for defence, and scent glands are characteristic of this group.

Acanthaspis Quinquespinosa an assassin bug that feeds on termites. The beak, or rostrum, is clearly visible.-

This is most predominant in bugs from the Pentatomidae family, whose smelly secretions have given them the common name stink bug. This disagreeable odour is accompanied by beautiful colours and attractive forms. The scent and the bright, warning colouration are the protective features of these bugs. Among the most common of these bugs, familiar to farmers and gardeners, are seed bugs, leaf-footed bugs, stainer bugs, jewel bugs, lace bugs, shield bugs, giant water bugs, bed bugs, assassin bugs and stink bugs.

The feeding habits of true bugs vary. Two-thirds of all heteropterans are herbivores. They have mouth parts designed specially to feed on plant liquids. Their proboscis, used for feeding, comprises needle-like stylets crafted from the mandibles and maxillae lying within a groove formed by the labium. This entire set-up is called a beak, or rostrum. Herbivores generally feed on the contents of plants' phloem and sometimes xylem (food- and water-bearing cells respectively). In addition, some species feed on flowers, ovules and unripe fruit to supplement their diet with nutrients, while others derive these nutrients from microorganisms in their gut.

A wingless female Haematorrhophus marginatus. The reduviid has special pads on its foreleg and mid-legs, with which it holds on to prey, which is sucked dry.-

Carnivorous heteropterans are as common as herbivorous ones. Bugs belonging to the Reduviidae family are commonly called assassin bugs, a description of their hunting ways. These predaceous bugs feed on a wide range of small creatures, including other insects. A reduviid belonging to the genus Acanthaspis actively hunts and feeds on honeybees, while an Acanthaspis quinquespinosa feeds on termites. Large aquatic bugs feed on insects and other creatures in their environment. Collectively, these carnivorous bugs keep a check on insect populations. But the bed bug, which feeds on human blood, has no natural predator.

This assassin bug, Ectrychotes, belongs to the family Ectrichodiinae, known for its bright colouration. The insect hides under leaf litter and preys at night.-

Homopterans

There is no difference in the fore- and hindwing of homopterans; as the name suggests, the wings are uniformly membranous. All homopterans are plant feeders and predominantly tropical in distribution. Some hoppers may bite humans, but they rely on plants for their nutrients. These insects are also famous for their various ways of communication. Their general form and appearance is quite different from that of true bugs. Cicadas, froghoppers, planthoppers, treehoppers and leafhoppers are all homopterans. Wingless, often un-insect-like in form, they are detested by gardeners; aphids, scale insects and mealy bugs also belong to this group.

The Pentatomid, or stink bug, produces secretions that give off a strong odour because of which it is considered a delicacy and eaten in some countries.-

All homopterans feed on the sap from the xylem and phloem of plants. As they are liquid feeders, they also tend to excrete fluid. Cicada sprays are famous in forests. Some of the ejected fluids, called honeydew, are actively sought by ants, who in turn provide protection to these bugs. These homopterans pierce plant tissues to lay their eggs.

The Shield Bug also produces unpleasant smells when stressed. Here, Cyclopelta siccifolia.-

Collectively, their breeding and feeding habits cause problems for farmers by injuring plants and paving the way for infection by pathogens.

The Seed Bug, or Graptostethus. It is commonly seen on the Ipomea plant. It feeds on seeds.-

The evolutionary versatility shown by bugs, in being able to occupy a wide variety of niches in the environment, brings them into direct conflict with humans engaged in agriculture. However, versatility is indicative of diversity. Human ingenuity needs to take advantage of this diversity to reduce conflict by enlisting their cooperation.

The Cotton Stainer bug, or Dysdercus similis. A yeast that resides in its head gets transferred to the cotton plant, staining it and reducing the value of the lint.-

locusts

The word locust has been used for a variety of insects and crustaceans. Any insect that appears in large numbers, like the cicada, for example, has also been referred to as a locust. However, the true locust is a short-horned grasshopper. Its close relatives, bush crickets or katydids, are found in the same habitat and are called long-horned grasshoppers. Grasshoppers, crickets and gryllids belong to the order Orthoptera, meaning straight-winged insects. Although found in similar habitats, katydids and grasshoppers differ in their food habits, the latter being a complete herbivore.

A Forest Leafhopper (Calodia sp.) basking on a leaf.-

The term locust is used to describe the swarming phase of grasshoppers. Research has shown that swarming5 is a result of overcrowding. When there is crowding and the hind legs of different grasshoppers touch, the production of serotonin a neurotransmitter found in humans as well is stimulated. The increased levels of serotonin bring about morphological changes and an increase in appetite. This results in increased feeding and an increase in the reproductive rate. Thus, grasshoppers breed profusely and increase in number, resulting in a locust swarm. One can imagine the devastating effect this has on plants. The transformation of grasshoppers to swarming locusts continues to increase because of the increasing rates of contacts between members of the growing population.

Leafhoppers from north-eastern India. Atknosoniella opponens and, below, Evacanthus sp. They are a xylem (plant water-bearing cells) feeders and hence excrete copious amounts of liquid.-PARAG GIRI

According to some people, there existed a custom in certain parts of India whereby a locust was caught in its initial growing stages, decorated, revered and then released in the fond hope that it will take the swarm away.

When an insect in such large numbers is found destroying carefully tended crops and is difficult to get rid of, it seems only natural that humans would contemplate using them as food. In this technology-directed century, the axiom of new-wave thinking is to do more with less. Micro-livestock refers to the farming of rapidly reproducing small animals, especially insects. This is still an emerging process. Despite the strong wave of vegetarianism, livestock farming is not going to diminish, and with the steady increase in the population, humans will have to find ways to produce more food in less space. Insects have been a food source for several cultures across the world. Termite queens are a favourite food of many villagers in Andhra Pradesh. The many flying termites that emerge during the rains to start a new family are collected by the villagers as food. Even among cultures that have dietary laws prohibiting the consumption of animals, certain species of grasshoppers are allowed as food.

Aphids (above and below, Aphis nerii, the oleander aphid) are the most common pests in gardens and are difficult to get rid of. Ladybird beetles feed on them.-

Insect-farming operations have a smaller ecological footprint than other livestock farming. Insects grow to maturity quickly, reproduce at explosive rates, occupy less space, require less water and feed, but have a high food conversion efficiency6. Insects are a rich source of protein. In contrast to cattle and poultry, with their increasing number of pathogens, insects are a safe source of nourishment.

Compare the nutritional value of common meat products with insect meat to understand why insects are beginning to be accepted as a food source: 6,100 grams of beef provides humans with 210 calories, 15 g of fat and 20 g of protein; 100 g of grasshopper meat provides 97 cal, 6.1 g of fat and 20.6 g of proteins; 100 g of caterpillars provides 268 cal, 17 g of fat and 28 g of proteins. Before long we will be buying Chocolate Chirpie Chip cookies (with crickets) at food courts. Movie theatres in South America sell roasted ants, not popcorn. This is not a reality show on television in the United States or India, but the hard-core reality of life in many countries.

There are already over 1,400 edible insect species familiar to humans. Many more are waiting to be discovered. These insects can thrive in environments that are hostile to current livestock farming and agricultural practices. Moreover, insect feed can be a means of waste disposal. Termite farms could use waste from the wood and paper or sugarcane industry as feed; such waste is currently incinerated or thrown into waterbodies.

The female and the male Lacusa fuscofasciata. Very little is known about the biology of this fulgorid hopper.-

More importantly, unlike cattle, insect livestock farming would neither produce greenhouse gases nor require the use of antibiotics. In their wanderings between blades of grass and the wastes from the kitchen, insects would, if humans agree, adapt to this new role too from insect farmers to farm produce and still roam freely.

The Yaqui tribespeople of North America narrate the story of a confrontation between a lion and a cricket. Long ago, the lion, in a fit of pique at being ignored by a singing cricket, challenged it and its army to a war with his carnivorous animals to establish that he was the king of the forest. Gleefully, the cricket agreed and came with its army of insects. Ants bit the feet of the wolves and the leopards, and bees and wasps stung their bodies and eyes, forcing the lion and his warriors to flee and leave the insects alone.

The Flatid Hopper, which feeds on plant sap, can be recognised by its large, triangular wings.-

The dominance of insects is a fact. Given the environmental degradation of this century, it would be of benefit to humans, and to the earth, if they get to know insects more closely and enlist their cooperation.

Geetha Iyer is an author, a nature enthusiast and an independent consultant in the fields of education and environment.

REFERENCES

1,3. Mueller, Ulrich G. and Gerardo, Nicole; Fungus-farming insects: Multiple origins and diverse evolutionary histories'; PNAS; Volume 99; No.24; pages 15247-15249.

2. Aanen, Duur K.; Eggleton, Paul; Rouland-Lefvre, Corrinne; Guldberg-Frslev, Tobias; Rosendahl, Sren and Boomsma, Jacobus J.; The evolution of fungus-growing termites and their mutualistic fungal symbionts'; PNAS; Volume 99; No.23; pages 14887-14892.

4. Snodgrass, Robert Evans; Insects Their ways and Means of Living'; Volume 5 of the Smithsonian Scientific Series (1930) published by the Smithsonian Institution Series, New York.

5. Rogers, Stephen M; Matheson, Thomas; Despland, Emma; Dodgson, Timothy; Burrows, Malcolm and Simpson, Stephen J.; Mechanosensory-induced behavioural gregarization in the desert locust Schistocerca gregaria'; Journal of Experimental Biology (2003); 206 (22); pages 3991-4002.

6. Dzamba, Jakub; Third Millennium Farming (3MF) Insect Farming in Cities'; University of Toronto (2009).

Acknowledgement

I have been able to do this series largely because of the time, encouragement and assistance given to me by Dr Chandrashekara Viraktamath, Emeritus Professor at Gandhi Krishi Vignyan Kendra, Bangalore, a world authority on leafhoppers. I owe a lot to the taxonomist Dr Prathapan Divakaran, of Vellayani, Thiruvananthapuram, who was always helpful. Thanks are also due to the entomologists Dr Priyadarsanan Dharma Rajan, Dr Seena Narayanan Karimbumkara, Dr K.G. Sivaramakrishnan, Dr J. Poorani and Dr K.A. Subramanian and to Pranav Balasubramanian, a Class XI student, all of whom helped me with identifying the insects. Thanks are due to my daughter, Sandhya Iyer, for her critical feedback.

Geetha Iyer

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