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Trouble in paradise – why fruits are poisonous

Wolfgang Stuppy
28 August 2013

An inquiring mind is essential for a seed morphologist and Wolfgang Stuppy is no exception. August's 'Seed of the Month' post explores not just one seed but poisonous fruits and seeds of the world.

Why are some fruits poisonous?

In a comment on my last blog about the ‘dead man’s finger’, Tonio asked a very good question: "Why are some fruits poisonous?" After all, colourful, fleshy, juicy fruits convey a message that’s universally understood, even by very small children: 'Eat me, I am a sweet treat!'

Selection of colourful delicious fruits

 

Sweet treats: a selection of harmless delicious fruits as we know and love them [Images from ‘The Bizarre and Incredible World of Plants’ by Wolfgang Stuppy, Rob Kesseler & Madeline Harley; Copyright Papadakis Publisher, Newbury, UK] 

Killer berries

All too easily, the naivety of little children can trick them into mistaking shiny red, blue or black berries for sweet gifts from Mother Nature. Such a mistake can have fatal consequences if the berries of privet (Ligustrum vulgare, Oleaceae), deadly nightshade (Atropa belladonna, Solanaceae), white bryony (Bryonia dioica, Cucurbitaceae), daphne (Daphne mezereum, Thymelaeaceae) or mistletoes (Viscum album, Santalaceae) are involved. I have twin toddlers myself who put everything in their mouths that looks remotely edible, especially any bright and shiny fruit they find in the garden. More than once I observed with horror how they grabbed something from a plant and quickly popped it into their mouth. Fortunately, it was never anything dangerous and I could convince them to spit out whatever they just ‘sampled’ (this didn't apply to an earthworm that disappeared within a couple of seconds from in front of Ben while I was being distracted by his brother).

Colourful but poisonous fruits of Euonymus europaeus

The colourful but very poisonous fruits of the European spindletree (Euonymus europaeus, Celastraceae) are very enticing to small children

Trouble in Paradise

After millions of years of evolution, the fleshy fruits of present-day plants should have had enough time to perfect their seductive skills and provide us with a cornucopia of super-delicious treats. After all, fleshy fruits want to be eaten so the pressures of natural selection should have driven them to become ever tastier and irresistible. So why, if the co-evolution between fruits and frugivores (= fruit-eating animals) has driven fruits to become increasingly attractive to animals, do so many wild fruits look delicious but taste so bad or are even poisonous? This seems an evolutionary paradox, if not an evil trick of Mother Nature. As with all misunderstandings, one needs to know the whole story. The truth is that Nature ain’t no paradise! More than anything else, fruits have to defend themselves against all kinds of predators. In this respect, little has changed since the olden days. From the very beginning, the potentially trouble-free relationship between fruits and genuinely beneficial dispersers has been spoiled.

Delicious looking but poisonous fruits of Parthenocissus quinquefolia

The delicious looking fruits of the Virginia creeper (Parthenocissus quinquefolia, Vitaceae) contain oxalic acid which can cause severe poisoning and even death if a large number of the berries are ingested.

Flowers and deadly fruits of Bryonia dioica

Flowers (top) and fruits (bottom) of white bryony (Bryonia dioica, Cucurbitaceae). Allegedly, about 15 berries can kill a small child

Fruits of Prunus spinosa commonly known as sloes

The fruits of Prunus spinosa (Rosaceae), better known as sloes, look delicious but have a very tart and astringent taste.

The good, the bad and the ugly

All kinds of animals, ranging from fruit flies to ourselves, learned to capitalize on the nutritious rewards provided by fruits without dispersing the seeds. These "pulp thieves" eat the flesh but do not swallow the seeds, either because their gape is too small (e.g. fruit flies, beetles) or because their intelligence and dexterity allow them to distinguish and remove indigestible parts of the fruit, like hard seeds (e.g. some parrots, monkeys and apes). By taking the reward without providing a transport service, pulp thieves have effectively become parasites in the previously mutualistic system.

Pulp of a prickly pear being eaten by fruit flies and a longhorn beetle

Pulp thieves at work in Mexico: tiny fruit flies and a large longhorn beetle indulging into the sweet flesh of a prickly pear without helping to disperse the seeds

Take the best and leave the rest

Other thieves are less interested in sweet sugary pulp. Armies of insects, for example, have become specialised in preying on the most precious parts of the fruits, the seeds. What makes seeds such worthwhile targets is the highly nutritious food reserve which is meant to provide the small embryo plant they bear with energy during its germination.

Acacia penninervis seeds and their XRAY which shows insect larvae infestation

A seed collection from Australia (Acacia penninervis). The bright spots inside the seeds in the x-ray image on the right show infestation with insect larvae

The worst culprits

Among the worst seed predators are beetles. True weevils (family Curculionidae), for obvious reasons also called snout beetles, form the largest group of beetles. Weevils can easily be recognized by their long snout, called a rostrum, at the end of which tiny chewing mouthparts are situated with which they bore their way in and out of plant tissue. The family includes more than forty thousand species and nearly all of them are plant predators feeding on leaves, shoots, roots, cambium, wood, flowers, fruits and seeds. For example, infestation of stored cereals, especially wheat, corn and barley, with the 3-4 mm long grain or granary weevil (Sitophilus granarius) can lead to the devastation of entire granaries.

Snout beetle found munching on a seed collection from Madagascar

 

An unknown snout beetle that was ‘caught in the act’ at the Millennium Seed Bank while munching on a seed collection from Madagascar
(Image from ’FRUIT – Edible, Inedible, Incredible’ by Wolfgang Stuppy & Rob Kesseler, Papadakis Publisher, Newbury)

More bad and ugly

However, granivorous (= seed-eating) insects are not the only animals preying on seeds. Birds and mammals also boast legions of granivores. Finches specialise on eating seeds and so do many rodents, including mice, rats, hamsters and squirrels. For many other animals, such as deer and pigs who feed on acorns if available, seeds form at least part of their diet. Apart from insects, birds and mammals with a hunger for seeds, Nature also harbours an endless diversity of much smaller predators prepared to devour any organic matter that is unable to defend itself: fungi and bacteria. With their resilient spores omnipresent in air, water and soil, these most dangerous of enemies can cause all kinds of diseases. A fruit riddled with fungal or microbial infection becomes unattractive to potential dispersers even if not completely destroyed. Either way, the result is failure of the fruit's vital mission to achieve the dispersal of its seeds.

Mould fungi on a peach

Ugly pulp thieves: mould fungi can quickly make any fruit, like this peach, unpalatable to any bona fide dispersers

The evolutionary arms race

Literally, from ‘day one’, fruits had to find a trade-off between staying sufficiently attractive to bona fide dispersers whilst at the same time developing ways, such as poisons, to ward off predators. So on the one hand, fruits and bona fide dispersers co-adapted to each other to the benefit of both parties. On the other hand, the ancient game of attack and counter-attack between plants and predators sparked off another, sinister kind of co-evolution: an evolutionary arms race. Whilst selection pressures drove plants to constantly upgrade their mechanical and chemical defences, not only in their seeds and fruits but in all parts of their bodies, predators strove to overcome them through perpetual adaptation. For example, the seeds of legumes (Leguminosae) contain a gamut of toxic deterrents, ranging from cyanogenic glycosides, tannins and toxic amino acids to lectins (sugar-binding proteins), trypsin inhibitors (blocking protein digesting enzymes in the intestine) and bitter-tasting alkaloids, to name but a few. Small amounts of golden rain (Laburnum anagyroides), lupin (Lupinus spp.) or crab's eye (Abrus precatorius) seeds can cause deadly poisoning in animals and humans. Even pulses, although bred for centuries to suit human consumption, still require careful soaking, boiling, sprouting or fermenting before consumption to de-activate the toxins.

Bean mix that need soaking

Even beans we buy from supermarket shelves need thorough boiling to render them harmless before consumption

Evolution is all about trade-offs

Alongside the chemical warfare against "larcenous elements", fruits still have to provide a worthwhile meal for bona fide dispersers. With so many parasites causing conflicting selective pressures, the traits of fleshy fruits are likely to be the result of a trade-off between becoming sufficiently repulsive to the "bad and ugly" whilst still remaining attractive to the "good". Therefore, the ecology of fruits and vertebrate frugivores can only be understood when taking into account the entire evolutionary triangle between fruiting plants, their mutualists and their predators and parasites, including granivores. Toxic chemicals in fruits and seeds most certainly evolved to mediate these interactions through balancing the potential cost of losing dispersers with the benefits of protecting seeds.
 

Seeds of Abrus precatorius and Ricinus communis

 

The crab’s eye (Abrus precatorius, Leguminosae) and the castor bean (Ricinus communis, Euphorbiaceae) contain some of the most poisonous substances found in nature (see my previous post on the illustrious castor bean). 

Finally some good news!

The good news is that not only the parasites co-adapted with fruits and seeds, but also the mutualists. Whether or not a certain chemical compound is "poisonous" depends on the species in question. For example, many birds, the most important group of animal dispersers, are able to eat fruits that are toxic to humans and many other mammals.

Fruits of Actaea pachypoda know as 'dolls eyes'

The fruits of the appropriately called ‘dolls eyes’ (Actaea pachypoda, Ranunculaceae) from North America are poisonous to humans but harmless to birds, their main dispersers (Image from ‘FRUIT – Edible, Inedible, Incredible’ by Wolfgang Stuppy & Rob Kesseler; Copyright Papadakis Publisher, Newbury, UK)

Mistletoes and Deadly Nightshade

The berries of the European mistletoe (Viscum album, Santalaceae), a winter delicacy for small birds such as the mistle thrush (Turdus viscivorus, Turdidae), contain several small proteins that are highly toxic to mammals. The sweet-tasting black berries of the deadly nightshade (Atropa belladonna) hold a very potent mixture of tropane alkaloids (e.g. hyoscyamine, scopolamine and atropine) that interfere with acetylcholine receptors in the nervous system. Atropine in particular causes severe symptoms in humans, including sweating, vomiting, breathing difficulties, confusion, agitation, hallucinations and finally coma and death. Atropin also has a pupil-widening effect that was already known in ancient Greece, where an extract of 'belladonna' (Italian for 'beautiful woman') was frequently applied by women to enlarge their pupils. Widened pupils, naturally evoked by arousal, were supposed to 'intensify' eye-contact in romantic encounters.
 

White berries of Viscum album, the European mistletoe

The berries of the European mistletoe (Viscum album, Santalaceae) are highly toxic to humans but for small birds such as the mistle thrush they are a winter delicacy

Ever wished you could fly?

Deadly nightshade is also believed to have been among the main ingredients of the hallucinogenic brews of medieval Europe, including "flying ointments" that gave "witches" a sensation of flight. Apart from running the risk of getting you burnt at the stake, this kind of early drug abuse held other dangers. Atropa belladonna is one of the most poisonous plants in the Western Hemisphere and three berries are already enough to induce severe poisoning, not only in children but also in domesticated animals such as cats, dogs and livestock. However, wild birds and certain mammals, among them rabbits and deer, are able to eat the fruits and other parts of the plants without suffering any ill effects.

Fruit of Atropa belladonna commonly known as deadly nightshade

The fruit of the deadly nightshade (Atropa belladonna, Solanaceae)

So here’s the final answer:

The presence of poisons which are harmless for one group of animals whilst they are toxic to another enables plants not only to ward off predators but also to select the intended guild of dispersers from the available repertoire of frugivores. 

 -Wolfgang-

 (This blog is based on an excerpt from my book FRUIT– Edible, Inedible, Incredible by Wolfgang Stuppy & Rob Kesseler; Copyright Papadakis Publisher, Newbury, UK. All photos by me, Wolfgang Stuppy, unless otherwise stated.)


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Comments

6 September 2013
Comment: 
This was so enlightening. I love the way you described the three-way evolutionary arms race between the moochers, the dispersants, and the plants. And it's fascinating how mammalian genetics are so different that a squirrel's treat can be a human's poison. It also implies that those different physiologies were driven in part by co-evolutionary adaptation between plants and dispersants. Thank you for clarifying, in such a beautiful way, something that I've wondered about for years.
29 August 2013
Comment: 
I enjoyed this post very much and "the illustrious castor bean" is a beautiful phrase, as is the final sentence. I wonder whether fungi sometimes produce their own noxious/poisonous compounds to make food especially unappetizing to ensure their own monopoly and prevent being eaten short of their own reproduction. Queue theories of ergot-tainted rye as the source of the Salem witch panic... Re: "Whether or not a certain chemical compound is "poisonous" depends on the species in question." I think it's worth clarifying that for all known substances and all organisms, "the dose makes the poison". When we use the word "poisonous" it's always a short-hand for "poisonous in volumes that we sometimes ingest and die of eating". In the wrong concentrations or when ingested in the wrong way, even the most benign substances like oxygen and water become poisonous. Conversely, very dangerous substances may not cause us harm if the dose isn't sufficient. There are traces of cyanide in some foods we eat that aren't usually sufficient to make us ill, even as it is widely considered a poison. We're moralists and we apply "good or bad" binary thinking not just to other people, but also to the material universe of elements and compounds. In this thinking, "natural" insecticides are always "good" while synthetic ones are always "bad". Of course the truth is so much more complex... P.S. I've heard rumors about the relationship of flying ointments to broomsticks that I can imagine the author omitting for reasons of propriety. It is worth noting that one can sometimes be poisoned just by handling a plant (as poison ivy, poison oak etc show most dramatically).

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