The white dapperling – a mushroom that isn’t poisonous…

Fungi are remarkable organisms, essential for the recycling of nutrients by breaking down detritus. Most of us recognise mushrooms and toadstools – the fruiting bodies of many fungi – but we are less familiar with the huge numbers of wind-borne spores that they produce. Should the spores land in a suitable location, a complex mat of hyphae (threads that form the mycelium) then spreads underground, or through other substrata, using enzymes to digest organic matter and promote further growth. Mostly, the mycelium is also a mystery to us, but we know that the fruiting bodies must have grown from something because they don’t have roots. We can only speculate on how the fascinating life cycle of fungi evolved [1] and how the hyphae became organised for their various functions, including the rapid growth of fruiting bodies.

Last week, two unusual mushrooms appeared overnight on our lawn. They were white, with white spore-bearing gills and each appeared to grow from a bag-like structure around the base of the stem. They intrigued me sufficiently to pick one and take photographs of it (see below). Like many of us, I am aware that some mushrooms are highly toxic [1], so I treated the specimen I picked with caution. Fortunately, our local garage has a free supply of plastic gloves to prevent contact between hands and petrol, and I donned some of these (previously purloined for use in the age of COVID-19) to avoid direct contact. Even so, I washed my hands several times when I came back into the house (also a COVID-19 habit) as I was sure there was a possibility it was one of the deadly forms [1].

I needed help with identification and put the images on the Facebook page of the British Mycological Society. Fortunately, one of the members, Geoffrey Kibby, a well-known expert, suggested that my mushroom might be a specimen of Leucoagaricus leucothites that is common in lawns and which may cause gastrointestinal upsets in some humans, but is considered edible by others [2]. It seems I was being over-cautious.

Being a romantic, I was fascinated by the common name of “our” mushroom - the white dapperling – and that started me thinking once again about the common names that we give organisms [3]. Fungi are a rich source of such names and some are wonderfully descriptive, as a scan of any field guide will show. Some common names are connected to folklore, as mushrooms and toadstools have always fascinated us, and we have projected all manner of attributes to different types. As a result, common names are easy to remember and are used when we chat about mushrooms and toadstools, although many species are known only by their official name. Here is an abbreviated list taken from two of the best guides [4,5] together with the Latin binomial for each (some of which change from time to time) [3]:

Old Man of the Woods – Strobilomyces floccopus

Slippery Jack – Suillus luteus

Penny Bun – Boletus edulis

Slimy Spike Cap – Gomphidius glutinosus

Caesar’s Mushroom – Amanita caesarea

Death Cap – Amanita phalloides

Destroying Angel – Amanita virosa

The Blusher – Amanita rubescens

Stinking Parasol – Lepiota cristata

Amethyst Deceiver – Laccaria amethystea

Tawny Funnel Cap – Clitocybe flaccida

Clustered Tough Shank - Collibia confluens

Poached Egg Fungus – Oudemansiella mucida

Herald of the Winter – Hygrophorus hypothejus

Curry-scented Milk Cap – Lactarius camphoratus

The Charcoal Burner – Russula cyanoxantha

The Sickener – Russula emetica

Poison Pie – Hebeloma crustuliniforme

Lawyer’s Wig – Coprinus comatus

Fairies’ Bonnets – Coprinus disseminatus

Weeping Widow – Lacrymaria velutina

Chicken of the Woods – Laetiporus sulphureus

Witches’ Butter – Exidia plana

Jelly Babies – Leotia lubrica

Great names for fascinating organisms, aren’t they?

P.S. I wonder where the fruiting body that produced the spores that resulted in "our" white dapperlings was located?

[1] https://rwotton.blogspot.com/2014/02/mushrooms-tasty-hallucinogenic-and.html

[2] https://www.zoology.ubc.ca/~biodiv/mushroom/L_leucothites.html

[3]

https://rwotton.blogspot.com/2017/05/latin-binomials-and-beauty-of-common.html

[4] Stefan Buczacki (1992) Mushrooms and Toadstools of Britain and Europe. London, HarperCollins.

[5] Roger Phillips (1994) Mushrooms and other fungi of Great Britain and Europe. London, Macmillan.

The amazing three-toed sloth

There are two common types of sloth – the three-toed (below) and the two-toed – living in Central and South American forests. Three-toed sloths do not move around as widely as their distant relatives [1] and they usually have a greenish colouration. This was described by Charles Waterton in his pioneering observations of sloths in their natural environment made at the beginning of the Nineteenth Century [2]:

I observed, when he was climbing, he never used his arms both together, but first one and then the other, and so on alternately.. ..His fur has so much the hue of the moss which grows on the branches of the trees, that it is very difficult to make him out when he is at rest.

If Waterton had a microscope, he would have observed that the green colouration resulted from algae growing over the surface of the hairs making up the coat; hairs of the three-toed sloth having [3]:

..irregular transverse cracks that increase in number and size with age. A wide variety of organisms have been reported to occur in the grooves and cracks of sloth hair.. ..the greenish color of the hair.. ..is due to green algae, which in most cases have been identified as Trichophilus welckeri.. ..The hair of the three-toed sloth absorbs water like a sponge, perhaps making it an even more ideal habitat for algae, and prompting speculations that the sloth perhaps receives nutrients from the alga via diffusion along the spongy outer portion of the hairs, followed by absorption into the skin. The algae growing on sloth hair may also produce exopolymeric substances that may give the hair a desired texture or allow beneficial bacteria to grow.

This is speculation, but we know that exopolymers are ubiquitous and have many important roles to play, both for the organisms that exude them and in the wider environment [4]. It is likely that they are a significant part of the sloth fur ecosystem.

Algae are not found abundantly in the fur of very young sloths and they are probably acquired during close contact with the mother [3]. It has been suggested that the relationship of Trichophilus welckeri with the sloth is mutualisitic [3]; the alga gaining nutrients that are released by the microbial community on the hairs and also befitting from being carried up into the canopy where light is more available for photosynthesis. The sloth grazes this good quality food resource (it is rich in lipids [1]) during grooming and it also benefits from the green colouration that the algae convey to the fur, acting, as Waterton pointed out, as a form of camouflage.

Renowned as slow movers, sloths have a very low metabolic rate that enables them to survive on a poor-quality diet, but considerable energy is expended in climbing down to the ground to defecate and in climbing back up to the canopy, with the sloth made heavier by the water retained in the fur. Three-toed sloths defecate on the ground in scrapes that they prepare with their hind claws, while clinging to vines or other trailing vegetation with their fore limbs. The mass of faecal pellets is then covered with leaves and the sloths begin their steady climb back to the canopy [5]. The sloths are vulnerable when on, or close to, the ground and the greatest mortality of sloths occurs during this activity. As the diet is poor and the rate of metabolism low, visits to defecate are approximately weekly, but why has the three-toed sloth evolved this habit, when two-toed sloths defecate from the canopy? The advantage to the sloth may be that egesta provide a fertiliser for their preferred trees (each three-toed sloth not moving far from a few favoured trees); the possibility of using the latrine as a form of marking or communication; and the opposite effect of hiding odours from predators that may hunt from the ground and be more mobile than the sloths [1].

So far we have seen an association between algae, micro-organisms and sloths, but the fur also harbours several types of invertebrates, one of which is found only on sloths and has a remarkable life cycle adapted to the behaviour of its host. This is the moth Cryptoses cholopei (above). Gravid females collected from sloths laid their eggs on any solid surface but the larvae that hatched did not feed on sloth hair, or on leaves, but only on sloth dung [5]. During sloth defecation, female moths descend to the faecal mass to lay their eggs and larvae emerge to feed exclusively on the faecal pellets. They do so within silk tubes [5] that bind pellets and which also form a cocoon for pupation. Adult moths then emerge to fly up into the canopy and locate a three-toed sloth and complete the life-cycle. Cryptoses gains from the relationship through:

(i) the enhancement of oviposition-site location (that is, being carried by the sloth to the next fresh dung pile), (ii) the use of the sloth as a refuge from avian predators, and, perhaps, (iii) the enhancement of its diet with secretions of the host or associated algae [5].

The second explanation may not be completely true, as jays have been seen feeding on the fur of sloths [6], but there are a wide variety of other invertebrate colonists that may provide food for the birds. Indeed, the ecosystem within the fur of the three-toed sloth is a complex one, consisting of algae, micro-organisms and protozoans, a wide range of invertebrates and the exudates of the sloth and of all the other members of the community. Among the micro-organisms are fungi that digest detritus, including dead moths, and which, in turn, release nitrogen-rich nutrients that can be utilised in growth by bacteria and algae. The fungal community is diverse [7] and some of the fungi living in sloth fur produce antibiotics that may affect the rest of the community living there. As Higginbotham and colleagues write [7]:

The high abundance and diversity of fungi associated with sloth hair, coupled with their bioactivity, may speak to a biological importance to sloths that is yet unexplored.

As if watching sloths is not wonderful enough, their exobiology presents an extraordinary story. How fascinated Charles Waterton would have been if the sloth fur ecosystem had been known to him. Isn't Natural History amazing? Just think of how much more we have yet to learn about the world around us.

[1] Jonathan N. Pauli, Jorge E. Mendoza, Shawn A. Steffan, Cayelan C. Carey, Paul J. Weimer and M. Zachariah Peery (2014) A syndrome of mutualism reinforces the lifestyle of a sloth. Proceedings of the Royal Society B 281: 20133006.

[2] Charles Waterton (1825) Wanderings in South America, the North-west of the United States, and the Antilles, in the years 1812, 1816, 1820, and 1824. London, J. Mawman.

[3] Milla Suutari, Markus Majaneva, David P. Fewer, Bryson Voirin, Annette Aiello, Thomas Friedl, Adriano G. Chiarello and Jaanika Blomster (2010) Molecular evidence for a diverse green algal community growing in the hair of sloths and a specific association with Trichophilus welckeri (Chlorophyta, Ulvophyceae). Evolutionary Biology 10:86

[4] Roger S. Wotton (2005) The essential role of exopolymers (EPS) in aquatic systems. Oceanography and Marine Biology: An Annual Review 42:57-94.

[5] Jeffrey J. Waage and G. Gene Montgomery (1976) Cryptoses cholopei: a coprophagous moth that lives on a sloth. Science 193:157-158.

[6] Kelsey D. Neam (2015) The odd couple: interactions between a sloth and a brown jay. Frontiers in Ecology and the Environment 13:170-171.

[7] Sarah Higginbotham, Weng Ruh Wong, Roger G. Linington, Carmenza Spadafora, Liliana Iturrado and A. Elizabeth Arnold (2014) Sloth hair as a novel source of fungi with potent anti-parasitic, anti-cancer and anti-bacterial bioactivity. PLOS ONE 9:e84549.

Fungi and Art

As a student of Zoology and Botany in the 1960s, much time in practical classes was spent making drawings; either of dissected animals, or of preparations of plants made by sectioning and staining. This was a practice little changed from the heyday of Natural History during the Nineteenth Century.

One of the great illustrators of that period was Philip Henry Gosse, and his son, Edmund, described his zealous approach [1]:

I have often known him return, exhausted, from collecting on the shore, with some delicate and unique creature secured in a phial. The nature of the little rarity would be such as to threaten it with death within an hour or two, even under the gentlest form of captivity. Anxiously eyeing it, my father would march off with it to his study, and, not waiting to change his uncomfortable clothes, soaked perhaps in sea-water, but adroitly mounting the captive on a glass plate under the microscope, would immediately prepare an elaborate coloured drawing, careless of the claims of dinner or the need of rest. His touch with the pencil was rapid, fine, and exquisitely accurate.

Unfortunately, my efforts were nowhere near the equal of those produced by Henry Gosse and his meticulous illustrations resulted from talent, practice and the training that he received as a boy from his father, a professional painter of miniatures. Edmund describes Henry's work as having:

..no distance, no breadth of tone, no perspective; but a miraculous exactitude in rendering shades of colour and minute peculiarities of form and marking. In late years he was accustomed to make a kind of patchwork quilt of each full-page illustration, collecting as many individual forms as he wished to present, each separately coloured and cut out, and then gummed into its place on the general plate, upon which a background of rocks, sand, and seaweeds was then washed in. This secured extreme accuracy, no doubt, but did not improve the artistic effect, and therefore, to non-scientific observers, his earlier groups of coloured illustrations give more pleasure than the later.

I have been fortunate to see some of Gosse's original work [2] and it certainly commands admiration. For Henry Gosse, illustrations (an example of which is shown above) were for a purpose other than art, although he painted watercolours of landscapes during old age, purely for his own interest.

Students today must find it strange that we spent so much time drawing, and Gosse may well have appreciated the digital techniques available now for capturing images, whether in situ, or by using light, or electron, microscopes. Although I accept that my draughtsmanship is poor, and I lack the tenacity and endurance of Henry Gosse, I do enjoy creating something "artistic" from Natural History. One of the more successful attempts comes from collecting fungi and making spore prints (three examples being given below). Although the fungi lose their lustre rapidly, spore prints can be preserved using artist's fixative and they provide a pleasing record of solitary walks in local fields and woods [3].

[1] Edmund Gosse (1896) The Naturalist of the Sea-Shore: The Life of Philip Henry Gosse. London, William Heinemann.

[2] http://www.rwotton.blogspot.com/2015/01/brilliant-illustrations-of-organisms.html

[3] http://www.rwotton.blogspot.com/2014/10/solitary-walks-in-nature.html

The Natural History of the Unmentionable

A Natural History of the Unmentionable is the sub-title of Nicola Davies’ book Poo, ¹ written for a young audience, but also an interesting read for adults. Nicola has a degree in Zoology from Cambridge University and her book carries this quote on the dust cover:

However you look at it, poo is probably the most useful stuff on Earth. It comes in all shapes and sizes and every animal has its own special sort. Find out what it’s for, where it goes, what we can learn from it and lots more in this lively and fascinatingly informative natural history book. You’ll never think of poo in the same way again!

I’m sure readers of her book never will think of poo in the same way.

We are conditioned from an early age to think that faecal matter is unpleasant and offensive and I, too, feel this way about human and pet excrement, especially as it is a means of spreading harmful bacteria and parasites. Although very young children can gain delight in their excreta, and stools were pored over by generations of physicians for clues of illness or state of mind, I’m very much of the view that the WC is essential in removing the stuff as quickly as possible. However, we seem to carry over our distaste of human and pet excreta to those produced by all animals, despite the considerable importance of this matter in the cycling of nutrients. Interestingly, faeces are also little studied by scientists, who conduct many investigations of feeding in animals but, like all of us, tend then to lose interest in what happens to the material that results from feeding, other than that which is absorbed and used for growth. There are, however, exceptions to this general rule.

We know that spreading faeces on land improves the growth of crops, and farmers are not put off by muck, as they know its value. There are also many examples of using excreta from livestock in gardening, especially to supply nutrients for growing roses or rhubarb. It is not just the rich supply of nutrients, but the way that these are released over time, as the muck becomes broken down and rain percolates the rich supply of nitrogen etc. into the soil. We use the same approach when applying compost produced either from kitchen waste, lawn mowings, trimmings from garden plants, etc. Have you ever wondered what happens when you add material to your compost heap? We know it decomposes, but what are the changes it undergoes?

The first step in breakdown is provided by fungi and bacteria, often associated with the material we add, but found in abundance in compost heaps. Fungi break down resistant materials such as cellulose and invade plant tissues, as well as growing over their surface; while bacteria become attached, often forming films, and these micro-organisms continue the break down of the plant remains. Animals like earthworms and many other types of invertebrates, some of them tiny, are very numerous in our compost heaps, where they feed on the decaying remains. The main source of nutrients for these animals is not plant matter but the attached micro-organisms and these are digested, leaving materials that are little affected by digestion. These are excreted as faecal pellets and masses - in huge numbers. The mature compost heap can thus be said to consist of largely of the faeces of various animals and plant material that is difficult to degrade. The latter provides a means of improving the texture of soils, especially clays, while the former is the source of nutrients. Faecal masses, such as those produced by earthworms, break apart quickly, but the pellets produced by other animals remain intact for much longer.  Pellets are thus a natural and small-sized analogue of the pelletised fertilisers sold in garden shops.

What goes on in our compost heap is, of course, a microcosm of what occurs more widely in Nature. When going on walks, we notice the droppings of farm animals like cows and sheep and the droppings of rabbits and deer, each having a characteristic form. Trackers following game recognise the faeces of their quarry and we use the appearance of droppings to monitor the numbers of otters, for example, noting whether they have been excreted recently. We are also familiar with bird droppings which, as solid and liquid excreta are mixed before being expelled (unlike many animals), are not usually formed into pellets. The same, of course, can be said for cows, but their loose droppings result from their particular gut structure, with incomplete removal of moisture and no effective means of compression before expulsion. What we don’t see are all the faecal pellets of invertebrates, as these are small and also blend in with the surroundings, so microscopic examination of soil surfaces is required before we see the extent of pelletisation. With the naked eye, we may notice the frass produced by larvae that bore into fruits and we may see the droppings of insects that live in silk enclosures, but that’s about it. The pelletisation is not only of advantage to the animal, in allowing the uptake of nutrient-rich fluids by compression of material in the hind-gut. Forming the waste into pellets ensures that micro-organisms surviving passage through the gut are packed tightly together with the substrates on which they act, with the additional colonisation by both bacteria and fungi once the pellets are excreted. Their action allows the slow release of nutrients that are then available to the plant community, just as in the application of garden compost.

This is just a small insight into the importance of faecal pellets and masses and there are many examples given in Poo ¹ (faecal matter from aquatic animals will also feature in a future blog post). I agree with Nicola Davies that we should not be upset by mention of the stuff, but recognise that it is an essential feature of Natural History - and of natural ecosystems.

¹ Nicola Davies (2004) Poo: A Natural History of the Unmentionable. London, Walker Books. With illustrations by Neal Layton.