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.

Decoration in humans and other animals

A wide variety of animals decorate their outer surface. In a review paper, Graeme D. Ruxton and Martin Stevens [1] have defined a decorator as:

..an organism that (by means of specialist behaviour and/or morphology that has been favoured by selection for that purpose) accumulates and retains environmental material that becomes attached to the exterior of the decorator.

This definition is a bit complicated as it is designed for an audience of scientists, but you get the drift. Ruxton and Stevens then give us some examples, beginning with decorator crabs (below left) that attach all sorts of materials to hooked hairs present over the body of the animal:

Several studies..have found that experimentally altering or removing decoration [from decorator crabs] increased vulnerability to predators.. ..Items used in decoration are often chemically defended plants or sessile animals, and it seems plausible that predators detect the crab but actively avoid attacking because of the repellent smell or taste from the decorations. However, not all decorations provide the animals with chemical defence, and it is likely that decoration often functions through crypsis via background matching, masquerade and/or disruption.

Another type of decoration is seen in insects that use faecal shields, an example being larvae of the tortoise beetle (above right), where faecal pellets are retained on an extension of the body, so that the solidified shield provides cover for attack by predators. The shield acts both in crypsis and as a physical defence [1], isolating the body from potential attacks; other insects use a covering of faecal material directly on the surface of the upper body. However, decoration in insects is not confined to the use of faeces: other components of "backpacks" may be cast skins from moults, or organic, and mineral, grains obtained from the surrounding environment and stuck on to the back by secretions, or held there on hairs extending from the body surface.

Decoration is also used by birds (and I am not including those, like bower birds, that make collections of bright objects remote from the animal itself). To quote Ruxton and Stevens [1]:

In birds, a range of species add substances to their feathers that alter their appearance (termed cosmetic coloration).. Staining of the feathers with soil has been observed in a number of large birds.. ..Both sexes [of the rock ptarmigan] sport all-white plumage at the start of the breeding season, as snow melts this becomes very conspicuous and females moult to produce feathers that appear to offer good camouflage. By contrast, males do not moult immediately, but smear their feathers with soil before later moulting into a brown plumage.

Free-ranging adult bearded vultures..typically have an orange colour on their underparts, neck and head conferred by iron oxide-rich soils.. .. Colour tends to be greater in (socially dominant) females than males and increases progressively from juveniles, to immatures, to sub-adults to adults.

Ruxton and Stevens conclude their review by saying [1]:

Decorating is a particularly diverse activity, and (like tool-use) it is difficult to produce an unambiguous definition that covers all cases effectively.. .. Anti-predator benefits are most commonly postulated, in contrast to humans where decoration functions strongly in social interactions.

Their last sentence set me thinking. Unless one believes in Creation, it is not possible for us to look at the behaviour of our own species without realising that much of it developed as we evolved so successfully away from the rest of the Animal Kingdom. In this post, I describe the origins of human decoration, confining myself to clothes, accessories and make-up, as these best fit the definition given above.

Humans lack a dense covering of hair over the whole body and it is likely that our first use of decoration was by draping ourselves in animal furs that were protective and helped to keep us warm. It could be argued that this enabled early humans to migrate to regions with cooler climates, something that was also facilitated by the discovery of fire, but it is unlikely that animal pelts provided camouflage against predators. Camouflage coverings are certainly important in providing crypsis in warfare and they form an important part of the clothing using by contemporary fighters (below), together with applied face paints. This is analogous to the main use of decoration used by animals but most of our clothing, in addition to its functions of keeping us warm and protected, is used in expressing social status, for mate selection, or for group identity.

Among contemporary costume, the business suit is currently de rigeur for men in many countries and in many walks of life, with only small changes in the design of a jacket and trousers. There is status in having a designer label and this is true also of all clothes, something that conveys both the quality of materials and tailoring, but also exorbitant cost. The expression of wealth in this way is important in Western Society, as is the quantity of items in an individual's collection. Surprisingly, while the business suit represents a work uniform (although casual clothes for men are more varied), women's fashion is based on variety, and it is considered acutely embarrassing to wear an outfit that is identical, or too similar, to that worn by someone else at the same social function. Despite trends in fashion, decoration in women is thus less about uniformity and more about the uniqueness of the individual. Why?

The answer to this question probably lies ancestrally in mate selection. Humans do not have a breeding season and mating can occur at any time through the year. Mate selection is based on genetic factors – the classic notion of handsome men and beautiful women pairing up – but also on decoration. Clothes are an important part of this and initial mate selection is often influenced by clothes, as these convey information about social status and identity, something that is important if mate selection is for the long-term and where breeding is likely. Of course, there are more factors than decoration involved in selection, but it forms an initial signal, with most encounters initiated by men.

In addition to the decoration provided by clothes, there are also accessories, especially used by women, and we all know individuals with a shoe and/or handbag addiction. The most similar parallel to animal decorators comes in jewellery in all its forms. This type of decoration may emphasise status, as in the integration of precious stones, or be used as a symbol of lack of availability, as in wedding rings. Similar forms of decoration are present in many tribal cultures, not just those of the Developed World, and extend to neck rings, necklaces, nose plugs and rings, ear plugs, earrings and many other forms. They are not confined to women either, as they are used by both sexes as indicators of cultures and sub-cultures, something unknown among animals other than humans.

It is ironic that one design of earrings is based on the activity of an animal decorator. Larvae of some caddis flies make cases of stones that are bound together with silk secreted by the insect. This habit has been utilised by jewellers who give larvae semi-precious stones and wait for each earring to be produced [2]. It's the only example I can think of where the activity of one decorator animal is used by another, albeit for a different purpose.

In addition to clothes and accessories, considerable attention is given to enhancing the appearance using paints and powders of various kinds. Use of ochre and ash in face and body colouration is a characteristic of some "primitive" tribal groups, but make-up in Western Culture is usually more subtle, with concentration on the face. As with clothes and accessories, there are variations but, in general, powders are used to enhance the complexion and to hide blemishes, while various products are used to decorate the eyes and lips to provide emphasis. Although men use cosmetics, women are the main users and, as with other forms of decoration, the underlying message is related to mate selection and/or belonging to a social group.  

Just as humans evolved rapidly, so did our use of decoration. It now has many forms and is constantly changing, except in tribal cultures and where national costume, or work customs and uniforms, create an identity. However, we are animals and the origin of our use of clothing, accessories and make-up lies far back in evolutionary time.

[1] Graeme D. Ruxton and Martin Stevens (2015) The evolutionary ecology of decorating behaviour. Biology Letters 11: 20150325.

[2] http://www.rwotton.blogspot.com/2013/11/caddis-flies-earrings-and-evolution

Why does the Comma have a comma?

Buddleia bushes are flowering in our garden and I love their rich scent. It’s not only me that is attracted to the plants, as their dark purple flower spikes are visited by large numbers of bees and butterflies that collect the supplies of nectar provided by the plants. The Buddleia benefits, as pollen is spread by the insects when they gather this “gift”, and the bees and butterflies gain fuel for flight and a high-energy source of food for rearing young in bees. Both groups of insects also use the sugars in nectar as a store; with bees producing honey and butterflies body fat.

As the insects move over the flower spikes, it is easy to look at them closely and the common Peacock and White butterflies have been joined by Commas (Polygonia c-album), which seem plentiful this year. The wings of Commas have a jagged profile and, as with most butterflies, have beautiful colouration on the upper surface of the wings and a brown colour on the under surface, with a pattern resembling bark or lichen. The ragged outline of the wings, and the patterns of their lower surface, are likely to provide protection against predation during rest, when the wings are closed. The butterflies are then camouflaged and look to me like pieces of bark or dead leaves. I say “look to me”, as our perceptions are so much governed by our own senses and we do not know how the butterflies look to their natural predators. We know that the Comma is eaten by birds like great tits,¹ but presumably in greater numbers when the wings are open and the butterflies active.

A feature of the camouflage of the under surface of the wings is the “comma” from which these butterflies gain their common name. The marking varies from species to species, and also within species, but it is a feature of Comma butterflies throughout the Northern Hemisphere. Why do they have this marking? A creationist might argue that it is something for which only God has the answer and, without wanting to sound facetious, creationists may also feel that God created the comma as a talking point and as a means of showing us His omnipotence. An evolutionist would have no difficulty pointing to the selection of mutations that provide the effective camouflage of the under surface of the wings, as the colouration presumably enhances the survival of individuals in which it occurred. The mutations require changes in the pigmentation of individual scales and also of the wing outline, but what were the stages that led to the forms we see today? Does the comma provide any selective advantage, or is it neutral? No-one knows the answers to these questions, nor do we know why the upper surfaces of the wings have their characteristic brightly-coloured patterns. Unfortunately, we are hampered in our inquiry by viewing Nature with human sense organs and from a human perspective. Of course, it’s the only approach we have and that is always worth keeping in mind, especially as humans are so recent in the history of living organisms.

¹ Nylin et al. (2001) Journal of the Lepidopterists' Society 55: 69-73