A Biology Lesson From Winnie-the-Pooh: Crypsis and Masquerade

'It's like this,' [Pooh] said. 'When you go after honey with a balloon, the great thing is not to let the bees know you're coming. Now, if you have a green balloon, they might think you were only part of the tree, and not notice you, and if you have a blue balloon, they might think you were only part of the sky, and not notice you, and the question is: Which is most likely?'

‘Wouldn't they notice you underneath the balloon?' [Christopher Robin] asked.

'They might or they might not,' said Winnie-the-Pooh. 'You never can tell with bees.' He thought for a moment and said: I shall try to look like a small black cloud. That will deceive them'

'Then you had better have the blue balloon' [Christopher Robin] said: and so it was decided…

…Winnie-the-Pooh went to a very muddy place that he knew of, and rolled and rolled until he was black all over; and then, when the balloon was blown up as big as big, and you and Pooh were both holding on to the string, you let go suddenly, and Pooh Bear floated gracefully up into the sky'

(Milne, 1926)

Still from The Many Adventrures of Winnie-the-Pooh

(Source: Disney Image by Disney)

What Winnie-the-Pooh (or the author A. A Milne I assume) probably did not realise was that Pooh was using two different types of mimicry when he made his feeble attempts to approach the bees nest and steal their honey unnoticed. In having his balloon blend in with the surroundings (the blue sky) he used crypsis. By covering himself in mud to try and look like an intimate object that would normally be in a sky (a dark cloud) he used masquerade. Unfortunately for Pooh, his skills at mimicry left quite a bit to be desired! In the animal kingdom, this is far from the case.

Animals that use crypsis don’t always have it as easy as Pooh did. In Pooh’s case, the sky was one colour and all he had to do was match that colour. A similar case would be of a green aphid blending into its background of a green leaf or a polar bear blending into the snow and ice. Not all environments are that uniform though. Animals can live in habitats that vary greatly in colour and can also vary from season to season proving crypsis to be difficult. An example pointed out by Allen and Cooper (1985) is the common meadow grasshopper Chorthippus parallelus found in grasslands in Europe. There are many morphs of this species that all appear to represent different sections of the background environment (pictured below) (Allen & Cooper, 1985).

(A)          Purple morph of the meadow grasshopper Chorthippus parallelus

(Source: Adur Nature Notes 2005. Image by Unknown)

(B)          Brown morph of the meadow grasshopper Chorthippus parallelus

(Source: naturephoto-cz.com. Image by Krasensky)

(C)          Purple, green and brown morph of the meadow grasshopper Chorthippus parallelus

(Source: Wyre Forest Blog. Image by Unknown)

(D)          Green morph of the meadow grasshopper Chorthippus parallelus

(Source: Natural History Museum. Image by Palmer)

(E)           Green and white morph of the meadow grasshopper Chorthippus parallelus

(Source: Lound Bird Club. Image by Warne)

An alternative to crypsis is masquerade. In masquerade, organisms copy an object that would be of no interest to their predator (or their prey) despite being obvious to them. This, unlike crypsis, counts on the fact that the predator (or prey) actually sees the individual but mistakes it for something else. Some examples of prey escaping detection are butterflies that look like dead leaves, or caterpillars that resemble bird droppings (Allen & Cooper, 1985). My personal favourite example of a predator hiding in order to capture is the carnivorous caterpillars of Hawaii (Eupithecia orichloris) which imitate sticks and wait for an unsuspecting fly (or similar sized insect) to venture onto the “branch” and become their next meal (Montgomery, 1982). This strategy is also used by prey avoiding predation (Allen & Cooper, 1985).

Anaea archidonia butterfly

(Source: Personal Documents. Image by Summers)

Papilio demoleus caterpillar

(Source: Wildlife Junior Journal. Image by Payne)

In some cases it is hard to determine whether an organism is being masquerading or being cryptic. If the object that the organism is masquerading as is abundant enough it may be considered to be cryptic. Returning to A.A Milne’s example, how many little black clouds would there need to be before our little friend Pooh goes from masquerading as a cloud to blending into a background of clouds and being cryptic? Or else, how many stones would there need to be in an area before stone grasshoppers (pictured below) are being cryptic?

Stone Grasshopper from Namibia

(Source: What’s That Bug? Image by Grimfoot)

References

Allen, J. A. & Cooper, J. M., 1985. Crypsis and masquerade. Journal of Biological Education, 19(4), pp. 268-270.

Disney, n.d., Still from The Many Adventrures of Winnie-the-Pooh, photograph, viewed 22 April 2014

<http://video.disney.com/watch/climb-a-tree-4bb39d8294da5a8833003b15>

Grimfoot, 2009, Stone Grasshopper from Namibia, photograph, viewed 22 April 2014

< http://www.whatsthatbug.com/2009/11/30/stone-grasshopper-from-namibia/>

Krasensky P, n.d., Brown morph of the meadow grasshopper Chorthippus parallelus, photograph, viewed 22 April 2014

< http://www.naturephoto-cz.com/chorthippus-parallelus-photo_lat-4538.html>

Milne, A. A., 1926. Winnie-the-Pooh. 1st ed. London: Methuen & Co. Ltd..

Montgomery, S. L., 1982. Biogeography of the Moth Genus Eupithecia in Oceania and the evolution of ambush predation in Hawaiian caterpillars. Entomologia Generalis, 8(1), pp. 27-34.

Palmer, G, n.d., Green morph of the meadow grasshopper Chorthippus parallelus, photograph, viewed 22 April 2014

< http://www.nhm.ac.uk/nature-online/species-of-the-day/biodiversity/climate-change/chorthippus-parallelus/>

Payne, JA, n.d., Papilio demoleus caterpillar, photograph, viewed 22 April 2014

< http://www.nhptv.org/wild/karnereasterntigerswallowtail.asp>

Purple, green and brown morph of the meadow grasshopper Chorthippus parallelus, 2013, photograph, viewed 22 April 2014

< http://www.wyreforest.net/wyreblog/2013/08/10/meadow-grasshopper-chorthippus-parallelus/_mg_2693-chorthippus-parallelus-meadow-grasshopper-franks-clearing-dowles/>

Purple morph of the meadow grasshopper Chorthippus parallelus, 2005, photograph. Viewed 22 April 2014

< http://www.glaucus.org.uk/July2005.html>

Summers, KM, 2014, Anaea archidonia butterfly, photograph, viewed 22 April 2014.

Warne, M, 2011, Green and white morph of the meadow grasshopper Chorthippus parallelus, photograph, viewed 22 April 2014

< http://www.loundbirdclub.com/wildlifesightings2011.htm>

The History of Müllerian Mimicry Part 2: How far we have come

If I have seen further it is by

standing on the shoulders of giants.

~ Isaac Newton ~

Since Friz Müller first attempted to explain the phenomenon of two poisonous or unpalatable species mimic each other there has been a considerable amount of research into the topic. As scientists have explored the relationships that mimics have with each other and their predators, they have been able to build on Müller’s ideas. Unfortunately, Müller has also been found to be wrong in some cases (which is understandable considering he made these claims 135 years ago!). Never the less, his contributions to the topic have not gone unnoticed and this phenomenon is still commonly referred to as Müllerian mimicry.

Last week, I posted a general explanation of Müller’s model he put forward. In his model he assumed that animals need to learn to avoid unpalatable species and that, in learning to avoid them, they eat a fixed amount of them before being turned off them all together. Let’s see how far research has come since then.

Do predators really need to learn to avoid prey? 

Müller’s first proposition was that animals need to learn to avoid prey that tastes bad. This is usually the case but not always. In studies concerning some very poisonous prey items (eg. Snakes), predators seem to innately avoid these species (Cladwell & Rubinoff, 1983).  Apart from these few cases, the majority of predators researched have demonstrated that they need to learn by their mistakes before they will avoid an unpalatable prey species. Examples include young birds learning to avoid noxious insects and butterflies in studies by Mostler in 1935 and Chai in 1996 (Cited in Sherratt, 2008) as well as inexperienced lizards attacking unpalatable butterflies before learning to avoid them (Boyden, 1976).

Do predators take a fixed number of prey regardless (independent) of the abundance? 

Müller’s second assumption was that there was a fixed number (n) of individuals a predator would take from a population before it had learnt to avoid it. In Müller’s theory he supposed that the number of individuals taken from two species not mimicking each other would be the same regardless of the size of the population. For example, if there were 100 individuals of one species and 900 individuals from another species that looked different from each other, Müller predicted that both species would have an equal absolute number taken from each population and resulting in the rarer population having a far greater proportion of the total population eaten relative to the more abundant population. Unfortunately for Müller, there has been no research to date showing that a “fixed n” exists (Sherratt, 2008).

Contrary to Müller’s hypothesis, an experimental study by Greenwood et. al. (1989) found that when birds were left to forage for unpalatable prey of two different appearances and in different abundances that the absolute number taken from the two different appearances were different. Greenwood et. al. (1989) randomly placed pieces of pastry flavoured with quinine hemi-sulphate (proven to be unpalatable to the birds) on grid in a ratio of yellow to red of 1:9 and repeated with a ratio of 9:1. Of all the trials conducted, the more common form had a larger absolute number of pieces of pastry eaten by the birds compared to the rarer form. This disproves Müller and confirms that there is not a ‘fixed n’. Never the less, the proportion of rarer forms eaten was larger than the proportion of abundant forms taken and therefore proves it would still be beneficial if these two forms were a mimic of each other. In a way, Müller was right, this development only means that there is no ‘fixed n’ and that the amount of benefit gained by mimicry is less than what Müller originally anticipated (Greenwood, et al., 1989).

Building on Müller’s Ideas: Research into other factors influencing mimicry

As well as the influences of abundance on predation on unpalatable food, there have been many studies that have found or proposed other factors could influence the number of unpalatable prey that will be eaten. Greenwood et. al. (1989) suggested that hungrier birds may be more likely to eat unpalatable if they assessed the cost of eating a bad tasting individual to outweigh the benefit of acquiring food (for instance, I don’t like beetroot and usually avoid it. But if I hadn’t have eaten for a few days, I’m sure I would jump at the chance if I had no other choices). Other possible influences on predation of mimetic species include predators’ ability to distinguish between mimetic species, differences in defences of species that mimic each other (eg having different toxins that make them them unpalatable) which may cause one predator to view both species as distasteful but another predator to view only one of the species as distasteful, and the intensity of unpalatability of the two mimetic species to name a few.

References

Fritz Müller in Brazil, n.d., photograph,  viewed 6 April 2014,
<http://en.wikipedia.org/wiki/File:Fritz-muller-1821-1897.jpg>

Boyden, T. C., 1976. Butterfly palatability and mimicry - experiments with Amevia lizards. Evolution, 30(73-81), pp. 1992-1998.

Cladwell, G. S. & Rubinoff, R. W., 1983. Avoidance of venomous sea snakes by naive herrons and egrets. The Auk, 100(1), pp. 185-198.

Greenwood, J. D., Cotton, P. A. & Wilson, M. D., 1989. Frequency-dependent selection on aposematic prey - some experiments. Biological Journal of the Linnean Society, 36(1-2), pp. 213-226.

Müller, F., 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Transactions of the Entomological Society of London, pp. xx-xxix.

Sherratt, T. N., 2008. The Evolution of Müllerian Mimicry. Naturwissenschaften, 95(8), pp. 681-695.

The History of Müllerian Mimicry

Attempts to explain what is now known as Müllerian mimicry were first made 135 years ago by German biologist Johann Friedrich Theodor (Fritz) Müller. Müller (1879) provided an evolutionary explanation to describe the phenomenon where two unpalatable species exhibit a similar appearance to each other. He was also the first person to present a “formal mathematical model to support an evolutionary hypothesis” (Sherratt, 2008, p. 682).

Müller (1879) hypothesised that if predators were required to learn from experience which prey items were distasteful, that two similarly distasteful prey items would benefit if they displayed similar appearances because this would reduce the number of individuals that die during the process where inexperienced predators ‘learn’ which prey items are distasteful. More specifically, Müller (1897) was saying a predator would only eat a given number of what they thought were a single distasteful species before they learned that they were distasteful regardless of whether it was in fact a single species or two species that mimicked each other (Sherratt, 2008).

Müller's formula explaining how it is beneficial for two poisonous species to have similar appearances (Source: Transactions of the Entomological Society of London. Image: Müller)

Using his proposed formula (pictured right) Müller (1879) put forward an explanation using two theoretical species in a community (Species A and Species B) and a theoretical number of individuals of a particular appearance must be eaten in the population before the predator species learns not to eat them. To put it simply, let’s pretend we are an animal who feeds on butterflies. When you are born you have absolutely no knowledge of what butterflies are good or bad tasting; all you know is that you have to eat butterflies. You eat a few butterflies but then you catch one that tastes revolting. You keep feeding, possibly thinking that it was just a dodgy butterfly. But then it happens again! This is another disgusting tasting butterfly that looks suspiciously similar to the last one that tasted bad.... For arguments sake, let’s say it takes you 5 attempts at eating that type of butterfly before you decide you will never eat a butterfly that looks like that again.

If there are two completely different species of bad tasting butterflies and one (Species A) is pretty small (eg. 2000 individuals) and the other (Species B) is relatively large (eg 10,000 individuals), 1 predator taking the same number of individuals out of both populations will make a larger difference in the smaller population than the larger one. For Species A, if we take into account for the entire population of predators and assume that there are 240 juveniles in the population each taking 5 individuals from a species, that is 1200 members of butterfly Species A that get eaten in one season. That equates to 60% of the population! If we compare that to Species B with 10,000 individuals, the predators still only take 1200 butterflies but it only equates to about 12% of the total population (See Figure 1).

Figure 1. Proportions of individuals eaten from two unpalatable
species that look different (Image: Summers)

Obviously, the larger population has the advantage here, but what if these two species looked similar? If a predator cannot tell the difference between them visually, they only need to remember one type of markings. If they eat one from Species A they will remember it and when they eat one from Species B they will see, what looks like to them, the same animal and avoid it also. This way, one predator only needs to eat five individuals from Species A or Species B and not five individuals from Species A and Species B. That equates to 1200 individuals from Species A or Species B and not 2,400 individuals from Species A and Species B combined.


Müller (1879) goes on to explain that when the predator takes individuals from species A and B thinking they are the same species, that the number of individuals eaten is dependent upon the number of individuals in each species and therefore the proportion taken from each species is e qual. In other words, the predator species will eat 200 individuals from Species A and 1,000 individuals B; 10% of each species’ initial population 

Figure 2. Proportions of individuals eaten from two unpalatable
species that look the same (Image: Summers)

References
Müller, F., 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Transactions of the Entomological Society  of London, pp. xx-xxix.

Sherratt, T. N., 2008. The Evolution of Müllerian Mimicry. Naturwissenschaften, 95(8), pp. 681-695.

Summers, K. M., 2014. Figure 1. Proportions of individuals eaten from two unpalatable species that look different photograph, viewed 31 March 2014.

Summers, K. M., 2014. Figure 2. Proportions of individuals eaten from two unpalatable species that look the same, photograph, viewed 31 March 2014.