The Colours of Animals is a zoology book written in 1890 by Sir Edward Bagnall Poulton (1856–1943). It was the first substantial textbook to argue the case for Darwinian selection applying to all aspects of animal coloration. The book also pioneered the concept of frequency-dependent selection and introduced the term "aposematism".
The book begins with a brief account of the physical causes of animal coloration. The second chapter gives an overview of the book, describing the various uses of colour in terms of the advantages it can bring through natural selection. The next seven chapters describe camouflage, both in predators and in prey. Methods of camouflage covered include background matching, resemblance to specific objects such as bird droppings, self-decoration with materials from the environment, and the seasonal colour change of arctic animals. Two chapters cover warning colours, including both Batesian mimicry, where the mimic is edible, and Müllerian mimicry, where distasteful species mimic each other. A chapter then looks at how animals combine multiple methods of defence, for instance in the puss moth. Two chapters examine coloration related to sexual selection. Finally Poulton summarizes the subject with a fold-out table including a set of Greek derived words that he invented, of which "aposematic" and "cryptic" survive in biological usage.
The Colours of Animals was well received on its publication, although the book's support for sexual selection was criticised by Alfred Russel Wallace, and its Darwinism and critique of Lamarckism were attacked by Edward Drinker Cope. Wallace liked Poulton's experimental work but was critical of his opinions on sexual selection. The Neo-Lamarckian Cope criticised Poulton's support for Darwin but liked the book's many observations of animal coloration. Modern biologists respect Poulton's advocacy of natural selection and sexual selection, despite the lack at the time of an adequate theory of heredity, and his recognition of frequency-dependent selection.
Book
Approach
Evidence for natural selection
Poulton explains in his Preface that
Evidence for sexual selection
Poulton strongly supports Darwin both on the general theme of natural selection, and on the power of sexual selection in species which are sexually dimorphic (where, usually, the male is showier than the female):
Poulton knew his view was controversial, but believed he was winning the argument:Poulton, 1890. p 286.
Frequency-dependent selection
In The Colours of Animals, Poulton introduced the concept of frequency-dependent selection (selection based on how abundant a form is) in the context of a polymorphism which he argued would otherwise soon vanish:Poulton, 1890. pp 46–47.
Mimicry and aposematism
The basic concept of warning coloration (aposematism, like the black and yellow pattern of a wasp) is approached very simply:
In the next paragraph Poulton ties aposematism to mimicry as follows:
Poulton introduced the term aposematism with the words:
Contents
The book's structure emphasises the extent to which Poulton, like Darwin, relied on a mass of evidence, mainly from insects, to make his case:
Chapter 1 The Physical Cause of Animal Colours.
Poulton introduces absorption, scattering, colour due to "thin plates" (structural coloration), diffraction and refraction.
Chapter 2 The Uses of Colour.
The effects of natural selection in creating or destroying colour are discussed. Colour can be non-significant, e.g. directly useful for absorbing heat, Poulton argues, but "By far the most widespread use of colour is to assist an animal in escaping from its enemies or in capturing its prey; the former is Protective, the latter Aggressive [resemblance, i.e. camouflage]."Poulton, 1890. p 19 The topics of mimicry, warning coloration, and sexual selection are introduced.
Chapter 3 Protective Resemblances in Lepidoptera.
Poulton distinguishes "special" from "general" resemblances, meaning mimicking a specific object "of no interest to its enemies", or just harmonising "with the general artistic effect of its surroundings", giving examples from moth caterpillars found in England such as the peppered moth and the brimstone moth.
Chapter 4 Protective Resemblances in Lepidoptera (continued), Dimorphism, Etc.
The privet hawkmoth caterpillar is used as an example of "general resemblance". Dimorphism, where caterpillars of a species are sometimes green, sometimes brown, is discussed. The delicacy of larvae is given as a reason for their "wonderful concealment": one touch from a predator "being practically fatal". The resemblance of Kallima and some moths to dead leaves is examined.
Chapter 5 Protective Resemblances In Vertebrata, Etc.
The camouflage of snakes, female birds that "undertake the duty of incubation", birds' eggs, mammals, fish, and marine molluscs is briefly covered.
Chapter 6 Aggressive Resemblances — Adventitious Protection.
The camouflage of predators including lizards, angler fish, mantises including Hymenopus bicornis and the bird-dropping spider is described. "Adventitious protection", making use of materials from the environment, is illustrated with examples such as the decorator crabs and caddis fly larvae, which build tubes "of grains of sand, small shells (often alive), vegetable fragments".Poulton, 1890. p 77
Chapter 7 Variable Protective Resemblance in Vertebrata, Etc.
The ability of animals including fish, lizards and frogs to change their colours quickly is discussed. The changing of the pelage of arctic animals is attributed to the indirect effect of the change in temperature, i.e. a physiological response not a simple physical effect.
Chapter 8 Variable Protective Resemblance In Insects.
Poulton describes in detail experiments demonstrating that moth pupae take on the colour of the background experienced earlier by the larvae. He conducted experiments in Aglais urticae, finding that pupae took the colour of the surroundings, and demonstrating extra-ocular light and color perception.
Chapter 9 Protective Resemblances in Lepidoptera (continued).
Poulton discusses the metallic appearance of insect pupae, which he says is the reason for the name "chrysalis". He rejects the (Lamarckian) view of the "origin of colour, by the direct influence of environment accumulated through many generations", which he agrees is "a very tempting conclusion", because of "clear evidence that the medium of the nervous system was necessary.Poulton, 1890. p 155
Chapter 10 Warning Colours.
The conspicuous warning colours of many insects, skunks, snakes and salamanders are discussed. "It must have been obvious to any one interested in natural history that the insects met with during a walk in summer may be arranged in two great groups: ... difficult to find ... and ... startling colours and conspicuous attitudes"Poulton, 1890. p 159 The association of warning with "nauseous or dangerous" animals is identified. The idea that warning coloured animals must be scarce relative to palatable ones is mentioned, along with the reason why different animals use the same warning colours.
Chapter 11 Warning Colours (continued).
Poulton discusses the relationship of colours used for sexual selection and for warning, and continues the discussion of warning with many examples, including Müllerian mimicry, noting that this can both make a pair of distasteful species converge in appearance, and make a group of such species all resemble each other.
Chapter 12 Protective Mimicry.
The chapter looks at Batesian mimicry (where the mimic is edible) in both tropical butterflies and English moths, beginning "We now approach one of the most interesting aspects of our subject".
Chapter 13 Protective and Aggressive Mimicry.
Poulton gives examples of mimicry in other insect groups, remarking the "very imperfect" resemblance of bee hawk-moths to bees, which totally failed to "impose on" a lizard, but noting that the much more convincing mimicry of the hornet clearwing moth was treated with extreme caution by an inexperienced lizard.
Chapter 14 The Combination of Many Methods of Defence.
The chapter describes animals including the puss moth caterpillar which combines a threatening display with camouflage and the ability to eject an irritant fluid for protection. Poulton also discusses the lobster moth caterpillar.
Chapter 15 Colours Produced by Courtship.
Poulton discusses sexual selection in birds, butterflies and moths, and spiders, which he treats as another process alongside but supordinate to natural selection, with arguments against the views of Alfred Russel Wallace. He notes that it was remarkable that biological research since Darwin had focussed mainly on comparative anatomy and embryology, whereas Darwin himself was interested in "questions which concern the living animal as a whole", and observes that there are "comparatively few true naturalists", as opposed to "anatomists, microscopists, systematists, or collectors".Poulton, 1890. pp 286–287
Chapter 16 Other Theories of Sexual Colouring.
In this chapter, Poulton looks at "the causes which Mr. Wallace and other writers believe to have been efficient in producing sexual colouring", such as the principle of "recognition marking". Poulton uses the example of the satin bowerbird as evidence for an aesthetic sense.
Chapter 17 Summary And Classification.
Poulton sums up his views with a fold-out table of "The Colours of Animals Classified According to Their Uses". His category names derived from Greek include the now widely used 'aposematic' and 'cryptic'.
Reception
On first publication in 1890
Wallace in Nature
The co-discoverer of natural selection Alfred Russel Wallace, reviewing Poulton in Nature, was interested by Poulton's observations on thin films producing iridescence: "In some cases dried insects lose some of their metallic colours, but these reappear when the specimen is dipped in water." However, Wallace objected to Poulton's suggestion that arctic birds and mammals are white to reduce heat loss by radiation, for which he argued there was no evidence in favour, while a thicker "covering, such as actually occurs in all arctic animals" would reduce heat loss effectively, and could be observed to do so.
Wallace was enthusiastic about Poulton's experimental work on how butterfly larvae vary their coloration according to the background, admiring "a number of ingenious experiments" in which Poulton illuminated the insects in light of one colour or another, causing reliable colour changes which could not be direct, like photography, but had to be mediated by the animal's nervous system:
In some cases even the cocoons spun by the larvæ are modified by the surrounding colours; and still more curious changes are effected in the larva itself when ... the same species feeds on several plants having differently-coloured leaves. Even the presence of numerous dark twigs has been shown to cause a corresponding change of colour in the larva of the peppered moth (Amphidasis betularia)."
Wallace's main criticism, occupying half his lengthy review, was of Poulton's acceptance of sexual selection. He begins by stating "Mr. Poulton fully accepts Darwin's theory of female choice as the source of the greater part of the brilliant colour, delicate patterns, and ornamental appendages that exist among animals, and especially among birds and insects." Wallace then cites Poulton on the courtship behaviour of spiders:
"'The female always watches the antics of the male intently, but often refuses him in the end, 'even after dancing before her for a long time.' Such observations strongly point towards the existence of female preference based on æsthetic considerations'"