Biology, images, analysis, design...
|"It has long been an axiom of mine that the little things are infinitely the most important" |
Colour in Aphids, Part 2:
Cryptic coloration, crypsis versus aposematism, and colour polymorphismOn this page: Cryptic coloration Cryptic or aposematic or both Red-green polymorphisms
Given that colour in aphids is a large and fascinating topic (albeit most research is on only a few species), we decided to do the job properly and address this issue as two blogs. Researching last month's blog on aphid colours and aposematism, we noticed a degree of scepticism among some authorities about whether crypsis is an important feature of aphid biology. Presumably this is based on the fact that colonies of some pest species such as (ant-attended) Aphis fabae are rather obvious on the plant. Those of us who venture beyond the lab, and actually try to find the beasties in the field, know that most aphids do their very best to stay concealed - unless of course they have another defense strategy, such as tasting vile, or being defended by aggressive ants...
How does cryptic coloration work?
Given the apparent vulnerability of aphids to predators, one would expect cryptic coloration to be a widely employed strategy. And indeed, as Dixon (1997) points out, most of the aphids that live on leaves are green, whilst those that live on the woody parts of the plant are brownish. This form of colour matching is termed homochromy and is very common with aphids. The first picture below show the superb crypsis of adult winged Hyalopterus pruni on plum leaves. The second picture shows the equally good cryptic coloration of Cinara kochiana on the dying branch of a fallen larch tree.
Note that photographing examples of crypsis is a frustrating affair because, if your subject is good at concealing itself, it will not show up well in your photo! These examples demonstrate not just colour matching but also texture and pattern matching, and all ages of aphids from the youngest nymphs to the adults are cryptically coloured. But this is not always the case.
In some Cinara species there is aposematic coloration in the adults, but cryptic coloration in the nymphs. The first picture below shows three dark metallic green apterae of Cinara confinis with a large group of nymphs which have classic disruptive camouflage coloration.
Similarly, adult alates of the hairy bark aphid Pterocomma pilosum, are strongly striped and very conspicuous, whereas their nymphs are cryptic and often very difficult to spot (see second picture above). It certainly makes sense for aposematic coloration to be delayed until the adult stage if it takes time for the aphid to sequester sufficient chemicals from the host to make it distasteful or poisonous. Provided predators do not come to associate the very conspicuous (and presumably distasteful) adult with a nearby group of much more palatable nymphs, then those nymphs will benefit from both reduced predation pressures and by partaking in a nutrient sink with their adult(s).
The mixing together of cryptic and aposematic forms is taken a step further by bark aphids when they form multispecies groups. Both the nymphs and the wingless adults of Pterocomma pilosum are cryptic but they regularly form mixed colonies with the aposematic Pterocomma salicis.
By so doing Pterocomma pilosum would seem to loose any possibility of camouflage on the bark. Perhaps the aposematic 'message' 'rubs off' on the cryptic species, and predators learn to leave the mixed species assemblages alone - or perhaps they only notice the aposematic aphids.
Cryptic or aposematic or both?
The first thing one notices in a close-up picture of Macrosiphoniella absinthii is its dramatic black and white coloration, especially when one finds a large colony. Given that the chemicals from the foodplant (absinthe) are likely to be distasteful, this would seem an obvious case of aposematic coloration for defensive purposes.
However, if we step back a bit, we realise it could be a form of crypsis: either pattern blending in amongst the flower head, or disruptive coloration where a block of highly contrasting coloration and sharp boundaries prevent a predator from detecting or recognizing the preys outline (Caro, 2009). Or could it have a dual function as Ruxton (2002) suggested for zebra stripes - cryptic when aphids are amongst the flower heads in low light, and aposematic when exposed on the flower heads. We suggested something similar for Tuberolachnus salignus in our August blog.
A striking example of this can be seen in the image (below) sent to us by Christoph Rieckmann, in Germany. Up-close and personal these Tuberolachnus salignus are anything but cryptic, but seen en masse the effect is entirely different.
Image copyright Christoph Rieckmann, all rights reserved
Willink (2013) tackled this issue for the polymorphic granular poison frog (Oophaga granulifera). This frog has multiple colour morphs, which range from a bright red dorsal colour (aposematic) to a green dorsal colour (cryptic) - with everything else in between! Populations of intermediate colours attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. Hence there is a continuum between cryptic and aposematic strategies.
And what about red-green polymorphisms?
Since academic interest in aphid colour has focused almost exclusively on red-green polymorphisms, we thought we ought at least mention them.
In our September blog we reported our discovery of a previously undescribed colour form of the green-striped fir aphid Cinara pectinatae. Once this aphid has found a suitable feeding site, it does not move very much, and is well anchored by means of its strong claws. It relies on its green cryptic coloration (see first picture below) to protect it from predators such as the coal tit (Periparus ater, a passerine bird).
In September this year we found a reddish-brown form (see second picture above) of the same species. These brown forms were just as well camouflaged as the green forms - except they were mimicking buds, rather than needles. The reddish-brown colour may be produced by a carotenoid pigment as in other better known red-green polymorphisms, or it may come from an erythroaphin. The polymorphism between these two forms is presumably maintained by the relative availability of buds and needles - the red form seems to mainly occur in autumn after bud development in the summer.
It has proved more difficult to establish the biological significance of other red-green polymorphisms in situations where the red morph has no obvious cryptic value. The pea aphid Acyrthosiphon pisum (see pictures of green and red form below) has been extensively studied.
The polymorphism appears to be maintained by balanced selection from two predatory species - the predator (the ladybird beetle) Coccinella septempunctata and the (hymenopteran) aphid parasitoid Aphidius ervi. Losey et al. (1997) found that when parasitism rates were high relative to predation rates, the proportion of red morphs increased relative to green morphs. The converse was true when predation rates were high relative to parasitism rates. Detailed laboratory and field studies confirmed that green morphs suffer higher rates of parasitism than red morphs, whereas red morphs are more likely to be preyed on by predators than green morphs are. Quite why there are these differences is less clear.
Colour in the english grain aphid is determined both genetically and in response to environmental factors (Jenkins et al., 1999).
In this case the biological significance of the colour polymorphism of Sitobion avenae is unknown, although seasonal changes occur in the frequency of colour morphs in the field.
Another pest aphid species, the peach-potato aphid (Myzus persicae) has multiple colour forms, from whitish-green, to orange, to red (see picture below). The different colour forms are again determined both genetically and environmentally, and have been linked to various physiological characteristics including susceptibility to insecticides (see for example Kerns et al. 1998).
One feature of aphid populations is that they can 'throw up' aberrant colour forms. The most dramatic colour form we have encountered so far is a golden-yellow form of the aphid Chaitophorus populeti shown below:
Most of the aphids on just this one aspen sucker were yellow patterned with gold. The functional significance of this colour polymorphism is unknown.
Read about aposematic aphid colouration.