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Plant Signaling & Behavior 5:1, 1-6; January 2010; © 2010 Landes Bioscience
Is crypsis a common defensive strategy in plants?
This manuscript has been published online, prior to printing. Once the issue is complete and page numbers have been assigned, the citation will change accordingly.
Speculation on signal deception in the New Zealand flora
Kevin C. Burns
School of Biological Sciences; Victoria University of Wellington; Wellington, New Zealand
Key words: aposomatic colouration, cryptic colouration, herbivory, moa, plant defence
Colour is a common feature of animal defence. Herbivorous
insects are often coloured in shades of green similar to their
preferred food plants, making them difficult for predators to
locate. Other insects advertise their presence with bright
colours after they sequester enough toxins from their food
plants to make them unpalatable. Some insects even switch between cryptic and aposomatic coloration during development.1
Although common in animals, quantitative evidence for colourbased defence in plants is rare. After all, the primary function
of plant leaves is to absorb light for photosynthesis, rather than
reflect light in ways that alter their appearance to herbivores.
However, recent research is beginning to challenge the notion
that colour-based defence is restricted to animals.
Temperate deciduous forests provide what is arguably the most
extraordinary display of colour in nature. Prior to leaf-fall in
autumn, the leaves of many deciduous tree species in Asia, Europe
and North America turn red, leading to brilliantly coloured
landscapes. Once thought to be a by-product of chlorophyll reabsorption prior to leaf abscission, autumn flushes in red leaf
colours are now known to result from the active synthesis of redcoloured pigments.2,3 Although the exact reason for the production of red-coloured pigments prior to leaf-fall is unknown, it has
recently been hypothesized to be a form of defence.4 Aphids are
common phloem-feeding herbivores in deciduous forests, which
disperse from the forest floor into tree crowns in autumn, and the
synthesis of red pigments could signal the timing of leaf fall and
the reduction in the supply of photosynthate.5,6 Although there
are also physiological explanations,7 red leaf colours could be a
reliable signal of unpalatably to herbivores.8
Lev-Yadun and Holopainen9 recently showed that there are
fewer red-coloured deciduous tree species in Europe than in
North America, and they speculate that historical processes
are the cause. During the advance and retreat of glaciers in the
Pleistocene, the European Alps would have hindered the movement of plants and their herbivores in response to long-term
climate change. Mountain ranges in North America run perpendicular to the equator, which would facilitate these migrations.
Therefore, if red leaves are signals to herbivores, geographic differences in leaf pigmentation may be ‘anachronistic’.10 In other
Correspondence to: Kevin C. Burns; Email: [email protected]
Submitted: 10/04/09; Accepted: 10/05/09
Previously published online:
www.landesbioscience.com/journals/psb/article/10236
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words, they may result from historical coevolutionary dynamics between plants and their herbivores, rather than present day
selection pressures alone.
Despite these important insights, our understanding of colourbased defence in plants is in its infancy and progress hinges on
quantitative tests in other parts of the globe. Previous work is
also restricted largely to aposomatic, or warning colours.11 Given
that cryptic colouration is widespread in animals, it might also
be common in plants. Yet we are far from determining if this is
true.
Here, I discuss several New Zealand plant species that seem
to be coloured in ways that would make them difficult for herbivores to locate. I suggest that these plants are anachronisms;
their unusual appearance is the result of selection from flightless browsing birds called moa, which went extinct following the
arrival of humans in New Zealand 750 years ago. I also discuss
the difficulties associated with testing for cypsis in plants and
finish by outlining a methodological approach to test for colourbased defence in plants when the putative herbivores are either
unknown or extinct.
New Zealand Lancewood
Pseudopanax crassifolius (A. Cunn) C. Koch Araliaceae, or New
Zealand lancewood, is one of the strangest looking plants on
Earth (Fig. 1). The primary reason for its peculiar appearance
is that it is strongly heteroblastic, meaning its gross morphology undergoes sudden and dramatic changes during ontogeny.
Although heteroblasty is unusually common in the New Zealand
flora, it is exceptional in P. crassifolius. In fact, it changes in
appearance so completely during ontogeny that Sir Joseph Banks,
the famous botanist that accompanied James Cook on the voyage
of the Endeavour, named the juvenile and adult forms of P. crassifolius as separate species.
After germinating, P. crassifolius seedlings (<10 cm tall) are
immediately unusual. Instead of being green, seedling leaves
are a strange mottled-brown colour. However, once plants reach
approximately 10–20 cm in height, they begin to produce strikingly different-looking leaves. These juvenile leaves are very long,
stiff and narrow. They also produce strange thorn-like dentitions
along their margins, each coinciding with a distinctive patch of
differently coloured leaf tissue. A final morphological transformation occurs once plants grow to approximately three metres in
height, when they begin to produce green, oblong leaves that are
rather ordinary in appearance.
Plant Signaling & Behavior
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down the oesophagus.14 Thorns
that arise from stems, such as
those produced by many species
of Acacia for protection against
large mammals, are ineffective
deterrents to bird browsers and are
correspondingly rare in the New
Zealand flora. In order to deter
bird browsers, plants need other
types of defence.15-20
Fadzly et al.12 found that colour
may have been a critical component of a defensive strategy that
evolved in P. crassifolius to deter
moa browsing. Spectrographic
analyses of seedling leaves from
the perspective of birds indicate
that their mottled brown colour
would have made them very difficult for moa to locate amongst a
background of leaf litter on the forest floor. The juvenile leaves would
have been difficult for moa to swallow, given that moa lacked teeth.
Without the ability to chew, they
had to swallow leaves whole or at
least in large pieces, which would
have been a difficult task, thanks in
part to their long, rigid shape and
sharp lateral spines. Spectrometric
analyses showed that the distinctive colour patches associated with
each spine would have been particularly conspicuous to birds, who
are sensitive to bright (achromatic)
visual signals. Paleoecological
records indicate that the maximum browsing height of the tallest moa species was approximately
three metres.13 So the sudden shift
to leaves that are ordinary in size,
shape and colour at approximately
three metres roughly coincides
with a height refuge from bird
browsers.
These results are important for
Figure 1. Mottled-brown seedling leaves (A), stiff, serrated juvenile leaves (B) and ordinary-looking adult
two reasons. First, they provide
plants (C) of Pseudopanax crassifolius.
one of the first quantitative examples for crypsis in plants. Second,
So why is P. crassifolius so unusual looking? A recent study sug- they illustrate that plants can alternate colour-based defensive
gests that browsing birds may have selected for its unusual appear- strategies during ontogeny, switching from being cryptically
ance.12 Prior to human arrival, New Zealand lacked native land coloured as seedlings, to aposomatically coloured as juveniles and
mammals (except for two species of bat) and instead was home to ultimately colour-undefended as adults, once they grew above the
giant, flightless birds called moa.13 Because birds lack teeth and reach of the putative browser. Many animals switch colour-based
cannot chew, they must swallow leaves whole, by first placing them defensive strategies during ontogeny.1 Fadzly et al.12 show evoluin their bill and then snapping their head forward to orient them
2
Plant Signaling & Behavior
Volume 5 Issue 1
tion might sometimes favour a
similar colour-based strategy in
plants.
New Zealand Mistletoes
Rather than referring to a single phylogenetic lineage, the
term ‘mistletoe’ refers to a polyphyletic group of plants that
have evolved parasitic lifestyles
independently.21,22 There are
two main phylogenetic lineages of mistletoes: the family
Loranthaceae, which evolved in
the Southern hemisphere, and the
family Viscaceae, which evolved
in the northern hemisphere.23,24
Both lineages have since dispersed out of their native hemispheres and many geographic
locales now house members of
both families.
Figure 2. Korthasella salicornioides infecting Leptospermum scoparium.
Australasia is home to an
unusually high diversity of
Loranthaceous mistletoes, which show varying degrees of host of alpine habitat. Alpine habitat does not support forest and is
specialisation; some species are found on only a single host spe- instead inhabited by herbs, tussocks and short-statured shrubs.
cies, while other exploit a large number of different host species. Alpine areas in New Zealand also contain a distinctive type
Several previous observers have noted that Australian mistletoes of rocky habitat called ‘scree slopes’, which occur on especially
often resemble their hosts with striking accuracy. Possums (order steep, alpine terrain. Scree slopes are demanding places for plants
Phalangeriformes) are important, arboreal browsers in Australian to grow, because the soil surface is comprised of large rocks that
forests and many host trees are heavily defended chemically. are moving continuously down slope. Although these rocks move
If Australian mistletoes have evolved to mimic their hosts mor- slowly, over the course of a perennial plant’s lifespan this movephologically, possums may confuse them with their chemically ment acts to separate vegetative plant parts from their root sysdefended hosts.25,26
tems. Numerous plant species from a wide range of phylogenetic
A similar situation may occur in New Zealand. Some backgrounds have adapted to this harsh habitat by producing
Viscaceous mistletoes, such as Korthalsella salicornioides (A. Cunn) stems that connect above- and below-ground tissues by continuTiegh., parasitise shrubs and small trees and often look remark- ously elongating as vegetative plant parts are pulled down-slope
ably similar to their preferred hosts (Fig. 2). Common herbivores away from their root systems.
Another distinctive attribute of plant species that are adapted
such as insects might therefore have difficulties distinguishing
mistletoes from chemically defended hosts. On the other hand, to scree slopes is that they are very difficult to find.27 Scree
Loranthaceous mistletoes in New Zealand look quite different slopes are typically slate-grey or even black, and plants such as
from their preferred hosts. One difference between families that Notothlaspi rosulatum match the colour of their rocky habitat
may explain their apparent differences in host resemblance is that with surprising accuracy (Fig. 3). Whether moa included them in
Viscaceous mistletoes attack mostly small-statured hosts, while the diet regularly is not known. However, if they did their colour
Loranthaceous species usually attack taller trees. Therefore, if may have made them easy for moa of overlook.
New Zealand mistletoes have evolved to resemble their preferred
Substrate colour matching seems to occur in a wide range of
hosts, the putative herbivore may have attacked small-statured other plant species inhabiting permanently rocky habitat. Perhaps
hosts preferentially. Although it is difficult to pinpoint which the best-known example is the genus Lithops, which grows in the
herbivore this might be, one obvious candidate is moa.
rocky deserts of Southern Africa and rightly deserves its common
name ‘stone plant’, given their remarkable resemblance to rocks
Scree Plants
and small pebbles. Like New Zealand scree plants, the ‘stone
plant’ syndrome is not restricted to this genus, and many speApproximately 15 million years ago New Zealand began a period cies from a range of phylogenetic backgrounds appear to have
of very rapid tectonic uplift, which transformed New Zealand converged on this distinctive appearance. Other notable examinto a mountainous archipelago characterised by extensive areas ples of cryptically coloured plants inhabiting rocky habitats are
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Plant Signaling & Behavior
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Figure 3. Notothlaspi rosulatum in flower.
s­ hort-statured cacti in North American deserts (Mammillaria
spp.28) and herbs that inhabit serpentine grasslands of California
(e.g., Streptanthus spp., Strauss unpubl.).
4
A Hypothesis
Under what conditions is crypsis a viable defensive strategy in
plants? Several conditions are necessary: (1) Plants need to be
preyed upon by visually orientated herbivores. If a plant’s main
herbivores locate plants using olfactory or tactile cues, visual
Plant Signaling & Behavior
Volume 5 Issue 1
mimicry would obviously be ineffective. (2) Plants need to be
habitat specialists, such that they grow in environments that provide a consistent visual background. Plant species that utilise a
wide range of habitats lack a specific background that they can
evolve to resemble, which would likely inhibit the evolution of
crypsis, unless species were locally adapted to different habitats.
(3) Plants must be short-statured, such that they grow in close
physical proximity to the visual background generated by their
preferred habitat. By definition, an object is cryptic because it
resembles its background. So when a plant grows away from a
background that it resembles, it looses any effect of crypsis. (4)
The preferred habitat must be unpalatable. If the visual background of a preferred habitat were itself palatable, for instance
when mistletoes parasitize palatable hosts, there would be no
adaptive benefit to resembling it. Under these four circumstances, crypsis appears to be a viable defensive strategy in plants.
Although there is little evidence to support this hypothesis to
date, this may be due to a lack of investigative effort rather than
realism.
A Methodological Framework to Test for Crypsis
How does one test the hypothesis that a plant is cryptically
coloured? The most obvious way is to conduct an experiment
by manipulating the plant’s colour and offering it to herbivores.
An experimental approach is the only way to provide a direct
link between plant colour and herbivore damage. Unfortunately,
this might not always be possible. There are numerous obstacles
to designing effective experiments in ecology.29 One such barrier
to experimental tests of plant crypsis is an absence of appropriate techniques to manipulate the colour of plants leaves. In the
case of New Zealand, another serious problem is that an important group of herbivores is now extinct, which makes a direct
experimental approach impossible. Abiguity concerning putative
herbivores may also be the rule rather than an exception. Some
researchers have argued that this situation applies to most plants
across the globe:
“Living organisms are beautifully built to survive and reproduce
in their environments. Or that is what Darwinians say. But actually it isn’t quite right. They are beautifully built for survival in
their ancestor’s environments… Since modern man has drastically
changed the environment of many animals and plants over a time
scale that is negligible by evolutionary standards, we can expect
to see anachronistic adaptations everywhere.” (Richard Dawkins,
quoted by30).
Many scientific disciplines, such as astrophysics, geology and
palaeontology, suffer from an inability to conduct manipulations
as a regular part of scientific inquiry. Similarly, experimentation
is beyond the reach of most questions in biogeography, because
most biogeographic phenomena operate on spatial and temporal
scales that are too large to manipulate. Instead, biogeographers
rely on observations and indirect hypothesis testing, in much
the same way as astrophysicists, geologists and palaeontologists.
However, biogeographers have developed a useful methodological
tool that can be used to good effect under these circumstances.
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‘Null models’ are pattern-generating algorithms that simulate
biological patterns in the absence of a structuring process.31,32
Simply put, null models test hypotheses by comparing field observations to randomised expectations. Although they are power
tools for identifying patterns in field observations, they cannot
be used to precisely identify the processes responsible for them.
By providing a means to test whether a plant shows an
unusual likeness to the appearance of its preferred habitat, null
models can provide the foundations for a research program on
plant crypsis. Qualitative judgements based on human vision are
insufficient to identify cryptic plants, because the human eye differs markedly from most herbivores, but see ref. 33. Apparently
cryptic colour patterns could also arise by chance relatively easily.
A plant whose colour is determined solely by physiological processes could easily disperse by chance into an environment that
is coloured similarly.
To test whether a scree plant is cryptically coloured, null
models can be used to redistribute a population of such plants
across a range of alpine habitats. Differences between the spectral properties of leaves and each alpine habitat can then be calculated to establish whether scree plants are less conspicuous in
their preferred habitat relative to other potentially suitable habitats. Similarly, null model simulations can be used to simulate
the distribution of mistletoes among potential host species. The
conspicuousness of observed mistletoe-host species combinations,
both in terms of morphology and reflectance spectra,34,35 can then
be compared to all other potential mistletoe-host species combinations. If observed species combinations are less conspicuous than
what would be expected by chance pairings of mistletoes and their
hosts, one can conclude a cryptic pattern exists. Null model comparisons also can be recalculated according to the visual systems
of different types of herbivores,36 to test whether results change
from the perspective of different types of herbivores.
While this approach cannot establish whether herbivores
would actually overlook a plant, it can be used to establish
whether a plant is especially inconspicuous. This is a powerful
insight and an important first step in testing the crypsis hypothesis. By providing a means to test for a cryptic pattern, null models can lead the way to understanding whether plants sometimes
hide from predators.
Acknowledgements
I would like to thank Nicholas Gotelli, Kevin Goold, Martin
Schaeffer and Sharon Strauss for helpful comments and discussions concerning plant colours.
Plant Signaling & Behavior
5
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