Tag Archives: masquerade

Faking it as a survival strategy

224139Cheats and Deceits: How animals and plants exploit and mislead. By Martin Stevens. Published by Oxford University Press (2016).

Last year, on a trip to Devon, I saw my first ever oil beetle (Meloe proscarabaeus). She was beautiful. Her black carapace glistened violet and blue in the sunlight. She was gravid and crawling along the footpath in search of a place to dig a nest burrow to lay her eggs. But what I did not yet appreciate was the extraordinary life cycle of these captivating beetles. The young of a related species, Meloe franciscanus, emerge from the nest and swarm up a nearby plant where they congregate in a mass mimicking the shape of a female solitary bee (Habropoda pallida) and release a chemical compound similar to the bee’s sexual pheromones.  This proves all too irresistible to male bees who are drawn to this aggregation and attempt to mate with it, presenting the larvae with the perfect opportunity to grab hold of the bee and clamber onto his back.  He then carries these passengers with him until he finds a female to mate with at which point the larvae instantly decamp onto the female. From here they then transfer to her nest where they devour the stored nectar, pollen and the bee’s eggs. The evolution of this complex mimicry is absolutely fascinating and forms part of Martin Stevens‘ interrogation of deception in Cheats and Deceits: How animals and plants exploit and mislead.

This book is an immensely informative and enjoyable exploration of the multiple roles deception plays in nature. Stevens sets out a detailed examination of a wide variety of instances of natural deception from well documented examples such as the evolution  of camouflage through industrial melanism in the Peppered Moth (Biston betularia) to current research into the resemblance to falling leaves in the movement and colouration of Draco cornutus, a gliding lizard from Borneo. It is to Stevens’ credit that this book makes for entertaining and effortless reading while clearly citing all the relevant research within context and pointing to areas where knowledge is still lacking.

The language of deception is important. Stevens takes the time to explain some of the more commonly used terms associated with deception such as camouflage (blending in to the environment), mimicry (assuming the appearance – be that visual, chemical, behavioural or acoustic – of another organism) and masquerade (taking the form of an inedible object – as with stick insects). Mimicry and masquerade therefore lead to misidentification while camouflage reduces detectability or impairs recognition. Mimicry also comes in various guises some of which can be described as: aggressive, when predators mimic harmless species to enable prey capture; Batesian, when a palatable species mimics the characters of an unpalatable species, as seen in the chicks of an Amazonian bird Laniocera hypopyrra mimicking toxic caterpillars; and imperfect mimicry, as with hoverflies roughly resembling certain species of wasps and bees (for which there are a number of competing theories).

This, of course, only scratches the surface of a vast area of research that Stevens specialises in as head of the Sensory Ecology and Evolution group at the University of Exeter where he continues to research these themes. His enthusiasm for his topic is highly infectious; you find yourself transported from an explanation of background matching in cuttlefish, to an historical aside concerning the development of military camouflage, and on again to a description of his own field experiments in testing the efficacy of disruptive colouration.

“We must trust to nothing but facts: these are presented to us by nature and cannot deceive. We ought, in every instance, to submit our reasoning to the test of experiment, and never to search for truth but by the natural road of experiment and observation.” ~ 18th-century chemist Antoine Lavoisier

The book does rely heavily on zoological examples, and although Stevens doesn’t entirely neglect plants his observations do tend to mainly focus on carnivorous plants and orchids. But to be fair, Stevens does make the point that more research into botanical forms of deception is required and suggests that this should be undertaken with a view to specifically exploring the roles of chemical signalling and sensory exploitation. One of the examples cited in the book is the orchid Epipactis veratrifolia which attracts female hoverflies to lay eggs on the plant by releasing chemicals that mimic the alarm pheromones of aphids (the food source of hoverfly larvae). This may rather be a means by which the orchid exploits an inbuilt perceptual preference for chemicals associated with hoverfly larval food sources – either way the plant is deceiving the insect in order to  ensure protection from aphid infestation.

A form of deception more commonly associated with orchids is that of exploiting male insects to pollinate plants by mimicking the female form through the shape and colouration of the flower. However, Stevens points out that this mimicry is sometimes (as in Cryptostylis orchids) not particularly convincing to human eyes, but is overwhelmingly so to the male wasp which tries to mate with the flower and thus collects the pollinium which will be deposited at the next Cryptostylis flower that he visits. With this example (as with the oil beetle, among others) the author cautions researchers of deception in nature to be aware of anthropocentric biases that may arise through our observations and study, and to (wherever possible) approach our subjects in the manner and with the senses of the deceived species.

I am utterly delighted and inspired by this book and am certain that I will return to it again and again as a point of reference. I have no hesitations in highly recommending it to researchers, field naturalists and those with a passing interest in natural history.


At the time of writing, Phil Torres and Aaron Pomerantz have discovered and documented kleptoparasitism of ants in a species of butterfly (Adelotypa annulifera) in the Peruvian Amazon which they believe might mimic ants through their wing patterns. This seems to me an ideal opportunity for further research looking at visual and chemical mimicry given both the wing patterns and larval associations.

What’s (not just) brown and sticky? Adaptive radiation in Stick and Leaf Insects in the order Phasmatodea.


The Indian or laboratory stick insect, Carausius morosus, a common pet.

The order Phasmatodea contains more than 3,000 extant species of insect found throughout the world, especially the warmer zones. These herbivorous (mostly arboreal) insects are most well-known for their crypsis, or camouflage, where their colour, shape and behaviour enable them to masquerade as twigs or leaves (hence their common names of stick and leaf insects).

Though there is still uncertainty about a definitive phylogeny, phasmids are considered one of 11 orthopteroid insect orders within the assemblage known as Polyneoptera. Phasmatodea are found alongside the modern orders: Blattodea (cockroaches), Dermaptera (earwigs), Embioptera (web-spinners), Grylloblattodea (ice crawlers), Mantodea (praying mantises), Mantophasmatodea (heel-walkers) and, of course, Orthoptera (crickets, grasshoppers, and katydids). According to phylogenomic analyses of nucleotide and amino acid sequences, some of these Polyneopteran lineages are thought to have emerged ~302 million years ago, with phasmids evolving after the Permian mass extinction.1

Fossil Evidence

Fossil evidence of phasmids is, however, extremely rare.   Specimens have been recovered in amber, most notably representatives of Euphasmatodea and Timematodea, with the oldest well-documented fossils being found in Cretaceous Burmese amber. Recent discoveries of the oldest-known fossilised leaf mimics (Phylliinae) from Messel, Germany in 2006 of Eophyllium messelensis date this foliacious mimicry to the Eocene.2

Although the fossil evidence is patchy, it is thought that traits relating to morphological plant masquerade within Phasmatodea first developed with stick mimicry in the Permian, followed by leaf mimesis developing in the Eocene when angiosperms largely replaced conifers as dominant trees.

phasmid fossils

Simplified cladogram with a partial geochronologic scale showing the phylogenetic position of E. messelensis and the temporal sequence of character evolution. Insert; Photo (A) of holotype of fossil leaf insect E. messelensis, from the Eocene Messel Pit, Germany and Photo (B) Cretophasmomina melanogramma from 126 mya from the Yixian formation in Inner Mongolia [2, 3]

Fossils of Cretophasmomima melannogramma discovered in Yixian, China in 2006 from the Cretaceous Jehol biota (approximately 129 mya), however, provides evidence of phasmid crypsis relating to a Gingkophyte, Membranifolia admirabilis, which displayed leaf-shaped plant organs.3  It is therefore thought that leaf mimesis may well have developed far earlier than previously thought.

Crypsis, Camouflage, and Masquerade

In order to avoid visual detection by predatory mammals, birds, reptiles and other invertebrates, many insects evolved morphological characteristics that enabled them to blend in to their surrounding environment. Specifically in the case of phasmids, these evolutionary adaptations have been very closely linked to the insects’ host and food plants leading to a coupling of ecological and evolutionary dynamics.4,5,6

Cryptic colouration, elongation of the body and legs, or, alternatively, broadening and flattening of the body to resemble leaves are all forms of masquerade adopted by phasmids to avoid detection by predators. This has led some researchers to conclude that predation may be an important driver of speciation in this order. Successful adaptation, through camouflage, may therefore lead to divergence in adaptive radiation. 4,5,6  

The basal-most extant recorded clade of Phasmatodea is the sub-order Timematodea, within which is found the genus Timema whose species are found throughout southwestern North America on a variety of host-plant species.7 Experimental studies have been conducted into the influence of ecological factors with regards adaptive radiation in Timema cristinae with particular emphasis on host plants and cryptic colouration.4,5,6,7


Above: Timema cristinae, endemic to California has repeatedly evolved ecotypes adapted to different host plant species. One ecotype features a distinct white stripe (right photo) on its back and feeds on the thin, needle-like leaves of a shrub called Adenastoma. The other phenotype has no stripe and feeds on Ceanothus (left). Below: Phylogeny of Timema species.

It was found that two distinct T. cristinae morphs had developed on two morphologically dissimilar plant species distributed in parapatric mosaics. The first plant, Adenostoma fasciculatum, has needle-like leaves, while the other, Caenothos spinosus, has broad, ovate leaves. Each T. cristinae morph (or ecotype) was found to be more cryptic on one of the two plant species depending on whether they displayed a heritable white dorsal stripe or not. One of the experiments found that bird predation significantly lowered numbers of T. cristinae that were maladapted to the host plant. Further studies concluded that through predator pressure, partial (but incomplete) ecological speciation has occurred in T. cristinae as the morphs still successfully interbred.5,6,7

This partial speciation may, however, form only one dimension of selective pressures that constitute adaptive radiation events. It was also shown that by comparing different Timema species that share the same host plant, that sexual isolation was not as marked as with between species on different plants (when compared with T. podura and T. chumash)7 lending credence to the notion of ecological speciation. It is therefore apparent that predators apply selective pressure leading to morphological crypsis and divergence, but that this does not necessarily directly lead to speciation, but is more likely an intermediate stage in adaptive radiation.

Flying, Jumping, and Holding Still

In the case of the Phasmatodea, it has been discovered that diversification occurred in a wingless state and that wings were subsequently derived on a number of occasions.

Of the 3,000 species of phasmids, only 40% are fully winged, while the remainder are partially winged or entirely wingless. While being fully winged conveys advantages of dispersal, escape and finding resources,  it has been claimed that increased female fecundity and crypsis may have served as a selective advantage in early phasmid evolution in a shift to winglessness. Apart from flight, wings and partial wings can also be used in threat or startle responses to deter would-be predators. By examining DNA sequence data and applying parsimony optimisation it was found that the ancestral condition of Phasmatodea is wingless.8

It was also found that certain phasmid lineages had “re-evolved” wings prompting suggestions that this reacquisition may confer adaptive advantages of being both winged and wingless as conditions necessitate over ecological time leading to further speciation.8


Timema chumash is unusual in phasmids in that it has been found to jump away from potential threats. Although it can only jump relatively short distances by extending the hind tibia, it can reach take-off velocities comparable to some larger European flea beetles. The leg positions and hind-leg length of T. chumash contrast with the morphology of other stick insects; its legs emerge ventrally from the thorax and its hind legs are proportionately longer than those of other phasmids. As T. chumash is wingless, it jumping is suggestive that it would enable a rapid fall from the plant it was perching on taking it out of the visual field of predators and providing it with another opportunity to camouflage itself nearby.9 These morphological and behavioural traits may present opportunities for further adaptive evolution.


A well-documented behaviour in many phasmids is that of catalepsy whereby the insect is able to remain motionless or produce extremely slow movement as a form of twig or leaf mimesis to aid with predator evasion. The mechanism by which this is achieved, is via the high gain of the femur-tibia joint control system,10 and has been recorded in fossil specimens.2  A key difference between phasmids and other orthopteroids is this significant coevolution of the mimetic body shape with catalepsy.10

Parthenogenesis, Hybridogenesis and Androgenesis 

Phasmids experience a wide array of reproductive modes with about 10% of the phasmid taxa being parthenogenetic and producing all-female offspring (thelytoky).11 Although parthenogenesis reduces genetic variability, it does not wholly suppress it.  Furthermore autopolyploids and allopolyploids can take advantage of higher mutational rates to increase heterozygosity. Androgenesis is also common and has been proposed as a likely pathway to cladogenesis in the genus Clonopsis11 and has already been recorded in Pijnackeria where tetraploid hybrids lacking maternal genes, but keeping the maternal mitochondrial DNA, speciated.12 The discovery of interracial and interspecific hybridogenesis in the genus Bacillus added further weight to the notion of maintaining (or even increasing) genetic diversity within phasmid lineages and creating opportunities for further speciation. 12  

No one reproductive mechanism is exclusively used, so that complete reversion from thelytoky to amphimixis is possible.  These “tangled interactions” allow for genetic diversity to persist within and between populations. When considered as part of a series of repeated and complex reproductive strategies including sexual reproduction, parthenogenesis, androgenesis and hybridogenesis, it must be concluded that evolutionary pathways for phasmids are far from dead-ends.11, 12

Following divergence from other orthopteroids, phasmids took advantage of the new food sources and flourished following the angiosperm revolution and have continued to adapt in relation to predatory pressures, host-plant availability, behaviours, and complex reproductive strategies. Clearly, apart from the opportunities presented in the Eocene for cladogenesis and speciation, there continues to be further evolutionary opportunities relating specifically to morphology and sexual isolation in adaptive radiation of phasmids.

Black beauty stick insect shutterstock_51123130-1

The Black Beauty stick insect, Peruphasma schultei, is known to exist only in a tiny area of 5ha (12 acres) in the Cordillera del Condor region of northern Peru, at altitudes between 1200-1800m.


1.  Misof, B.  et al. (2014), Phylogenomics resolves the timing and pattern of insect evolution. Science. 346 (610), 763-767.

2. Wedmann, S., Bradler, S., and Rust, J. (2006), The first fossil leaf insect: 47 million years of specialized cryptic morphology and behavior. Proceedings of the National Academy of Sciences. 104 (2), 565-569.

3. Wang, M., Be´thou, O., Bradler, S., Jacques, FMB., Cui, Y., and Ren, D. (2014), Under Cover at Pre-Angiosperm Times: A Cloaked Phasmatodean Insect from the Early Cretaceous Jehol Biota. PLoS One, 9 (3), e91290

4. Farkas, TE., Mononen, T., Comeault, AA., Hanski, I. and Nosil, P. (2013) Evolution of Camouflage Drives Rapid Ecological Change in an Insect Community. Current Biology. 23, 1835-1843.

5. Nosil, P., Crespi, BJ., and Sandoval, CP. (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature. 417, 440-443.

6. Nosil, P. and Crespi, BJ. (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proceedings of the National Academy of Sciences. 103 (24), 9090-9095.

7. Nosil, P. and Sandoval, CP. (2008) Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects. PLoS One. 3(4), e1907

8. Whiting, MF., Bradler, S. and Maxwell, T. (2003) Loss and recovery of wings in stick insects. Nature. 421, 264-267.

9. Burrows, M. (2008) Jumping in a wingless stick insect, Timema chumash (Phasmatodea, Timematodea, Timematidae). The Journal of Experimental Biology. 211, 1021-1028.

10. Wolf, H., Bässler, U., Spieß, R. and Kittman, R.  (2001) The femur–tibia control system in a proscopiid (Caelifera, Orthoptera): a test for assumptions on the functional basis and evolution of twig mimesis in stick insects. The Journal of Experimental Biology. 204, 3815-3822.

11. Scali, V. (2009) Stick insects: parthenogenesis, polyploidy and beyond. In: Life and Time: The Evolution of Life and its History. Cleup, Padova. 171-192