Author: Gino Brignoli

Currently employed as FSC BioLinks Project Officer for London, I am coordinating invertebrate-focused place-based volunteer training and delivering a range of recording project activities across London. I am also developing and delivering online training courses and content focusing on invertebrate taxonomy, field ID and ecology through a virtual learning platform. You can find out more about the project here. Previously ant genomics and evolution Research Assistant at Queen Mary University of London. With a keen interest in ecology and entomology, I have volunteered with the Lepidoptera department and Soil Biodiversity Group at the Natural History Museum, and on the Thorn to Orchid and Water for Wildlife projects with London Wildlife Trust.

The Walking (Un)Dead: Zombie ants and the strange effects of parasitic fungi on ant behaviour.

In the understorey of a tropical forest, a carpenter ant, of the species Camponotus leonardi, has descended from the canopy away from her regular foraging trails and staggers drunkenly along a branch. Her movements are jerky and conspicuous. She twitchily moves forwards and suddenly starts convulsing with such ferocity that she falls from the branch onto the ground before again taking up an erratic fitful path that zigzags and circles back on itself. Around noon, after several hours of climbing and aimless lurching (now no more than about twenty-five centimetres above the ground) the ant finds herself on the underside of a sapling leaf where, without warning, she forcefully sinks her mandibles into one of the leaf’s veins, gripping it firmly between her tightly locked jaws. Within six hours the ant is dead. After two days, white hairs bristle from between her joints and a few days later these have become a brown mat covering the whole insect and a pinkish-white stalk has started to erupt from the base of the ant’s head. The stalk continues to grow and within two weeks it has reached twice the length of the ant’s body reaching towards the ground below.

This is a description of a “zombie-ant”, part of the life-cycle of a parasitic fungus, Ophiocordyceps unilateralis. This bizarre behaviour was first recorded by Alfred Russell Wallace in Sulawesi in 1859, but was not researched in much detail until quite recently. It has since been discovered that the fungus disrupts the normal behaviour of the ant through chemical interference in the brain, causing the infected ant to behave in ways that will improve the fungus’ opportunities to spread its spores and so reproduce. The fungus grows throughout the body cavity of the ant, using internal organs as food while the ant’s strong chitonous exoskeleton serves as a kind of capsule, protecting the fungus from drying out, being eaten, or further infection.

The earliest known record of a fungus visibly parasitizing an insect dates from about 105 million years ago, it is a male scale insect, preserved in amber, with two fungal stalks projecting from its head. But this fossil cannot tell us if the infected insect’s regular behaviour was changed or disrupted in any way. Evidence of “Zombie-ant” behaviour dates from around 48 million years ago from fossilised leaves that show the distinct markings on either side of leaf veins left by the lock-jawed mandibles of Eocene epoch ants. This association is evidently ancient and seemingly very common, with about 1,000 species of fungal parasites of insects known to exist today. These fungal pathogens have evolved to become either strictly species-specific or more generalist in their target insects, with some able to infect hundreds of different species. The variety of fungal pathogens and potential hosts has created some peculiar behaviours in insects which have most likely co-evolved with the fungi.

It is sometimes difficult to know which of these insect behaviours are entirely involuntary and driven by the fungus to improve its own reproductive success; and which the insects have evolved as a form of defence against infection. One of these unresolved odd behaviours is when the ant host climbs to an elevated position in what is known as “summit disease”. This increases the area over which spores can spread through wind dispersal, and removes the ant from close proximity with its colony or relatives. It is unclear if this behaviour is a zombie state caused by the fungus or if it is an altruistic act of self-sacrifice by the ant. By moving to an area away from its relatives it might be saving the rest of the colony from the immediate spread of infection by what is sometimes called “adaptive suicide”.

In this age-old struggle for survival the ants have developed adaptations to protect themselves and their nests from fungal infections. Grooming themselves and socially cleaning each other, allogrooming, they remove potentially harmful spores before these can penetrate the cuticle and take hold. Some ants spray poison in their nests to act as fungicides and if that fails to stop an infestation, they partition their nests by sealing off contaminated chambers. In some cases infected individuals are carried out of the nest by healthy workers; and as a last resort the entire colony relocates, abandoning the nest.

Zombie-like behaviour in insects is also caused by other types of parasites including bacteria and even other invertebrates. Such parasites are extreme versions of the multitudes of microscopic organisms that exist in and on all living things. This raises fascinating questions about the nature of any organism’s true independence in what are undoubtedly highly complex interrelated living systems. Zombie-ants provide us with a glimpse into this intricately tangled-web of molecular influences and behavioural adaptations – often leading us to wonder: who, ultimately, controls whom?

References:

Andersen, S.B., Gerritsma, S., Yusah, K.M., Mayntz, D., Hywel-Jones, N.L., Billen, J., Boomsma, J.J. and Hughes, D.P. (2009) The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype. The American Naturalist, 174(3): 424-433.

Hughes, D.P, Andersen, S.B., Hywel-Jones N.L., Himaman W., Billen, J. and Boomsma J.J. (2011) Behavioral Mechanisms and Morphological Symptoms of Zombie Ants Dying from Fungal Infection. BioMed Central: Ecology, 11(13).

Pontoppidan M.-B., Himaman W., Hywel-Jones N.L., Boomsma J.J. and Hughes D.P. (2009) Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants. Public Library of Science: ONE, 4(3): e4835.

Shang, Y., Feng, P. and Wang, C. (2015) Fungi That Infect Insects: Altering Host Behaviour and Beyond. Public Library of Sciences: Pathogens, 11(8): e1005037

Hughes, D.P., Wappler, T. and Labandeira C.C. (2010) Ancient death-grip leaf scars reveal ant–fungal parasitism. Biology Letters, 7: 67-70.

Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. and Pell, J.K. (2006) Bizarre Interactions and Endgames: Entomopathogenic Fungi and Their Arthropod Hosts. Annual Review of Entomology, 51: 331-57

Bekker, C. de, Quevillon, L.E., Smith, P.B., Fleming, K.R., Ghosh, D., Patterson, A.D. and Hughes, D.P. (2014) Species-Specific Ant Brain Manipulation by a Specialized Fungal Parasite. BioMed Central: Evolutionary Biology, 14(166).

All images ©Alex Wild http://www.alexanderwild.com

Marshland meander: A visit to RSPB Rainham Marshes

I have been a card-carrying member of the Royal Society for the Protection of Birds for about 15 years. In that time I have seen some great successes and a variety of challenges faced by the society. The RSPB is the largest nature conservation charity in the UK (with over 1 million members) and also the oldest. Originally set up in 1889 by a group of women who were concerned about the hunting of birds for their feathers (which were a la vogue – especially the decorative use of grebe skins and egret plumes in the hats of Victorian ladies).

The ‘Birds’ component of the RSPB’s moniker is still very relevant today as they continue to work on species protection projects that focus on individual UK bird species which are in decline or under threat such as stone curlews, black-tailed godwits, corncrakes and lapwings. In fact this strategy proved highly successful in the past as with the red kite re-introduction project which saw numbers of a globally threatened species rise to 1,800 breeding pairs in Britain between 1980 and 2011. This methodology has, however, led to some criticism of the single-species approach for tending to select high-profile charismatic species, and employing management practices that may disadvantage non-target species. It also raises the question of why a particular species should receive conservation preference over any other. To this end the IUCN Red List of Threatened Species was established to help assess the conservation status of species by identifying threatened species and promoting conservation action. We aren’t even aware of the totality of extant species, nor do we have a full understanding of which of those are, or me be, under threat. Insects are a good example; with only 6,051 insect species listed in the IUCN Red List database (of somewhere between 1 million known species and up to 8.5 million expected to be found) there is still an enormous amount of work to be done.

The RSPB’s conservation work, does however involve more than the protection of individual species. Another component of this work is habitat management which is undertaken at more than 200 reserves maintained by the society. This presents the RSPB with opportunities to work towards conserving other (unfeathered) species either on their own or in collaboration with partner organisations. At a time when environmental protections in the UK are likely to be significantly eroded and underfunded, there is some small comfort to be drawn from the fact that there are many conservation organisations like the RSPB that will continue to work to maintain, manage and support wildlife and wild places. But conservationists will need to be focused and their priorities will need to be very clear.

In 2013 the RSPB added the tagline “Giving nature a home” to its logo exemplifying how it has become a conservation charity that now also focuses its attention on wild spaces and the plight of all the other featherless organisms. Though this could be seen as a large charity cannibalising and intervening in the work of smaller (and more focused) organisations in the sector, the sheer scale and associated land-area that the RSPB maintains does allow for a more holistic approach with regards ecosystem and habitat conservation – effectively creating opportunities for protecting and conserving a wide range of species through landscape-level management. What is significant here, though, is that we need to be able to maintain an interesting matrix of connected habitats of varying sizes in order to be able to support as much biodiversity as possible.

RSPB Rainham Marshes is one of the reserves in the society’s portfolio which was established in 2000 in an area of Essex along the river Thames that was formerly Ministry of Defence land and closed to the public for over 100 years. Part of the Inner Thames Marshes SSSI that stretches over an area of 479.3 hectares this area is a haven for wetland birds. On my recent visit I got to see some of these including swans, lapwing, oystercatcher, marsh harrier, shoveler, shelduck, mallard, canada geese, little grebe, grey heron, redshank, sedge warbler, reed bunting, as well as swifts, linnets, goldfinches, kestrel, sand martins and a displaying skylark. Hauled out on a sandbar on the far bank of the river was a group of 7 harbour seals. As fantastic as these were, why I really came to Rainham was for the invertebrates. The low-lying grazing marsh with wet grassland, ditches, scrub and reed beds on an urban and light-industrial fringe make for a complex habitat mix with a number of interesting ecotones.

It was for the most part a beautifully sunny afternoon, but quite windy at times making some of the photography quite challenging (as you’ll notice from a few rather blurry shots in the following slideshow). I’ve also made note of a few additional butterflies that I was just too slow to photograph – small heath, large white, peacock, red admiral and large skipper – as well as a broad-bodied chaser that zoomed past my head.

All of the invertebrates featured were found through observation and searching by hand because I wanted to photograph them as undisturbed and in as natural a setting as possible. This has meant that species that would have been found by using a pooter, sweep net or beating tray are lacking from my finds. Nonetheless, I was delighted with the dazzling green of the swollen-thighed beetle (Oedemera nobilis) perfectly placed at the heart of a dog rose its femurs bulging like metallic pantaloons, found quite soon after leaving the visitor centre. A leisurely walk along the bank of the river skirting the reserve presented many empid flies, jumping spiders, bumble bees and my first record of a knobbed shieldbug (Podops inuncta) scuttling for cover across a concrete embankment where I chose to stop for my ploughman’s lunch.

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Please feel free to send me corrections if I have misidentified anything or if you can get closer to species with those I’ve only managed to identify to genus.

I then cut away from the river, crossing a channel of pebbles and loose rock aggregate where a mix of stonecrop, bramble and ragwort pushed up through the gaps. Here were more bees and another personal first of a couple of black-striped longhorn beetles (Stenurella melanura) on bramble flowers. This area also had a scattering of detritus washed up from the river: bits of plastic, wood, a child’s sky-blue bicycle lying on the mudflat. Beneath a plank I found a scuttling centipede and a cluster of earwigs all with abdomens raised and forceps flailing in defence. Then on along a grassy path and down an embankment, stopping to investigate the umbels of giant hogweed for ants, flies, wasps and other insects taking advantage of this high-energy nectar source. A bit of a detour through the grass saw a flurry of sightings: common blue (Polyommatus icarus), small tortoiseshell (Aglais urticae) and a summer chafer (Amphimallon solstitiale). Unfortunately a bit early in the year for the now fairly well-established and easily recognisable wasp spiders (Argiope bruennichi), but I think another visit in late Summer should do the trick.

I dropped in at the visitor centre for a fruit juice and then headed off into the reed beds along the boardwalks where I saw a female scorpion fly (Panorpa sp.) with her particularly oddly-shaped extended mouthparts and chequered wing patterns. Here too, on thistle, were 6 hairy shieldbugs (Dolycoris baccarum) sporting Art Deco-like purple and green thoraxes, and black-and-white banding along their antennae and laterotergites. Disappointingly, I only managed to get one photograph of a dragonfly, a blue-tailed damselfly (Ischnura elegans) before closing time. And as I made my way to the exit marvelling at all the wonderful creatures I had been fortunate enough to see I was surprised by a female mallard leading her ducklings along the boardwalk who, on sight of me, dropped over the edge and disappeared into the reeds.

Faking it as a survival strategy

Cheats 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.

Postscript

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.

Getting down and dirty with the Earthworm Society of Britain

I attended the Earthworm Society of Britain‘s annual general meeting at Cannock Chase Forest where I got to meet fantastic amateur enthusiasts, very knowledgable naturalists with a general interest in worms, and some hardcore earthworm specialists. It was an immensely enjoyable couple of days of field recording in various habitats found here including broadleaved woodland, grassland and heath as well as microhabitats such as dead wood.

“It may be doubted whether there are many other animals which have played so important a part in the history of the world, as have these lowly organised creatures”. Charles Darwin

Since Darwin’s observations and experiments with earthworms was first published in 1881 under the title The Formation of Vegetable Mould, Through the Action of Worms, With Observations on Their Habits a new area of little-known research relating to these fascinating creatures was born. Despite this, we still find a lamentable lack of data regarding the distribution of earthworms throughout the UK and are continuing to research the ecosystem-wide implications of their below-ground activity.

In attending the society’s field day and AGM I was curious to find whether earthworms would pique my interest as a naturalist and scientist or whether I had developed a nostalgic yearning for simpler times. I have vivid memories of when, as a child, I would gingerly lift the edge of the damp burlap sack to scoop out trowel-fulls of fusty earth from half an oil drum in which my grandfather bred earthworms to bait his fishing hooks. I think the answer is that they are probably both true. This area is rich for contributions to research and recording while also being a great opportunity to get my hands stuck in some dirt and forget about my everyday worries. And when Amy Stewart so eloquently points out in response to the relevance of Darwin’s research and the significance of earthworms, that they’re “…only carrying out the natural order of things, folding the ruins of a farm, a city, or a society into the lower strata of the earth. When our civilizations end, and when we as individuals die, we don’t ascend, not physically. We descend. And the earth rises up to meet us”, how could I resist?

Day 1

Looking for earthworms is a messy affair and you have got to be prepared to get dirty. Armed with spades, sorting trays and all-weather gear we set out to see what the various sites had to offer.

ESB We started with the damp, waterlogged woodland near the classroom we had booked for the day and were immediately set upon by midges and mosquitoes. Ankle-deep in mud, and stippled with insect bites we dug 5 soil pits here with a reasonable haul of worms before making a break for an area of bracken further up the slope and farther away from the biting flies. We didn’t find any earthworms in the bracken pits, but were entertained by a greater spotted woodpecker feeding her voracious and loudly calling young in a nearby nesting hole before we again set off to a new site. A stop on the way to explore the banks of a stream and some adjacent dead wood in varying states of decay provided a few more worms for our count as well as other obligatory detritivores – millipedes, centipedes and woodlice.

It was in the pits dug from the grass verge alongside a footpath with flowering speedwell and buttercups where the highest number of earthworms were found, along with leatherjackets and other unidentified fly and beetle larvae. Our small party of slightly bedraggled and filthy earthworm explorers then headed back to the Forestry Commission classroom. Looking to all the world like a group of unsuccessful treasure hunters or end-of-shift gravediggers we traipsed back to the promise of piping hot tea and freshly made sandwiches while a retinue of dog walkers, mountain bikers and Segway riders passed us by. After lunch we could be found sitting in drifts of leaf litter in an old disused drainage ditch beneath a small stand of beech trees opposite the car park where we turned up a few more worms.

Then on to the AGM. First we were treated to a fascinating presentation on the worldwide diversity of earthworms (look out for the fried egg worm when in the Philippines) and an update on the ongoing search for the world’s longest earthworm (currently hotly contested between researchers in the Amazon and another in South Africa) by the society’s chair. Thereafter, the recording officer presented an assessment of the state of earthworm recording in the UK compared to other ‘more charismatic’ species such as butterflies – I think it’s fair to say that we have some way to go yet, but that significant progress has been made since the establishment of the society. New members were elected to the committee (I am delighted to have been accepted as the new treasurer) and all matters were concluded and followed by dinner and drinks in a local pub.

Day 2

The next morning started with a sighting of a pair of Little Ringed Plovers on a derelict brownfield site near the hotel where we were staying before we bundled into cars and headed back to Cannock Chase with the intention of doing some mustard sampling, digging soil pits in the heath and surveying areas that were being grazed by cattle. We set off on foot from the car park along the road until we reached a small wooded area with birch trees and much dead wood where we started collecting worms accompanied by the call of a cuckoo.

And then on to the next site where the shallow, stony and root-filled heathland pits that we eventually managed to dig were predictably uninhabited by earthworms; but we did manage to extract some from beneath some carpet tiles that had been scattered on a grassy area nearby using the diluted mustard concoction below (which I’ve been told is as indispensable as a spade to earthworm recorders).

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A little further down the path a rather large felled tree was rolled away to reveal more worms and a host of other creatures including a palmate newt, a toad, an unidentified moth larva, pill millipedes, centipedes and carabid beetles. We were also treated to a view of a tree pipit calling from the top of an oak and the slightly stumbling flight of a scorpion fly. We then made our way on to the grazed area where we wanted to do our final sampling for the day. Or we would have, but as we walked past the cinnabar moths and the many humped yellow meadow ant nests we realised that we may have misjudged the distance somewhat, so picked up the pace but didn’t get there with enough time to do any sampling. As a consolation we did spy a green tiger beetle scuttle across the chalk path as we now hastened back to the car park for a final catch up before scrubbing our hands clean and going our separate ways.

More information

You may have noticed that for a blog post on earthworms, this has been fairly light on any detailed earthworm records. This is because we don’t yet have our full set of records from those who attended the field days, and for my part as I am still a complete novice I am still working my way through the ID process. For ID resources, there is an excellent key by Emma Sherlock and an online multi-access key developed by Richard Burkmar, both of which I highly recommend.

For a bit more information about earthworms and some of the work of the Earthworm Society watch this short youtube video produced by Eco Sapien and the FSC explaining why earthworms are important.

To get involved you can either contact the Earthworm Society directly or if you first want to try your hand at surveying earthworms you can take part in the citizen science project Earthworm Watch.

What is the cause of the Zika outbreak in the Americas?

I recently read an article by Claire Bernish¹that said that the release of GM mosquitoes was the cause of the Zika virus outbreak in Brazil – this immediately set alarm bells ringing. As it turns out, any real evidence to support these claims was lacking and Christie Wilcox, writing for Discover magazine,²has done a fantastic job in demolishing this argument by showing the inaccuracy of the dates and the distances involved. The GMM release site was 300 km away from the epicentre of the Zika outbreak and the release was in 2011-12, not 2015 as was stated in a similar article by Oliver Tickell in The Ecologist.³

“The Earth is round, not flat (and it’s definitely not hollow). Last year was the hottest year on record, and climate change is really happening … And FFS, genetically modified mosquitoes didn’t start the Zika outbreak.” – Christie Wilcox

Although I have my own concerns regarding the control of mosquitoes by means of genetic modification, I think that the scare-mongering surrounding GMMs and the Zika virus does more harm than good – especially when the scientific data is at best deficient and at worst entirely fabricated. Amongst the inevitable conspiracy theories that have surfaced the “best” argument that has been put forward seems to be that “Nature will find a way”. On another note, I also find the seeming disdain of laboratory scientists towards ecologists to be somewhat worrying and rather baffling. These fields have so much potential crossover that I hope any enmity can be set aside so that robust scientific research and enquiry can be conducted in a collaborative way.

image-20160126-19651-1eko782 — Aedes aegypti. Emil August Goeldi (1859-1917). Source: Wikimedia Commons.

This brings me to Amy Vittor’s excellent and comprehensive assessment of the potential sources of Zika in the Americas and her highly plausible proposition for why we are seeing such high infection rates.⁴ The Zika virus was first recorded in a rhesus monkey in the Zika forest in Uganda in 1947, then in the Aedes africanus mosquito the following year. The virus is now also found to be transmitted by Ae. albopictus and Ae. aegypti mosquitoes. These species are now found throughout the tropics and subtropics and as their ranges have expanded, so too has the possible reach of Zika and other mosquito-borne diseases associated with them. It wasn’t until 2007 that a large-scale outbreak of Zika infecting humans first occurred, infecting 75% of the population of the island of Yap in Micronesia.^{4, 5}

The spread of the virus is in all likelihood the result of human-aided dispersal of both the virus and Aedes mosquitoes. As the virus may not be detected by infected humans (up to 80% of infected people do not show any symptoms)^4,5 and there is currently no cure, it is possible for an infected person to travel to an area where the virus has not been recorded and to spread it to previously unexposed mosquito populations there, so creating new vectors.

zika-virus-epidemiology — Source: Laboratoryinfo.com ⁶

But what has changed to bring about this rapid spread of the disease in the Americas? If we accept that international travel by humans and the worldwide transportation of goods have enabled the means to transport the disease and its vectors, why are we only seeing these effects in the Americas now? There are a combination of further factors that have, as Vittor points out, come together to create the perfect environment for Zika to take hold and spread, including: the creation of more suitable mosquito habitat as a result of deforestation and planting arable crops or urbanisation; climate-change linked increases in temperature and/or humidity in areas that were previously too cold or dry to support mosquito populations; the failure of previous Aedes aegypti population control programmes; and the large pool of susceptible human hosts living in close proximity to each other and to these mosquito-favourable habitats.⁴

Mark Lynas, writing in The Guardian newspaper, also very effectively takes on the various GM mosquito conspiracy theories and then goes on to conclude that innocent lives will be lost if we do not embrace this technology.⁷ Although there is no doubt that mosquitoes are responsible for spreading an array of terrible diseases; the fact that we have created the conditions and opportunities for the mosquitoes and these diseases to extend beyond their historical ranges and infect many more people must surely be accepted as our own responsibility. I think it is a sad indictment of our scientists and ecologists if they cannot (or will not) work together towards an overarching framework to protect people from the effects of our own actions. We need to promote and encourage the use of ‘good science’ to inform our decisions and ultimately our actions.

Further research into and analysis of mosquito ecology is urgently required so that we can more fully understand the implications of mosquito eradication (by genetic or conventional controls) on the various associated ecosystems and diseases. If we do not ask questions about the potential impacts of our proposed actions, we are destined to repeat the same mistakes that have led us to this point. Perhaps, we should also examine the implications of increased habitat loss, climate change and urbanisation, and consider whether we are prepared to live with the consequences or take action to limit the most deleterious effects.

References:

1. Bernish, C. (2016) Zika Outbreak Epicenter in Same Area Where GM Mosquitoes Were Released in 2015 http://theantimedia.org/zika-outbreak-epicenter-in-same-area-where-gm-mosquitoes-were-released-in-2015/

2. Wilcox, C. (2016) No, GM Mosquitoes Didn’t Start The Zika Outbreak. http://blogs.discovermagazine.com/science-sushi/2016/01/31/genetically-modified-mosquitoes-didnt-start-zika-ourbreak/#.VrXcU8eExo4

3. Tickell, O. (2016) Pandora’s box: how GM mosquitos could have caused Brazil’s microcephaly disaster http://www.theecologist.org/News/news_analysis/2987024/pandoras_box_how_gm_mosquitos_could_have_caused_brazils_microcephaly_diasaster.html

4. Vittor, A. (2016) Explainer: where did Zika virus come from and why is it a problem in Brazil? https://theconversation.com/explainer-where-did-zika-virus-come-from-and-why-is-it-a-problem-in-brazil-53425

5. Duffy, R. et al. (2009) Zika virus outbreak on Yap Island, Federated States of Micronesia. New England Journal of Medicine. 360(24):2536-43 http://www.nejm.org/doi/full/10.1056/NEJMoa0805715#t=articleTop

6. Giri, D. (2016) Zika Virus : Structure, Epidemiology, Pathogenesis, Symptoms, Laboratory Diagnosis and Prevention http://laboratoryinfo.com/zika-virus-structure-epidemiology-pathogenesis-symptoms-laboratory-diagnosis-and-prevention/#sthash.BYXGYuyI.dpuf

7. Lynas, M. (2016) Alert! There’s a dangerous new viral outbreak: Zika conspiracy theories http://www.theguardian.com/world/2016/feb/04/alert-theres-a-dangerous-new-viral-outbreak-zika-conspiracy-theories

Genetically modified insects and the precautionary principle

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Last week the Guardian newspaper reported on the findings from the UK House of Lords’ science and technology committee into the development and use of GM insects. According to the committee’s chairman, Lord Selborne:

“GM insect technologies have the potential not only to save countless lives worldwide, but also to generate significant economic benefits for UK plc, where we are an acknowledged world leader.”

No surprises there. The case for GM insects to be developed as a form of vector control has many proponents and seizing an economic opportunity is to be expected from the Lords. Apart from a cursory explanation of the means of developing GM insects, and a mention of the fact that the committee would like to see a reform of European Union regulation around GMOs (more on this later), the reporter fails to consider any environmental issues that may arise from the release of transgenic insects, in what seems to me to be a failure of research and the rehashing of the committee’s summary report.

Thankfully, in an attempt to provide a balanced argument the Guardian also published a piece that was more critical of the report, describing it as “an unsophisticated form of moral blackmail” and laying out the possible extinction risks associated with gene drive systems. The scientific knowledge gap is highlighted by these authors, who write:

“We are not against GM insects. Our point is that we do not know enough. Nobody knows enough.”

Though I commend these authors for responding to the Lords’report in a more critical way, there are still a couple of findings in the report that hadn’t been directly addressed and which I think need exploring further.

The first is the issue of EU regulations of GMOs that the Lords describe as “failing lamentably” and would like to see amended. This critique is aimed at EU Directive 2001/18/EC which states that “due attention be given to controlling risks from the deliberate release into the environment of genetically modified organisms”. This is to be conducted through case-by-case environmental risk assessments, public consultation, a requirement to consult all relevant scientific and ethical committees, and development of “a mechanism allowing the release of the GMOs to be modified, suspended or terminated where new information becomes available on the risks of such release” before consent will be granted. It is a very robust piece of legislation which, when linked with Regulation (EC) No 1946/2003 that restricts the release and transboundary movement of any GMO within EU member states, makes this not “lamentable” as the Lords would have us think, but sound legislation based on the Cartagena Protocol which states that products from new technologies must be based on the precautionary principle and allow nations to balance public health against economic benefits. And which allows countries to ban imports of a genetically modified organisms if they feel there is not enough scientific evidence that the product is safe. It seems to me that an attack on the governing EU legislation is also an attack on the Cartagena Protocol which environmentalists need to be aware of.

The international consensus of the definition of the Precautionary Principle is:

“When human activities may lead to morally unacceptable harm that is scientifically plausible but uncertain, actions shall be taken to avoid or diminish that harm.”

And this brings me to my second concern about the House of Lords report, wherein Professor Rosemary Hails states that:

“the Precautionary Principle properly applied would also take into account the risks of not developing a particular technology and the benefits forgone. It is a misuse of the Precautionary Principle that has led us to this place.”

This reconstitution of the Precautionary Principle is a matter of great concern and has already been discussed at some length by the House of Commons Science and Technology Committee in their Fifth Report: Advanced Genetic Techniques for Crop Improvement: Regulation, Risk and Precaution wherein Sir Mark Walport framed the precautionary principle not as a response to scientific uncertainty, but as a guide to evidence-based decision-making. He said:

“Decisions must be informed by the best evidence and expert advice. The application of the ‘precautionary principle’ can help to guide this. This simple idea just means working out and balancing in advance all the risks and benefits of action or inaction, and to make a proportionate response. All too often, people citing this principle simply overreact: if there is any potential hazard associated with an activity, then it should not be done, or, if it is already being done, it should be stopped.”

By removing the imperative for evidence and advice that is provided to governments to be based on the principles and rigour of scientific enquiry, the report is effectively providing ministers with a means of bypassing environmental legislation. A recent example of this is when George Eustice MP recently cited food security as a reason to maintain the use of neonicotinoid pesticides under this bastardised definition of the Precautionary Principle.

If it were as simple as Sir Mark maintains to identify and stop hazardous activities we would not be facing some of the world’s current health and environmental catastrophes. That is why we must legislate against them and that is why scientific evidence needs to be the basis for that legislation. And when that evidence is lacking or inconclusive, aren’t we safer not taking the risk in the first instance? If, as Prof. Hails maintains we need to consider the risks of not using certain technologies for their potential benefits we have to ask ourselves whose benefits are we talking about.

The Great Pottery Throw Down

The title of this blogpost is taken from the latest BBC television series that has just finished screening in the UK. The premise for this series is based on the model developed for the hugely successful The Great British Bake Off, in which contestants compete against each other day-after-day to produce a variety of baked goods that are then judged by experts. Replace baked goods for ceramics and you will have grasped the intricacies of The Great Pottery Throw Down in its entirety. But what, if anything, is the significance of this to the study of invertebrates?

Well, having recently read Animal Architecture by Ingo Arndt and marvelled at the complexity and ingenuity of animals to create structures such as the heaped nests of wood ants, the towering cathedrals of termites and the delicately partitioned nests of paper wasps; I was rather taken with the notion of insects as ‘makers’. Serendipitously, I stumbled across the website of naturalist and artist, John Walters – specifically across his marvellous illustrations and accounts of Heath Potter Wasps, Eumenes coarctatus.

wasp_november_2009-1 — Eumenes coarctatus. Source: Wikipedia

Potter wasps, Eumeninae, are the most diverse group of Vespidae, with over 3,500 species in 210 genera found throughout the world. Of these, 23 species in 9 genera are found in the UK. They derive their common name of potter (or mason) wasps from the fact that the females tend to construct nests from mud and clay. These nests can take multiple forms, but one of the most elegant (in my view) is the vase-shaped nest of Eumenes coarctatus, the solitary Heath Potter Wasp.

Using heather, gorse or dead grass stems as nesting sites, the female will build her clay vessel over the course of two to three hours. During this time she will repeatedly fly from a water source to a quarry site, where she will form a ball of mud in her jaws, which is then transported to the construction site where she builds the nest. Once she has shaped the neck and lip of the nest she lays a single egg in the chamber suspended on a strand of silk. She will then search for, sting and collect a number of small caterpillars, especially pug and horse chestnut moth larvae, from the heathland vegetation and then fills the pot with them. A final trip to the water source and quarry then provides enough clay to seal the pot with between 9 and 38 paralysed caterpillars trapped inside. A female heath potter wasp may produce up to 25 pots in her lifetime (2 to 3 months) and occasionally she will cluster pots as shown in the series of photographs below. It is possible that these clusters prefigure the development of eusocial colonies as seen in some other vespids.

index.php — Development of a cluster of clay nest cells built by a single Eumenes coarctatus. Bovey Heath, Devon. Photos by John Walters.

When the wasp larva hatches from its suspended egg it drops onto the paralysed prey on which it feeds for about a week before pupating. The emergence of the adult depends on the timing of the building of the pot. If the pot was built before the end of June, the adult wasp will emerge 2 to 3 weeks later; if the pot is built in early July, the adult will still emerge in the same year; however, if the pot is built after this date emergence will be delayed until the following April or May.

potterwasps19july2012boveyheath — Illustration of Heath Potter Wasps taken from the field notes of artist and naturalist John Walters.

Though the E. coarctatus larvae are predatory, the adults feed on the nectar of heathland plants such as gorse, heather, bramble, angelica and alder buckthorn.

nhmsys0000875934-1 — Distribution map of Eumenes coarctatus in the UK. Source: NBN

Found on lowland heaths in England (from South Devon to East Sussex, and north to Buckinghamshire) the Heath Potter Wasp is classified as nationally scarce, though not designated a BAP species.

I also love Jean-Henri Fabre’s description of Eumenes taken from The Wonders of Instinct:

“A wasp-like garb of motley black and yellow; a slender and graceful figure; wings not spread out flat, when resting, but folded lengthwise in two; the abdomen a sort of chemist’s retort, which swells into a gourd and is fastened to the thorax by a long neck, first distending into a pear, then shrinking to a thread; a leisurely and silent flight; lonely habits.”

John Walters has also made a video of a wasp building a nest.

Michael Archer’s Key to British Potter and Mason Wasps is a very useful resource for identifying the various UK species.

The Little Bombardier

Best stay out of the way.

There are more than 500 species of Bombardier beetle (a form of ground beetle – Carbidae) in the tribes Brachinini, Paussini, Ozaenini, or Metriini all displaying the highly effective defence mechanism of releasing a superheated pulsing jet of noxious chemicals sprayed directly at would-be predators. I have always been fascinated by the ammunition of Bombardier beetles – their highly accurate and violent chemical attack brought on whenever you touch them – but it was only on reading Eisner’s essay that I started to fully grasp the incredible complexity of these beetles.

These diagrams are reproduced from Thomas Eisner’s fascinating book For Love of Insects which explores the variety of ways in which insects use chemicals for defence, signalling and prey capture. I cannot recommend this book highly enough for anyone interested in the pursuit of entomology or study of chemical ecology.

Screen Shot 2015-12-04 at 07.33.26 — Diagram of a bombardier beetle with its 2 glands in place. R = reservoir; r.ch = reaction chamber; gl = glandular tissue; dt = duct

Screen Shot 2015-12-04 at 07.38.01 — The mechanism of operation of the bombardier glands. E = enzymes in the reaction chamber; R indicates that either a hydrogen (H) atom or a methyl group (CH3) can occur at that site on the hydroquinone or quinone molecule.

The chemical process involves hydrogen peroxide rapidly decomposing into oxygen and boiling water, while the hydroquinones oxidize into benzoquinone in the beetle’s reaction chambers. This mix explodes out of the beetle with an audible popping sound, in a volley of rapid-fire blasts – in a manner likened to the pulsing propulsion system of Germany’s V-1 “buzz bomb” in WWII. The consequent foul chemical burn (at 100°C) incapacitates smaller attackers like ants, and deters larger predators such as the unfortunate frogs in one of Eisner’s experiments.

By examining the propulsion mechanism using high-speed synchrotron X-ray imaging Eric Arndt from MIT confirmed Eisman and his colleagues’ qualitative passive ‘pulse jet’ model. This research shows that a flexible membrane and a valve passively control the spray pulsation – as pressure increases in the reaction chamber because of the chemical explosion, the membrane stretches and the valve closes. The membrane then relaxes and the valve reopens once the pressure has been reduced following the ejection of the liquid, and so the process repeats.

The only UK resident species of bombardiers are Brachinus sclopeta, the streaked bombardier beetle, and Brachinus crepitans, the common bombardier beetle, and both are rarely seen. B. sclopeta is so rare that it has only recently been accepted as a native species (past records were thought to be of rare migrants) and prior to 2005 had been presumed extinct since 1928. Because the beetles prefer habitats with thin soil, rubble and bare ground they tend to favour brownfield sites and have been found in east London; but with the continuous and unrelenting development of this area, these beetles’ futures are very precarious despite being listed as UK BAP priority species, and considered critically endangered by the IUCN. However, insect charity Buglife worked with developers to secure a site near London City Airport that is now the only known intact colony of the species in the UK. You can read Richard Jones highly informative blog about the relocation and conservation of this species.

Brachinus crepitans, though more common than B. sclopeta, is restricted to Southern England and Wales and especially the coastal areas of the South-East where it is considered nationally scarce. It is more commonly found in continental Europe, central Asia, the Middle East and North Africa, with central Sweden being the northernmost extreme of its range.

Brachinus crepitans. Image source: Wikipedia

Distribution of Brachinus crepitans. Source: NBN Gateway

Usually seen in May and June, the beetle favours calcareous grasslands, arable field margins and chalk quarries. It is usually found in dry, sunny areas – typically under stones. Little is known about its life-cycle, but it is thought that the larvae are external parasites on the pupae of other species of beetle, particularly those of the ground beetle Amara convexiuscula and a staphylinid beetle, Ocypus ater.

I think these gorgeous and enthralling beetles definitely warrant being surveyed for this coming Summer.

References:

Eisner, T. (2003) For Love of Insects. Harvard University Press, Cambridge Ma.
Lyneborg, L. (1976) Beetles in colour. Blandford Press, Dorset.
Bombardier beetle found near Honeybourne. Worcestershire Biological Records Centre (December 2015): http://www.wbrc.org.uk/WorcRecd/Issue11/BombBtle.htm
Isaak, M. 1997. Bombardier Beetles and the Argument of Design (December 2015):
http://www.talkorigins.org/faqs/bombardier.html
Streaked Bombardier Beetle. Buglife (December 2015) https://www.buglife.org.uk/campaigns-and-our-work/streaked-bombardier-beetle
Brachinus sclopeta UK Priority Species Data Collation. Joint Nature Conservation Committee. http://jncc.defra.gov.uk/_speciespages/2093.pdf

Deep-sea biodiversity. A taster.

I want to share an amazing experience with you and to start to think about some of the issues raised in thinking about deep-sea biodiversity.

Back in 2012 I was incredibly fortunate to join an artist, Michelle Atherton, on a 4-hour-long submarine dive off the coast of Roatán, Honduras. We travelled up to 2,000 feet (610 metres) below sea level into the mesopelagic zone. All of the images in this blogpost are stills taken from the artist’s video during this trip.

go-deeper — The submarine, *Idabel*, that would take us on our exciting adventure 2,000 feet into the ocean depths.

Marine ecosystems support approximately half of global primary productivity and a range of ecosystem services operating from local to global scales. It is widely acknowledged that deep-sea ecosystems are the most extensive on Earth, represent the largest reservoir of biomass, and host a large proportion of undiscovered biodiversity (Ramirez-Llodra et al. 2011; Snelgrove et al. 2014; Tyler, 2003).

As sampling techniques and underwater exploration have improved, so the identification of new deep-sea species has grown year-on-year (Levin and Dayton 2009; Miloslavich and Klein, 2009; Ausubel et al. 2010; Danovaro, Snelgrove and Tyler, 2014). There is, however, still a lack of data for the middle waters and deep-sea ecosystems.

Screen Shot 2015-12-03 at 17.11.14 — On a cross-section of the global oceans, the spectrum from red to blue extends from many to few or no records. The records are concentrated near the shores and in shallow waters, while the largest habitat on Earth, the vast middle waters, is largely unexplored. Ausubel et al (2010)

Deep-sea megafauna have evolved a variety of adaptations to deal with the unique circumstances associated with the depths, such as: darkness, cold, high atmospheric pressure, ocean currents and unreliable food sources. This has resulted in peculiar morphological traits such as dark or red-colouration or even translucence to avoid detection; bioluminescence to attract prey often on a ‘lure’ or as a flash to serve as a warning or create confusion. The fauna are also quite often soft-bodied, small in size and sedentary or carried by the motion of the water.

Mnemiopsis leidyi

Bathypterois phenax

Grimpoteuthis sp.

Acanthacaris caeca

Polyp of a solitary octocoral

Squat lobster

Leptostomias sp.

Chaunaax suttkusi

Chaunax stigmaeus

Featured: Chaunax stigmaeus, the redeye gaper anglerfish; Leptostomias sp. dragon fish with bioluminescent chin barbel lure; unidentified polyp of a solitary octocoral; Dumbo octopod Grimpoteuthis sp.; squat lobster surrounded by snake stars Asteroschema sp. entwined with wire coral Cirrhipathes leutkeni; Acanthacaris caeca deep-sea lobster; bioluminescent comb jelly Mnemiopsis leidyi; Suttkus Sea Toad Chaunax suttkusi; and Bathypterois phenax tripod fish resting on the ocean floor.

With the recent discovery of Jurassic deep-sea fossils of extant families in the Austrian Alps providing evidence of colonisation of shallow waters from the deep (Thuy et al. 2014), the deep sea should be considered a biodiversity refugium.

Anthropogenic impacts such as bottom trawling and deep sea gas and oil extraction do, however, pose a significant threat to this biodiversity and ecosystem functioning (Costello et al. 2010; Baker, Ramirez-Llodra and Billet 2013; Ramirez-Llodra et al. 2011). It is imperative that an international conservation framework be agreed and implemented in order to preserve this ecosystem that we are only now beginning to explore.

tumblr_nfstu2PU4C1qbsotxo4_r1_1280 — A group of stalked sea lilies, Endoxocrinus parre carolinae, and three yellow featherstars, Crinometra brevipinna on a glass sponge with anemones on either side.

References:

Ausubel, J.H., Crist, D.T., Waggoner, P.E. eds. (2010). First Census of Marine Life 2010: Highlights of a Decade of Discovery. New York, Census of Marine Life.

Baker, M., Ramirez-Llodra, E., Billett, D. (2013). Preface [in special issue: Deep-Sea Biodiversity and Life History Processes] Deep Sea Research Part II: Topical Studies in Oceanography, 92. 1-8. DOI: 10.1016/j.dsr2.2013.03.040

Costello, M., Coll, M., Danovaro, R., Halpin, P., Ojaveer, H., & Miloslavich, P. (2010). A Census of Marine Biodiversity Knowledge, Resources, and Future Challenges. PLoS ONE, 5 (8) DOI: 10.1371/journal.pone.0012110

Danovaro, R., Snelgrove, P.V., Tyler, P. (2014). Challenging the paradigms of deep-sea ecology. Trends in Ecology and Evolution. 8:465-75. DOI: 10.1016/j.tree.2014.06.002

Levin, L.A. and Dayton, P.K. (2009). Ecological theory and continental margins: where shallow meets deep. Trends in Ecology and Evolution. 24: 606-627.

Miloslavich, P. and Klein, E. (2009). The world conference on marine biodiversity: Current global trends in marine biodiversity research. Marine Biodiversity. 39(2):147-152

Ramirez-Llodra, E., Tyler, P.A., Baker, M.C., Bergstad, O.A., Clark, M.R., Escobar, E., Levin, L.A., Menot, L., Rowden, A.A., Smith, C.R., Van Dover, C.L. (2011). Man and the Last Great Wilderness: Human Impact on the Deep Sea. PLoS ONE 6(8): e22588. DOI: 10.1371/journal.pone.0022588

Thuy, B., Kiel, S. Dulai, A., Gale, A.S., Kroh, A., Lord, A.R., Numberger-Thuy, L.D., Stöhr, S., Bisshack, M. (2014). First glimpse into Lower Jurassic deep-sea biodiversity: in situ diversification and resilience against extinction. Proceedings B of The Royal Society. DOI: 10.1098/rspb.2013.2624

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.²

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.⁷Experimental 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

Timema cristinae, endemic to California has repeatedly evolved ecotypes adapted to different host plant species. One phenotype has no stripe and feeds on Ceanothus (left).

One ecotype features a distinct white stripe on its back and feeds on the thin, needle-like leaves of a shrub called Adenastoma.

cladogram — 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.⁴ 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

phylogeny

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.

crypsis

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).¹¹Although 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.

References:

^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

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