When weapons collide: attempting to understand how exaggerated traits evolve and diversify

It’s been a very exciting week for me, and not just because I am writing this in between thunderstorms while doing field work up in the beautiful Genting Highlands of Malaysia. The results of the Marsden Fund were announced this week in New Zealand and one of the successful projects was one that I was involved in writing, with Greg Holwell as PI, on the evolution of animal weaponry. The best part is that there will be a postdoctoral position available for me back at the University of Auckland next year. It has been a really fun year so far in Singapore, but it hasn’t been so easy for my husband to find work and he is keen to head back to NZ to return to his job there. As any early career scientist can understand, it is hard to find a balance between getting research experience abroad and staying close to partners and family. We made a choice early on to stick together and had recently decided to move back to NZ once my first year at NUS was up, despite not being sure what 2016 would have in store for me professionally. With all this in mind, the timing of our success in the Marsden fund couldn’t be more perfect!

Our project aims to understand more about why weapons are so diverse in animals and will be focused on a fantastic group of invertebrates: the long-legged harvestmen (Opiliones: Neopilionidae) of New Zealand. These curious looking arachnids are found throughout the wet forests of NZ, usually hanging out on mossy tree trunks, on the underside of fallen trees, or in caves. Harvestmen are a type of arachnid, and are often mistakenly identified as a spider, but are actually more closely related to scorpions. Harvestmen can be distinguished from spiders in that their bodies look to be made up of just a single oval-shaped structure, due to the broad fusion between their cephalothorax and abdomen. Spiders on the other hand have a distinctive constriction between their cephalothorax and abdomen. If you want to look really closely you will also notice that harvestmen have just a single pair of tiny eyes on the middle top surface of their body, while spiders have a numerous eyes of varying sizes arranged on the front of their head area (cephalothorax).

Two species of harvestmen from New Zealand highlighting the diversity in chelicerae form

Two species of harvestmen from New Zealand highlighting the diversity in chelicerae form

One of the most striking aspects of the long-legged harvestmen in New Zealand are their hugely enlarged jaws, called chelicerae, that are held out in front of their bodies and look rather terrifying if you didn’t know that they are completely harmless. There are at least a dozen species within this family in New Zealand, and there is a fascinating array of shapes and sizes of chelicerae among the species. In some species the chelicerae are very long and skinny, while in others they are enormous, bulbous and spiny.

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A male Forsteropsalis harvestmen from Wairata near the East Cape of NZ

All arachnids have chelicerae, and in spiders they house the venom glands used during prey capture. Harvestmen, however, have no venom glands and their chelicerae instead are used to cut up their food into nice little bite-sized pieces that they then gobble up. From experience of handling lots of these creatures, I can tell you that the little pincer structures on the tips of the chelicerae are so small and weak that at worst they can give you a cute little nip. It doesn’t hurt and it certainly won’t harm you.

They may look scary but the jaws on these guys are quite harmless...unless you are a (already dead) fly!

They may look scary but the jaws on these guys are quite harmless…unless you are a (already dead) fly!

The use of these chelicerae for food handling is unlikely to explain why they are so huge among NZ harvestmen. Interestingly, in this group it is only the males of each species that have mammoth* chelicerae; females have small, “normal-sized” jaws. This kind of sexual dimorphism is often driven by strong selection on males to evolve structures that allow them to compete with other males, with the ultimate goal to be able to mate with a nearby female.

A female harvestmen with reduced chelicerae

A female harvestmen with reduced chelicerae

Sexual selection, a special type of natural selection where traits evolve to increase an individual’s ability to get more mating opportunities, works under two main mechanisms: intersexual selection where females choose male mates based on their quality or something that they can provide the female (like feeding or egg-laying sites), or intrasexual selection based on direct competition between males for access to females. When there is an imbalance in the reproductive success among males in a species, say because some males are better at gaining the attention of a female or can secure better resources, then this can drive the evolution of traits that increase the success of those disadvantaged males.

The most well-known examples of traits that a male uses to increase its reproductive success are called ornaments. A classic example would be the bright, flashy colours of a peacock’s train that females use to actively choose the best mates. Alternatively, males can bear weapons, such as horns, spines, claws or big teeth that allow them to physically battle with other males. When the disparity in reproductive success between males is really large this can lead to intense competition, which in turn drives strong selection for ever increasingly large weapons that allow males to win fights and more mating opportunities.

My intro slide from Behaviour2015 showing some of my favourite animal weapons

My intro slide from Behaviour2015 showing some of my favourite animal weapons

Scientists have been fascinated with the evolution of exaggerated traits for decades, and we know a lot about the costs and benefits of ornaments and weapons to the males that bear them. However, we still don’t really understand why there is so much diversity in the function and morphology of weapons. In a symposium on animal weapons and competitive assessment** that I recently co-organised at the Behaviour 2015 conference in Cairns, I noticed that although researchers from around the world are working on very different animal systems, we seem to be collectively in awe of the sheer diversity of weaponry (their shape, size, number and presence) both within and among the species we like most. Particularly for groups of closely related species we might expect to see similar adaptations for weaponry because there should be some ideal form that the structure takes that make them ideal for use during fights. However, this is not what we see; even among groups of very closely related species we see an incredible variety of weapons displayed by males, including some species within those groups that don’t have weapons at all.

Dung beetles in the genus Onthophagus are perhaps the best group to highlight this pattern. There are several thousand of different species, of which many display enlarged horns used in fights to control access to tunnels under dung pads where females lay their eggs. There is a staggering amount of variation in the way horns are expressed in this group, with some species producing a single horn from different parts of head or thorax, while others are tiny multi-horned little tanks.

Just one of the many beautiful species of horned Onthophagus beetles (Photo credit: Udo Schmidt)

Just one of the many beautiful species of horned Onthophagus beetles (Photo credit: Udo Schmidt)

Our observations on one species of harvestmen, Pantopsalis cheliferoides, suggest that the main driver of big male chelicerae is through sexual selection, which we discuss in our latest paper out this week in Scientific Reports. During my postdoc with Greg Holwell we set out, with honours students Anna Probert and Daniel Townsend, to gain some basic observational data to confirm our hypothesis that males are using their chelicerae as weapons. In the lab we watched males fighting between each other, firstly in a ritualized manner where they unfolded and extended their chelicerae and waved them rapidly in front of their rival. In more escalated battles the opponents would clash together and tumble about until one male chose to run away.

The most exciting finding from our study though, was that we identified a new type of trimorphism in weapon form. In other animals, it is common to observe huge amounts of variation in size among males, often related to the condition of the individual. In another species of harvestmen, Serracutisoma proximum, found in south-eastern Brazil, there are two distinct male forms (dimorphism): “majors”, which have big bodies and elongated second legs used in territorial fights, and “minors”, which have smaller bodies, shorter legs, and creep into another male’s territory to mate with his female. Males are assigned to either morph in relation to their body size, a trend seen across many other animal species where males possess big armaments. Male dimorphism and the alternative behaviours associated with weapon expression, have been identified in numerous harvestmen species around the world. So, although less well-known than their spider cousins, the harvestmen make excellent model systems for learning more about weapon evolution.

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Majors fighting2 Incredible male harvestmen (Serracutisoma proximum) fighting with elongated legs (Photos used with permission from Bruno Buzatto)

Recently researchers working on other invertebrates have found examples of trimorphism in weaponry, meaning that there are three weapon forms, which can be similarly divided up by looking at the relationship between weapon and body size. Several species of beetle and weta have been shown to have trimorphic males, but little is known about why this polymorphism has evolved and how the behavioural tactics vary between the different male groups. In all known examples of dimorphism and trimorphism in weapons, however, males are split into armed and unarmed groups in relation to their body size, such that small males typically have small weapons (or none at all) while large males have the exaggerated form.

Male Wellington tree weta (Hemideina crassidens) like this one here have enlarged mandibles, but there are actually three different male morphs with varying degrees of mandible exaggeration. (Photo by: Tony Wills)

Male Wellington tree weta (Hemideina crassidens) like this one here have enlarged mandibles (jaws). However, there are actually three different male morphs with varying degrees of mandible exaggeration. (Photo by: Tony Wills)

In our current study, we found that body size was associated with weapon size, in that small males had small chelicerae, and large males had large chelicerae. However, using statistical modelling of different measures of weapon size and how this related to body size, we found that big males could display one of two different exaggerated forms. The most common males that we found in the forests around Waitomo had very long, thin chelicerae that were more than 8 times longer than their bodies are wide. A second morph was smaller in body size with correspondingly small but long chelicerae. Amazingly, we also found a third, rarer subset of males that were large in body size, but displayed short, broad chelicerae. Although shorter in length, these chelicerae are still highly exaggerated, but have enlarged in the opposite direction than the males with long, slender chelicerae. This finding is really fascinating, because we don’t know of any other examples of multiple exaggerated weapon forms within a single species. In all other armed species, males can be divided into a group of males with enlarged weapons and another group of males that lack weapons altogether or have a much reduced form. Our early behavioural observations suggest that the shape of the chelicerae may correspond to different fighting tactics, but we have a lot to learn about the relative advantages of being a male with long slender versus short broad weapons.

Three male morphs of Pantopsalis cheliferoides with different investment in chelicerae size and shape. Illustrations by Emma Scheltema

Three male morphs of Pantopsalis cheliferoides with different investment in chelicerae size and shape. Illustrations by Emma Scheltema

Now that we have the funding to extend this study, I’m really looking forward to being able to explore more about this unique form of trimorphism and what it might be able to tell us about how weapons diverge. While we know from numerous studies on a diverse range of animals that bigger males with increasingly big weapons win fights, we don’t know the role of shape in battle performance. As nicely shown by our group of long-legged harvestmen in NZ, there is often incredible variation in weapon shape among different species. The within-species variation in weapon shape shown by Pantopsalis cheliferoides, however, gives us an invaluable opportunity to figure out the role of weapon shape and how this might lead to divergence.

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* Interestingly, Doug Emlen, an expert on animal weapons, says that although mammoth tusks were undeniably huge, they only made up about 6% of the animal’s body mass. The chelicerae in the harvestmen that we are working on make up about 50% of a male’s body weight, making these weapons some of the most extreme in the animal kingdom!

** On a side note, at the Behaviour 2015 conference it was also really neat to see how many people are now using Twitter to swap stories about the talks and posters they attend. Actually, when I was a bit bored between experiments I counted them and there were 95 tweets about the weapon and contest symposium! You can check out all the tweets from the conference at #behave15.

Further reading:

Painting et al 2015. Multiple exaggerated weapon morphs: a novel form of male polymorphism in harvestmen. Scientific Reports. 5, 16368; doi: 10.1038/srep16368.

If you are interested in weapons you should read Doug Emlen’s new book “Animal Weapons: The Evolution of Battle“. In the book Doug explains the prerequisite conditions that lead to the evolution of weaponry. As well as many careful and detailed explanations about the theoretical aspects of weapon evolution, supported by wonderful examples of armed animals from around the world, Doug also throws in lots of great anecdotes from his adventures as a biologist, including stories of his time as a graduate student which saw him picking through howler monkey dung in search of tiny horned dung beetles. And because I often feel that the minibeasts of the world tend to get neglected in documentaries and public media, I appreciated that Doug showcased lots of examples of weaponry in insects and other invertebrates. It’s a fabulous book written for anyone with an interest in biology and I can highly recommend it.

Incredibly long chelicerae on a male Forsteropsalis harvestmen from Waitomo

Incredibly long chelicerae on a male Forsteropsalis harvestmen from Waitomo

It’s the little things – learning to appreciate our invertebrate fauna

Radio New Zealand National’s critter of the week was the Canterbury knobbled weevil (Hadramphus tuberculatus), described by Nicola Toki as the “stegosaurus of the insect world”. This small but rather adorable looking weevil was once widespread across the Canterbury Plains of New Zealand, but thought to be extinct since its last sighting in 1922. Incredibly, in 2004 Laura Young, a graduate student at the University of Canterbury at the time, rediscovered a population of the weevil among the speargrass she was studying in Burke’s Pass. Like so many species, this charismatic little insect is likely to have been doubly impacted by introduced mammalian predators, as well as a huge loss of habitat as the Plains were transformed into pasture.

The Canterbury knobbled weevil, rediscovered in 2004.

The Canterbury knobbled weevil. Photo by Vikki Smith, from Wikipedia Creative Commons

Despite further surveys completed since the weevil’s rediscovery, no other populations have been found and this species remains listed as critically endangered. A PhD study done on the weevil by Emily Fountain at Lincoln University estimated the population to be 138 individuals in 2009, declining to 76 in 2011.

As Nicola alludes to in the radio interview, insects and other invertebrates unfortunately receive a lot less love and attention from the public than the megafauna such as birds and whales that we perceive to be more charismatic. I wrote a little bit about this in an article for the Maungatautari Ecological Island Trust in 2014 so I thought I would repost it here.

It’s the little things – learning to appreciate our invertebrate fauna

We live in an invertebrate’s world. The famous entomologist E O Wilson observed that when you walk through a tropical rainforest over 90% of the animal body mass around you is made up of invertebrates, and yet we are more likely to notice the birds than the bees. New Zealand is also well-endowed with spineless creatures – insects alone are estimated to number more than 20,000 species compared to 170 bird species*. Our insects have an extremely high rate of endemism (over 90%), meaning they are found nowhere else in the world, and many have bizarre life-history strategies such as flightlessness.

Invertebrates play a key role in the healthy functioning of our ecosystems, but when we pause to admire our natural surroundings we rarely give these animals a second thought. Invertebrates include over 95% of all known species worldwide, so it should be no surprise that we would be in trouble without them. These smaller creatures are responsible for bringing a large proportion of the food we rely upon to our tables through pollination, and play an integral role in the decomposition of organic matter such as leaf litter to promote forest health. Invertebrates are also an important food source for many of our favourite birds and native fish.

Ground dwelling inverts, like this millipede in Waitomo, are integral to healthy forest decomposition

Ground dwelling inverts, like this millipede in Waitomo, are integral to healthy forest decomposition

Although we can appreciate the importance of invertebrates, the huge gap in our knowledge of most species explains in part why they remain a low priority for conservation. Their mind-boggling diversity alone acts as a roadblock because it is hard to know where to begin with setting priorities and developing management plans. Invertebrates are, however, susceptible to the same pressures that our flagship bird species are under, such as habitat loss, introduced species and pollutants, and they are declining at a rapid rate. The recent publicity about honey bee colony collapse disorder affecting much of North America and Europe is testament to this point, and perhaps serves as a very serious wake-up call about why we should care about insects.

For all their challenges, there are opportunities for invertebrate conservation that are in many ways more achievable than efforts to conserve a bird or mammal. Many insect species, for example, only require a small area of habitat to sustain a population, and captive breeding can often be done effectively in a laboratory for much less cost than a vertebrate. New Zealand already has several examples of this, such as 81 hectares of inland sand dunes put aside to conserve the unique habitat of the Cromwell chafer beetle (Prodontria lewisi), and 200 hectares of gorse scrub fenced off to protect a remnant population of Mahoenui giant wētā (Deinacrida mahoenui). Several wētā species are the target of captive breeding programmes, such as the wētā punga (D. heteracantha), which has recently been translocated to Motuora Island from Auckland Zoo.

Not a Mahoenui giant wētā, but a special weta nonetheless. This species is the Raukumara tusked weta was only discovered in 1995. This photo was taken in Wairata on a trip to find harvestmen in 2013

Not a Mahoenui giant wētā, but a special weta nonetheless. This species, the Raukumara tusked wētā, was only discovered in 1995. This photo was taken in Wairata on a trip to find harvestmen in 2013

As a behavioural ecologist, invertebrates are a source of scientific wonder for me, and the fact that they are severely understudied means the opportunities for research are endless. When I began my PhD on the New Zealand giraffe weevil (Lasiorhynchus barbicornis) I was astonished to discover that almost nothing was known about this species, despite being one of our larger endemic insects, and in my opinion one of the most charismatic. Despite providing fantastic opportunities to learn more about our natural world, this situation is common the world over, and is surprising given the relative ease of working on invertebrates in comparison to birds and mammals.

Working on inverts in the forest is fun! Here I am with my field assistants painting and measuring weevils.

Working on inverts in the forest is fun! Here I am with my field assistants painting and measuring weevils in 2011

Adult giraffe weevils are attracted to sick or recently fallen trees, where they aggregate in sometimes very large numbers** to copulate and lay their eggs. The larval stage of a giraffe weevil takes place within wood, where they tunnel around possibly feeding on fungus. It is this larval stage of giraffe weevil biology that has the most important effect on forest ecosystems by aiding in the decomposition of dying or fallen trees. My research, however, focused on adult behaviour, particularly trying to figure out why male giraffe males have such a hugely elongated rostrum (extension of the head). While females use their rostrum to drill holes in trees in which they lay their eggs, males use their rostrum as a weapon, and in some battles like a jousting-pole, where they fight between themselves to secure the best female. The quirky behaviour doesn’t stop there though. If you watch an aggregation of these creatures carefully enough, you might spot a couple of very small males hiding underneath a mating pair or trying to squeeze themselves in between a large male and his female. This sneaking behaviour seems to have allowed small males to gain just as many mating opportunities as their larger foes. My ongoing research aims to continue to peel away the layers of this fascinating story, while also delving into the world of some of our other invertebrate species in an attempt to do my small part to increase our understanding of the smaller but no less wonderful species that co-inhabit this earth.

Male giraffe weevils use their elongated heads and enlarged jaws to fight among themselves for females

Male giraffe weevils use their elongated heads and enlarged jaws to fight among themselves for female

*The number of native New Zealand birds varies depending on the source you use, but suffice to say there are a lot less bird species than insects! Check out the fantastic New Zealand birds online for more information.

** Using coloured paint combinations to accurately identify individuals, I once counted over 100 adult giraffe weevils aggregated on a single tree in one day at my field site in West Auckland. Although thought to be an uncommon species, my field work around NZ showed that this species is actually a lot more widespread and far less rare than previously thought.

Getting wrapped up in Sixteen Legs

A quick update from here in the spider lab! Last week we had visitors from the Bookend Trust in Australia who are putting together a documentary called Sixteen Legs. The project (actually it is a suite of projects) is a fantastic collaboration between scientists, artists, writers, school kids and performers. The documentary will showcase cave fauna, and more specifically, the bizarre biology and behaviour of the Tasmanian Cave Spider (Hickmania troglodytes) .

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A beautiful Tasmanian cave spider (Photo: Joe Shemesh/Bookend Trust, used with permission)

The Tasmanian Cave Spider are huge spiders with leg spans up to 18 cm! They belong to an ancient, relict group (the Hypochiloidea) which dates back to Gondwanaland.

Tasmanian cave spiders are troglophiles, meaning they are adapted to live mostly in caves or in neighbouring dark places like hollow logs, although unsuspecting humans do occasionally find them in their bathrooms. Animals that live permanently in caves are called troglobites, and cannot survive away from their cave habitat.

Troglofauna often have special adaptations to living in dark habitats such as a loss of skin pigmentation and eyesight. To cope with living underground they may have increased sensitivity to smell, hearing and touch. Monsoscutid harvestmen (Opiliones) found in the cave systems of New Zealand have a unique adaptation to allow them to find food in such dark places. Unlike most harvestmen, these species have relatively well developed eye sight that allows them to orientate to the shining light of glow worms; their favourite prey.

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A harvestman in the genus Forsteropsalis found in the caves around Waitomo, New Zealand

Niall Doran and colleagues have been studying the biology of the Tasmanian Cave Spider for 20 years and have revealed some incredible aspects of their natural history that makes the basis of the Sixteen Legs film. The courtship behaviour of this species is a particularly drawn-out but fascinating process, sometimes lasting more than 5 hours. Males locate females, probably using smell given their dark location, and then proceed to pluck the web with his first two pairs of legs to attract the female’s attention.

A female cave spider on her web (Photo: Joe Shemesh, used with permission from Bookend Trust)

A female cave spider on her web (Photo: Joe Shemesh, used with permission from Bookend Trust)

Once the female appears convinced by the male’s courtship performance and chilled out sufficiently for the male to approach further, mating begins. This is a rather complicated arrangement, involving the male attempting to lock the female’s front legs together with his own legs. Although smaller in body size, males have elongated forelegs that play an integral part of their mating rituals. Once the female is locked in place, males use their very long second pair of legs to secure the female further, using a little crook on the legs to embrace her around her chelicerae (jaws). This locks the female’s jaws apart so she cannot attack the male while he is in such a vulnerable position.

The stage is now set for successful sperm transfer, which the male does by inserting one of his palps (a modified leg-like structure that holds sperm) into the female’s genital opening on the underside of her abdomen.

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A female spider locked in place for mating by the males crooked legs around her jaws. Photo from Doran et al 2001 J Zool 253: 405-148

A male Cosmophasis jumping spider showing his bulbous palps (the white structure on the front of the body) used to transfer sperm

A male Cosmophasis jumping spider showing his bulbous palps (the white structure on the front of the body) used to transfer sperm

This beautiful dance played out between the couple is not the only interesting aspect of their natural history. After mating, female’s create a large silken egg-sac that hangs from the cave wall. The egg-sac is double-layered meaning that the eggs themselves are housed in a separate compartment from the outer sac wall, which keeps them protected from fluctuations in humidity and from possible fungal and bacterial infection. This turns out to be really important because the eggs have an incredibly long gestation time; it takes nine months for them to develop, just like a human baby!

As well as telling the story of the Tasmanian Cave Spider and their cave-dwelling friends, Sixteen Legs will include tales from people and their perspectives of spiders. From arachnophobes to the scientists that dedicate their lives to studying spiders, Sixteen Legs will cover it all. On their way back from filming a few scientists and celebrities in the UK, the team stopped in at NUS to chat to me and Chia-Chen Chang, another PhD student in the Li lab. We talked about my current spidery research as well as my previous work on harvestmen in the caves and forests of Waitomo, as well as how I actually ended up being interested in arachnids.

Being interviewed by Craig Wellington for the Sixteen Legs documentary

Being interviewed by Craig Wellington for the Sixteen Legs documentary

Showing the team how cute jumping spiders are; a great cure for arachnophobes?

Showing the team how cute jumping spiders are; a great cure for arachnophobes?

You can get updates about the progress of the documentary on their Facebook page or follow the Bookend trust on Twitter.

For more detailed information about the behaviour of the Tasmanian Cave Spider, which is where I got all the stories from for this blog, check out the paper in Journal of Zoology: here.

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Photo used with permission from the Bookend Trust

Behaviour 2015 Symposium – Animal Contests: Assessment and the Evolution of Animal Weaponry

I’m excited to have co-organised a symposium on contest assessment and animal weapons at the Behaviour 2015 meeting about to kick off this Sunday night.

Greg Holwell and I wanted to have the chance to get researchers in this field together to talk about our most recent projects and hopefully discuss some avenues for new direction and collaborations. For me it was an exciting chance to get in touch with researchers that I became aware of during my PhD days and finally get the opportunity to meet in person.

We have some great speakers lined up covering a really broad range of topics within the greater context of animal contests and the evolution of weaponry. We’ve divided speakers up roughly such that the first 1.5 sessions will be mostly those talking about weaponry, while the third session will focus more about contests and assessment theory.

If you are at Behaviour 2015 please come and join us for what will be a great symposium.

Where: Room 8 Cairns Convention Centre

When: Thursday 13th August from 11:30 to 6pm.

The last 15 mins (5:45pm) will be a discussion session, and I hope the talks we have listened to will help solve problems and spark lots of new ideas.

We’ll be tweeting with the official #behave15 hashtag! (and we might add our own symposium related one TBD)

Here is the list of our speakers (in order of appearance) with their website links where possible:

Doug Emlen (11:30) – Extreme animal weapons – the importance of duels

Erin McCullough (11:45) – Structural adaptations to diverse fighting styles

Christina Painting (me! 12pm) – Weapon polymorphism in arthropods

Glauco Machado (12:15) – Variation in weaponry over large geographical scale

Bruno Buzatto (1:30pm) – Coevolution of weapons and testes

Leilani Walker (1:45pm) – Contests & weaponry in sheet web spiders

Kevin Judge (2pm) – Evolution of weaponry in North American field crickets

Clint Kelly (2:15pm) – Effect of immune challenge on weapon performance

Devin O’Brien (2:30pm) – Stabilizing selection on weapon size in frog legged beetles

Tobin Northfield (2:45pm) – Induced defense in scorpion venom

Sophie Mowles (3pm) – Using CT scanning to investigate multimodal assessment signals

Stephen Reber (3:15pm) – Acoustic rival assessment in crocodilians

Alexandra Schnell (4pm) – Contests in giant cuttlefish

Rowan McGinley (4:15pm) – Assessment strategies in jumping spider fights

Irene Camerlink (4:30pm) – Aggressive personality & fighting

Tomasz Osiejuk (4:45pm) – Soft song & predator presence in ortolan bunting

Daniela Perez (5pm) – Handedness in fiddler crab fights

Tsuyoshi Takeuchi (5:15pm) – Erroneous courtship hypothesis

Max Ringler (5:30pm) – Acoustic ranging in poison frogs

I’m going to be talking for the first time about some of the work done on harvestmen polymorphism during my first postdoc with Greg Holwell. We found exciting patterns of weapon expression in a species of harvestmen found in wet forests in the North Island of New Zealand. More about this soon or come along and hear my talk!

Weapon polymorphism in arthropods_front slideSee you there!

Spiders at the Xishuangbanna Tropical Botanic Garden

June was a busy month for the spider lab. After a week spent frantically setting up all our new spider pets in the lab and getting experiments underway we packed our bags again and took off to south west China. Our destination was the Xishuangbanna Tropical Botanic Garden (XTBG) which is found next to a small town called Menglun in the Yunnan province. The gardens are so well tucked away in the south west corner of China that you can just about peek over the border to Laos, with Myanmar not far away on its western side either.

XTBG is surrounded by a large river, with multiple bridges crossing it at various points, connecting both the local town and the large research institute associated with the gardens. We stayed in a hotel in Menglun and walked each day across a big suspension bridge into the garden after a delicious breakfast of rice noodles in a soup packed with herbs and spices.

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View from the suspension bridge to the gardens (left), Daily breakfast of rice noodles with herbs & spices (right)

One of our goals was to collect Siler semiglaucus jumping spiders, the focal species for PhD student Zeng Hua. Siler are tiny but covered in intricately colourful patches. Zeng Hua doesn’t know yet what the role of all these colours are but she aims to find out and is particularly interested in how they are used by males to advertise to females during courtship. Siler semiglaucus and other species in this genus are quite common around much of South East Asia and China, including Singapore, and worth keeping a look out for next time you are in this part of the world. Keep your eye out on park-land shrubs and trees; we’ve had particular luck finding them in long grass.

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Siler semiglaucus male (left) and female (right). Note the fluffy patches on the males forelegs that he waves around during courtship.

During our time at the gardens we were hosted by Prof Yang Xiaodong, a scientist based at the XTGB Chinese Academy of Sciences. Daiqin and I were both invited to give seminars about our research, and luckily I had a few slides on the ready so took Prof Yang up on the offer. The only problem was that not only was I lacking any professional looking clothes to wear, the clothes I did have smelt like I had been in the field for days (because I had), but hopefully the giraffe weevil videos distracted everyone.

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Hopefully not boring everyone about giraffe weevils & their friends

After our talks we were invited to an amazing banquet with a bunch of other scientists based at the XTBG. This was just one of many feasts we took part in during the week including a wonderful spread put on by ladies at a local Dai restaurant. Dai people are an ethnic minority in China and live predominantly in the Xishuangbanna area. Here they eat a lot of delicious wild vegetables (fern fronds, various roots etc) with their staple sticky rice. I also found their housing really interesting too, which usually comprised of two stories with the upper level dedicated to living space and the lower level used for storing livestock (we mostly saw chickens), food and transport.

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Preparing the 3 types of sticky rice (left), Enjoying Dai food on our last evening in XTGB (right)

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A Dai village near Menglun

One of the highlights of the trip was discovering the fireflies flashing their glowing abdomens as they emerged during the evenings on our walks home from the gardens. Fireflies have a slightly misleading name, because rather than being a fly, the mysterious glowing light belongs to several types of beetle families including the Lampyridae, Phengodidae, and Rhagophthalmidae. All of these beetles belong to the larger super family of Elateroidea, of which most familiar to many would be the click beetles. Fireflies use their distinctive flashing signals to locate mates of the right species, which is important when several species are flying around at the same time. Unfortunately I didn’t get any pictures but can recommend this great video which shows timelapse videos of fireflies in the night sky.

Another fun find was this ant-mimicking crab spider (Amyciaea forticeps). Like so many spiders, this species mimics ants and in this case the mimicry is specific to weaver ants (Oecophylla smaragdina). Morphological adaptations to looking ant-like are called myrmecomorphy and there are hundreds of examples of these among spiders.

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Ant-mimicking crab spider – check out the eye spots on the spiders abdomen (right)

There are several Amyciaea species like the one we found in China around the world, and there are multiple species that mimic Oecophylla smaragdina. In Australia this species of weaver ant has green gasters (the bulbous bit at the end of an ant’s body), but in Asia the gasters are red. Interestingly, the colour of the crab spiders in these two regions of the world match the colour of the ants; in Australia A. albomaculata is green, while in Asia other Amyciaea are orange/red (like the one we found, above).

Although not much work has been done on Amyciaea spiders, they appear to be “aggressive mimics“. This means that they mimic weavers ants so that they can blend in among an ant colony and use these ants as food. As well as matching the colour of weaver ants, Amyciaea also have two black dots on their abdomen which look like ant eyes and move in a jerky ant-like fashion.

Aggressive mimicry among spiders is not very common; most examples are considered Batesian mimics, where the spiders look like ants to avoid predators. Many predators have a strong aversion to ants because they can be dangerous; they can sting, bite and spray acid as well as  being able to recruit their nest-mates to launch an attack on invading predators. Ants, therefore, are a useful model for a spider to look like if it means avoiding a larger suite of predators. One of the most predominant groups of Batesian ant-mimicking spiders are the Myrmarachne, of which there are about 200 species.

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Two species of Myrmarachne that we collected in Malaysia

We commonly see Myrmarachne around Singapore, and on both of our spider collecting trips abroad. Like many ant-mimicking spiders, Myrmarachne have a constricted “waist” (their abdomen has a narrow part) and they usually wave their front legs to resemble ant antennae. The way they move is also distinctly ant-like, in that they run in jerky little bursts. All of this make them really tricky to distinguish from an ant and it has taken me a while to be able to spot them among their ant models.

Myrmarachne also tend to be highly sexually dimorphic, meaning that the males and females look different. Among these ant mimics the dimorphism is due to males often having very enlarged chelicerae (jaws), while in females they are comparatively reduced. These enlarged chelicerae sticking out of the front of a male’s head should make them less convincing mimics. However, it is hypothesised that males are still able to deceive potential predators by looking like an ant carrying something in its mouth (like a seed or piece of dead insect).

Sure enough, when Ximena Nelson and Robert Jackson at the University of Canterbury looked at predation rates on male versus female Mrymarachne spiders, they confirmed that males are still convincing mimics. Both male and female Mrymarachne were avoided by Portia, a spider which will hunt other spiders but avoids ants. However, when they did a similar experiment presenting Mrymarachne to an ant-eating spider they found that males were targeted more often than females, probably because they are perceived to be an easier catch by looking like an ant weighed down with food.

Not all ant-mimicking spiders look very convincingly like their models. Orsima ichneumon, the jumping spider from Malaysia that I am working on at present, has various ant-like features such as a constricted abdomen and erratic movement when running around the vegetation. They also have very elongated spinnerets (silk producing structures) at the tip of their abdomen which point in different directions such that one set looks like insect mouthparts, and the other like antennae. As the spider moves the spinnerets bob up and down on the substrate they are walking on making their rear-end look quite convincingly ant-like. These adaptations aside, what really makes Orsima stick out is their incredible colouration. These colours certainly take away from their ant-like appearance, and I am interested in how these colours (as well as their other morphological adaptations and behaviour) are selected for; what is important for mate choice (i.e. what are lady Orsima interested in) and what is used to avoid or deter predators? Hopefully I’ll know more about that soon!

Orsima ichneumon - an ant-mimicking spider?

Orsima ichneumon – an ant-mimicking spider?

Following the pipeline trail

Since we returned from China a couple of weeks ago (more on that in the next blog) I have been trying to get stuck into experiments. Although it is exciting to be collecting data, I’ve been locked in a windowless room most days and feeling a bit desperate to get outside for some fresh air. What better excuse to escape the lab than the need to head to the field for more spiders!

Unfortunately, the jumping spiders I’m working on (Orsima ichneumon) are not widely known from Singapore. They have been recorded here though, and so Caleb and I set off to Upper Peirce Reservoir in the central catchment on advice from Joseph Koh (local spider expert) who found one there some years ago.

upper pierceJoseph recommended following an unmarked trail where a series of pipelines cut through the forest. Orsima seem to like edge habitat like this and in Malaysia we had most luck finding them in areas where it was shady but got some sun. They particularly seemed to like hanging out on ginger fronds covered in vines.

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The pipeline trail at Upper Peirce Reserve

Despite much beating and searching we didn’t have any luck on our quest for Orsima today, but we still had a lot of fun. For the first time on any outing in Singapore we didn’t see another human soul on the trail. Also, despite it recently feeling a little quiet in the forest we spotted and heard lots of wildlife including a baby clouded monitor, greater racket tailed drongo, bee eaters, tailor birds and macaques. One of the mama macaques was even nursing a tiny baby and posed long enough for a photo.

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Long tailed macaque mama with baby

Of course, loads of beautiful spiders fell into our umbrellas as we were beating, but the find of the day was something I had never seen before – a mantidfly! This is one of the strangest insects I have ever seen, being a confusing blend of mantid and wasp. Techincally, mantidflies are not flies either – they are lacewings (Neuroptera). This particular species is a pretty convincing wasp-mimic, with its yellow and black patterning. Like a mantid, it has modified (raptorial) forelegs for capturing prey which Caleb tested out by feeding it a fly. This exciting find reminded me how incredibly diverse the invertebrate world is and how much more I am yet to see – it is so great to get a surprise everytime we go out.

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Wasp-mimicking mantidfly, wow!

mantidfly2Here are just two of the many jumping spiders that we spotted today. We saw a lot of the very cute bumblebee jumpers as well as a couple of different Telamonia species including this bright yellow and orange one.

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Bumblebee jumper (Omoedus ephippigera), Telamonia sp.

While it wasn’t an entirely successful trip I’m hopeful that we will eventually find the elusive Orsima in Singapore, and our finds today made it feel like it was worth the day away from the lab.

Searching for Orsima jumping spiders but finding other treasures instead

Searching for Orsima jumping spiders but finding other treasures instead

Congratulations Bex!

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The world isn’t done hearing about giraffe weevils just yet!

Rebecca Le Grice finished her Masters at the University of Auckland in February under supervision of Greg Holwell and myself looking at competitive assessment, lifetime mating success, mark-recapture and other fun things on giraffe weevils. Bex has just been awarded an A+ and 1st Class Honours for her work – this is very much deserved for all her hard work, both in the field and back in the office doing some pretty complicated analyses.

Congrats Bex, looking forward to some great publications from your work.

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Here’s Bex enjoying a nice cup of tea at her field site (Photo: R Le Grice)

City living and jungle escapes in South East Asia

Singapore is a puzzling place to live. I am truly enjoying the diversity in culture, food and having the opportunity to do science in a new part of the world. But sometimes I feel like we are living in a bubble. Perhaps it is partly because it has been difficult to make friends here and so we spend a lot more time doing things as a couple than we might have at home. It could also be something to do with the constant temperature and humidity that never really waivers and makes me feel like I should be on holiday instead of going in to the office each day. Maybe too it is just that we haven’t been here long enough to feel like we belong and are still busy discovering new places to eat and explore without building much of a routine.

Whatever the cause, come the weekend I am desperate to get away from all the towering apartment blocks and find a quiet place to walk. This is pretty hard in Singapore and I am embarrassed to say that the kiwi in me gets a little annoyed when having to share a track with large numbers of other people. But then I think how nice it is that so many others are enjoying their weekend in the bush and I try to focus on the bird calls rather than the people. For a tiny and highly developed island, Singapore has a surprising number of wildlife to spot when exploring the remaining rainforest and urban parks. For my birthday recently, we took a trip to Sungei Buloh Wetland where Caleb outdid himself by spotting 3 different species of snakes, including a baby mangrove pit viper. (click on any of the photos to enlarge)

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A juvenile mangrove pit viper (Cryptelytrops purpureomaculatus) and an oriental pied hornbill (Anthracoceros albirostris) at Sungei Buloh Wetland

A huge bonus about working as a behavioural ecologist in Singapore is getting to do your field research in neighbouring tropical places. Our lab group recently took a road trip around Peninsula Malaysia in search of our various spidery study species, and Caleb got to come along as our trusty field assistant. We spent most of our time around the University of Malaya Gombak Field Station which is located in the foothills inland from Kuala Lumpur. Having breakfast on the deck over-looking the jungle is up there with my all-time favourite activities, especially when naughty long-tailed macaques spy at you from the trees.

I’ve recently started a new project on a magnificent jumping spider, Orsima ichneumon. This species belongs to the same subfamily that our lab does most of its research on, and I couldn’t help but jump on it myself when I found out that very little is known about its biology. Look at those colours and the strange ant or wasp-like morphology!

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The wonderful Orsima ichneumon

Unlike in temperate areas, finding enough study specimens in the tropics can be a bit tricky, where diversity is incredibly high but abundance of each species typically lower. However, we eventually found a great spot of weedy undergrowth and shouts a plenty of “got one!” rang out in chorus with the pleasant sound of bush whacking. Here, my boss also introduced me to the use of an umbrella as a beat sheet (advocated by Joseph Koh in his book on Bornean spiders) – a rather genius invention for use in the wet tropics and can be very handy during sudden downpours!

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Happy spider collectors on a jungle path

Until recently I wasn’t a big fan of beating as a collection method as I’ve always enjoyed the challenge of spotting things by eye. I’m converted now though and like a colleague recently said to me, it’s like discovering treasure when you peer into the umbrella. Not only did we discover many jumping spiders, but also lots of adorable beetles.

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Beetles from the beat sheet

In the evenings Caleb cracked out his macro photography set up and we catalogued the day’s findings.

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A selection of salticids

I should also mention that we spent a lot of time eating splendid Malaysian food. It’s hard to choose favourites but I have a new fondness for stinky petai beans and anything with copious amounts of sambal (chilli sauce). Also for anyone following Caleb’s adventures with satay, don’t worry – he got his fill of that sweet peanut sauce on chicken on our last night in Kuala Rompin.

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Left to right: Petai beans being prepared at a seafood restaurant in Kuala Rompin, Lunch in the Cameron Highlands, Corn on the satay coals

Overall it was a very successful trip. I can finally get some experiments underway back in the lab now and have returned feeling really refreshed after the break from city life. There may have been a lot of mosquitoes, leeches, spew-breaks and scratches (and even a mystery insect spray burn on my eyelid) but there is nothing like a good week in the bush to make you feel like we live on a pretty special planet.

chrissie in the jungle

Taking time out to watch birds at the Gombak Field Station

Horseshoe crabbing in Singapore

Last Saturday Caleb and I took part in a nationwide census of horseshoe crabs around Singapore. Since moving to a new country with such diverse wildlife we wanted to get involved in events which help us learn about local wildlife and conservation issues. This is the third survey organized by the Nature Society of Singapore since 2010 and aims to monitor horseshoe crab populations at 9 sites across the island. The society are particularly interested in how factors such as habitat loss, algal blooms and the fishing industry could be having on declining populations.

What is a horseshoe crab?

Despite their name, horseshoe crabs are not crabs and they aren’t even a type of crustacean. Instead they belong to the subphylum Chelicerata which also includes the more commonly encountered arachnids (spiders, mites, scorpions). Horseshoe crabs themselves belong to a special group of very ancient marine arthropods from the order Xiphosura, of which they are now the only living members of an ancient and otherwise extinct group.

Horseshoe crabs around Singapore

Two species of horseshoe crabs can be found in the waters around Singapore – these are the mangrove horseshoe crab (Carcinoscorpius rotundicauda) and the larger coastal horseshoe crab (Tachypleus gigas). They can be distinguished easily by looking at their “tails” (also known as telsons or caudal spikes), which are used to help them cruise around underwater and to help them right themselves if flipped over. The tails of coastal horseshoe crabs are triangular in cross-section and serrated and can be compared to mangrove horseshoe crabs which are round and smooth. Wild Singapore has some great info and pictures on how to tell them apart here.

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Mangrove horseshoe crab (Carcinoscorpius rotundicauda) & Coastal horseshoe crab (Tachypleus gigas) (Photos: Wikimedia Commons by Amada44 & Shubham Chatterjee, respectively)

Little is known about the biology of the two species found in Singapore but it is thought that unlike the American species which is famous for its annual mass spawning on sandy beaches along the Atlantic coast, the local species here probably breed year round.

The survey at Seletar Reservoir

Our work at Seletar Reservoir involved getting into teams and moving up and down the mud flat to survey for horseshoe crabs. It didn’t take long before we found out that the mud is extremely deep here (several stuck gumboots) and so it was actually pretty difficult to effectively survey the site. A huge thunderstorm also abated plans a bit, but after hiding out in a fisherman’s hut we ventured out to check out some of the fishing cages along the jetty.

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Some of the volunteer students checking out the stranded horseshoe crabs in fishing cages

Here we found 18 horseshoe crabs that had been trapped inside two fishing cages. Luckily they were all still alive when we pulled them out so we took some quick measurements and sexed the animals before releasing them back onto the mud.

IMG_0020We had to distinguish between male and females by flipping the crabs over to check out their undersides. Males can easily be identified by looking at their front legs (pedipalps) which are swollen at the ends to resemble little boxing gloves. These are used to latch on to females for mating. The pedipalps of females look the same as their walking legs. Males are also generally smaller than females for all species of horseshoe crab.

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Ventral view of mangrove horseshoe crabs: male on left with swollen “boxing gloves” near tip of pedipalps compared to females on right that have normal legs

A few brave souls also jumped into the deep mud beyond the jetty and found two large female mangrove horseshoe crabs with males attached. Both of these females had multiple satellite males hanging around, probably trying to fertilize eggs that the females were depositing in the mud (see Interesting Mating Behaviour below).

Threats to horseshoe crabs around Singapore

Populations of horseshoe crabs around Singapore are unfortunately declining, probably in large part due to loss of habitat around coastlines. Land reclamation has resulted in a loss of sandy beach habitat for the coastal species of horseshoe crab, so much so that this species is rarely sighted in Singapore now. Mangrove forests too have declined from 13% of Singapore’s land area to just 0.5%, leaving very few breeding sites left for the mangrove horseshoe crab.

The Nature Society also spends a lot of time pulling horseshoe crabs from fishing nets where they are accidentally stranded and risk death due to exposure at low tides.

Blue blood and the biomedical industry

Horseshoe blood is an incredible blue colour, due to the oxygen-carrying part which is called hemocyanin and contains copper. Vertebrates, on the other hand, have hemoglobin which contains iron, giving oxygenated blood its more familiar red colour.

horseshoe crab blood

Horseshoe crab blood (Image from PBS Nature documentary “Crash: A tale of two species”)

Horseshoe crab blood has become an extremely valuable tool in the biomedical industry. In the 1960’s it was discovered that horseshoe crab blood will clot when it comes into contact with bacterial endotoxins, effectively closing off the bacteria and preventing any further infection. Similarly for humans, bacterial endotoxins can be very dangerous, especially if they enter our blood stream which can happen during medical injections. Since the 1970’s, horseshoe crabs have been collected, harvested for their blood and used in LAL tests (Limulus amebocyte lysate). Any potential contamination in drugs for intravenous use will be detected during these tests because of the way the blood coagulates and forms a gel around the contaminant. From what I can see online, EVERY drug is tested using horseshoe crab blood which is truly amazing.  I had no idea before writing this blog that human medicine relies so greatly on these ancient creatures of the sea!

Check out this short clip from PBS Nature to learn more about how horseshoe crabs are used in the biomedical industry.

Interesting mating behaviour

I first learned about horseshoe crabs when reading work by Prof. Jane Brockmann from the University of Florida. Since 1989 Jane has been working on the American species of horseshoe crab (Limulus Polyphemus), which is found along the Atlantic Coast and in the Gulf of Mexico. Given my research background studying sneaky versus fighting male giraffe weevils, I found the mating behaviour of horseshoe crabs fascinating.

Jane and her team identified that males use two different mating tactics – younger males in the best condition attach themselves onto females and ride on to the beach with their partners, giving them the best chance for fertilization. Older males or those in poor condition adopt an alternative behaviour coined “satellite behaviour” which involves crowding around male/female pairs on the beach during spawning in an attempt to father a proportion of the eggs fertilized. This tactic is possible because females lay thousands of eggs into the sand which are not fertilized until males release free-swimming sperm – resulting in a huge amount of sperm competition between males.

Surprisingly, Jane found that satellite males are able to gain a large proportion of the paternity of offspring (on average 40%), demonstrating that it is worth the risk of possible death to engage in this battle for fertilization (unattached males are more likely to be flipped over in the waves, stranded by outgoing tides and eaten by migratory birds!).

Recent work by this team have reveled the interesting and complex trade-offs involved with being an attached versus satellite male. For example, although attached males have a greater overall mating success, they also suffer costs involved with their mating tactic such as being unable to feed as easily resulting in nutritional stress.

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Thanks to the Nature Society of Singapore for letting Caleb and I tag along and learn a lot of interesting things about a species we had never encountered before. If you are in Singapore and want to volunteer to help the society with their rescue missions you can find information here.

Further reading

Nature Society Horseshoe Crab Research & Rescue Programme: details about the project can be found here as well as links to some great articles written about the plight of horseshoe crabs around Singapore

Fact sheet from Wild Singapore: general information as well as helpful guide to distinguishing between the two species found in Singapore

Lots of information about horseshoe crabs by the Ecological Research & Development Group including anatomy, natural history, research etc. Most research has been done on the American species but you can spend ages on this site learning lots of neat things about horseshoe crabs.

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Sunset over Seletar Reservoir at low tide

Drawings by Emma Scheltema

Last year the Holwell lab was lucky to meet Emma Scheltema, who was kind enough to do a bunch of illustrations for us of our various study species. I’m looking forward to including her work in our upcoming publications.

You can see some of her beautiful work here but for her full portfolio you should check out her website.

malesfighting_shaded_gscale_webverTwo male giraffe weevils grappling  – one of Emma’s creations