"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

August 3, 2015

Hymenoepimecis argyraphaga

Those who have been reading this blog for a while realise that August is the month when I featured some guest posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class.  One of the assessment I set for the students is for them to summarise a paper that they have read, and write it in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2015. To kick things off, here's a post by Alison Cash on a paper published in 2001 about a parasitoid that uses its spider host to weave a tangled web.

Left: The usual web constructed by a Plesiometa argyra. Right: A web constructed under Hypmenoepimecis' influence
Photo from this paper.
The parasitoid wasp Hymenoepimecis argyraphaga can be considered to be pretty unremarkable at first glance. However, the life history of this killer insect contains more drama and intrigue than an episode of Game of Thrones - maybe with just a little less incest. This wasp is found in the tropical forests of Costa Rica. Here, when an expectant mother wasp is prepared to lay her solitary egg, she seeks out one particular species of orb-weaver spider - Plesiometa argyra.

This spider is known for its elaborate web-spinning abilities, with which it uses to capture its prey. Each day, it meticulously recreates its skilled masterpieces and for this talent H. argyraphaga targets it with the burden of raising its life-sucking young. The larva of this wasp not only makes a meal of the spider, it also turns the unfortunate arachnid into its personal slave via mind control - using it to create a perfect haven to pupate.

When the female wasp locates a P. argyra, it temporarily paralyses its victim with a sting before it glues an egg on the spider and leaving. After 10-15 minutes, the spider wakes out of its stupor, and resume life as normal, apparently unaware of its new and sinister backpack. The egg soon hatches and the larva anchors itself to its spider host, riding it triumphantly for the next two weeks, all while feeding on the spider's blood (call hemolymph) from small holes it has punctured in the host's abdomen.

Once the larva has matured and is ready to begin its transformation into an adult wasp, the relationship becomes more menacing. The larva injects the spider with a cocktail of chemicals that alters its web-weaving behaviour. Under this influence, the spider custom-build a unique reinforced web, fit to encase the wasp larva in its a cocoon while it metamorphoses. Once the spider had completed this highly altered web, the spider moves to the center of the web where it remains somewhat dazed. The wasp larva then dismount from its naive eight-legged steed, then kills it and suck the corpse dry for its last supper as a larva. It then weaves a cocoon which nestles securely in the middle of the web, suspended away from potential threats. After ten days, the adult emerges to begin the grisly cycle once again.

What sets this wasp apart from many other parasitoids is that it modify the host's behaviour, via an injected chemical cocktail, in such a specific and detail manner. Instead of weaving the usual intricate five-step web, P. argyra is reduced to repeated the first two step of web construction. The scientist who conducted this study observed that by blocking the ability to construct the multi-step web, the result was a "custom-built" structure which is more durable and less likely to be damaged by falling debris. Even when the larva is removed from the spider before it is able to kill its host, the webs made by the previously parasitised spiders are still malformed for the following few days, but eventually return to normal, which suggest that the behavioural change is induced by a chemical rather than just physical interference by the parasitoid larva.

By chemically inducing this altered host behaviour, H. argyraphaga ensures that it will successfully raise another generation of spider-enslaving wasps.

William G. Eberhard. (2001). Under the influence: Webs and building behavior of Plesiometa argyra (araneae, tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (hymenoptera, ichneumonidae). Journal of Arachnology, 29(3), 354-366.

This post was written by Alison Cash

July 28, 2015

Special Report: #NZASP15 Part II: Ups and downs of shark parasites, networks, and Toxoplasma gondii

This is Part 2 of my report on the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP) in Auckland, New Zealand (#NZASP 2015), which I attended earlier this month. If you had missed Part 1 of my report, you can read it here.

My previous post ended on a note about shark tapeworms, so I thought we should start this one off on the same note. In the previous post, it was established that the giant squid (at least in its juvenile form) is a part of some shark's diet, and is thus used by some tapeworms to reach their shark host. The talk by Trent Rasmussen from Otago University further expands on the role played by such prey items in determining the tapeworm community of sharks.

The parasite fauna of any given species is governed by a wide range of different factors. For tapeworms in sharks, a previous study showed that body size and depth range were good predictors for the diversity of tapeworms found in any given shark species. Trent's study expand upon that by including dietary range as an additional factor, and found that while body size and depth range were good predictors for tapeworm diversity, diet breadth - or the diversity of prey consumed by the said host shark - was an even better indicator.  With each type of prey harbouring different types of tapeworm larvae, having a varied diet is a great way to acquire an eclectic set of parasites. It seems that for sharks, your tapeworms are what you eat

Speaking of which, that leads into Robert Poulin's talk about the ups and downs of parasite life cycle. Many parasites have complex life cycles and have to go through many different animals in order to complete it. The problem with such a way of life is that there is massive attrition at each stage of the life cycle: for some parasites (like the tapeworms which infection sharks) they need their current host to be eaten by the next host to complete its life cycle (known as "trophically transmitted parasite"), and the likelihood that the parasitised prey will be eaten by the right predator species out of all the prey individuals in a population is very, very low. Given this cost, do such parasites have adaptations to offset the losses at each stage of their lives?

Digenean trematode cercariae
(free-swimming larvae)
That was the central question behind the study described in Robert's presentation, which he conducted with postdoctoral researcher Clément Lagrue and their team. From their study, it seems digenean trematodes (or flukes) seems to have evolved a key innovation that allows them to offset that some of that losses - and all it takes is the body of a snail at the first stage of their life cycle. The study itself was a massive undertaking which involved taking samples from four New Zealand lakes, at four different spots at each lake for a total of sixteen sites. At each of the site, they collected pretty much everything they could which added up over 650 thousand individuals animals, and they ended up dissecting over 400 thousand invertebrates and counted all the parasites that they found.

From this, they found that while was a reduction in the number of individuals for trophically transmitted parasites like tapeworms or roundworms, for digean flukes, there was actually an increase in the number of individuals in the population by two- to three-folds between their first host and the second host. Because flukes converts its first host, the snail, into a parasite clone factory, it is able to turn a single successful infection into thousands of infective larvae for the next step of their life cycle. The final stage of the life cycle of the fluke still involves being eaten by the right host, which means they are in the same boat as the tapeworms and roundworms, but at least they had been working with better odds than those other parasites.

Events like conferences are all about networking, but out in the wild amongst reptiles, "networking" is not so much about exchanging email and ideas as much as it is about exchanging parasites. Stephanie Godfrey from Murdoch University presented a talk about her research on how parasites can spread among social network in reptiles, and how models of such networks can be used to manage wildlife disease.

Photo by Caroline Wohlfei
One of the study she described involved testing the prediction strength of different epidemiological models, using the parasite-host system of ticks on Sleepy lizards (Tiliqua rugosas). These lizards live in the semi-arid desert of outback Australia where there are few shelters for the ticks. In such habitats, the parasites have an infectious window of 11-24 days to hop on a lizard or they will they expire, so the bushes where such where lizards congregate and take shelter inadvertently become places for tick exchange. When the lizard stop at those sites, they drop off tick larvae which lay in wait for another host to come along. Her study was a mark recapture experiment which involved releasing two "pulses" of tick larvae with known genotypes to see where they end up.

She test the ability of three different types of models to predict how the ticks would spread in the lizard population; one based on (1) social network, another based on (2) spatial proximity, and finally one based simply on (3) lizard behaviour. It turns out that network model had the highest predictive power, but the spatial model was not far behind, and it also depended on whether it was modelling the first or second larval pulse; a variability which was most likely due to seasonal variations that affected tick larvae survival

Finally, I end this post with a note about Toxoplasma gondii - the famed rodent-whisperer. If there is ever a parasite that has captured the public's imagination, it is this one. In the eyes of most people, Toxoplasma gondii might as well be called "Deus ex Parasita" or "Plot Parasite" as it has been suggested as being responsible for everything from schizophrenia, to brain tumours, to influencing human culture and even for making the French so, well, French.

Is that a rodent I see before me?
But what is the basis behind this reputation? Amanda Worth and other scientists from Murdoch University have been questioning whether such behavioural alteration necessarily benefits the parasite. In contrast to the usual narrative, T. gondii seems to do really well without ever ending up in a feline - the cat can act as a site for sexual reproduction, but it seems T. gondii can get by perfectly fine with just asexual reproduction (for a full coverage of this, see this from the zombie ants blog here).

Additionally, studies which investigated the question of T. gondii host manipulation often do not take into account pre-existing behavioural difference between individual rodents. In her study, Amanda compared the behaviour of both uninfected and T. gondii-infected mice, and to control for within-species variations, she observed the behaviour of the experimental rodents both before and after exposure to the parasite. Her results were...well, not as clear-cut as the other studies may have made it out to be.

For example, she noticed that some mice already had preference for cat urine before they were exposed to T. gondii. And while the T. gondii-infected mice spent more time hanging out in the open, they did not show a particular preference for cat pee (in contrast to the usual narrative about T. gondii). In the non-exposed mice, individuals that are more bold also tend to be more active, thus these two behaviour seems to be linked. But in T. gondii-infected mice, those two behaviour are not as well connected. While uncoupling certain behaviours in some cases may render an animal more susceptible to its predator, but whether that would make a rodent more likely to be eaten by a cat is another question.

So it seems that in this particular study, the effect that the infamous T. gondii inflicted upon their rodents hosts is relatively limited. Maybe there are variations between different T. gondii strains in regards to their capacity for altering host behaviour. Studies on other parasites have shown that within a given species, individual parasites or strains are known to vary in their propensity for host manipulation. Either way, it seems that there is Toxoplasma gondii the parasitic organism,  and then there is Toxoplasma gondii - the near-mythical entity which exists in our collective imagination; a parasite which is capable of masterfully manipulating people's behaviour so that they will believe just about any story that has "cat parasite" in its headline.

Next month, it will be guest posts time on this blog and I will be posting the best student blog posts from the Evolutionary Parasitology class of 2015 - so be sure to stay tuned for that! Until then, you can check out some of the student blog posts from last year here.

July 17, 2015

Special Report: #NZASP15 Part I: From seashells on the seashore to giant squid of the deep

Recently I attended the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP) in Auckland, New Zealand. It has been quite a while since the Kiwis and the Aussies had a joint parasitologist conference, and seeing as many of my former colleagues are located in New Zealand, it was a great opportunity to catch up with some of them. Note that the content covered in this blog post reflect my own interests (which in turn in is reflected in the kind of papers I cover for this blog) - there were many other presentations which I did not attend, so if you attended this conference, my post may not necessarily match that of your experience. However, here are some of the highlights from my perspective.

The conference began on a poignant note with the posthumous election of Ian Whittington, who sadly passed away in October 2014, as a fellow of the ASP. Ian Whittington was a very prolific scientist whose main research focus was on the biology and ecology of fish parasites, in particular a group of ectoparasitic flatworms call the monogeneans. The monogeneans are a ubiquitous and diverse group of parasites, and some of them are major pests for aquaculture. He was also a great mentor and his research group took a holistic approach to studying parasites which considered multiple aspects of their biology including their structure, behaviour and ecology throughout the entirety of their life cycles. He is greatly missed by many.

Photo of monogenean-covered kingfish by Kate Hutson
Fish parasitologist Andrew Shin gave a presentation dedicated to Ian Whittington on the cost of parasites to aquaculture. In his presentation, he talked about how parasites (such as monogeneans, but many others as well) cost the aquaculture industry millions of dollars in stock losses and treatment cost, and important role that parasitology plays in controlling such problems. He also described a system that he co-developed with Ian Whittington which automated the process of identifying and quantifying parasites on farmed fishes.

The process involves briefly dunking an afflicted fish in a freshwater bath, then this system - which consist basically of a flatbed scanner, microscope, and special software - is able to scan through the resulting soup of fish scales, mucus, and parasites to not only detect and count the number of monogenean parasites present, but also identify what stage of development they might be at, based on various characteristics of their body. The system can process 260 parasite specimens in 90 seconds, allowing aquaculture managers to quickly ascertain the level of infestation and act accordingly.

As a follow up to Andrew Shin's talk, Kate Hutson, a researcher and senior lecturer from James Cook University, provided an overview about a monogenean parasite call Neobenedenia, a genus that is developing into a major aquaculture pest. There are six recognised species of Neobenedenia - one particularly precocious species is found all over the world, infecting many different types of fish - this is the species which causes major problems for aquaculture. This is a very adaptable parasite which is able to change its form depending on the host they end up on, thus genetically identical individuals can end up looking quite different depending on their host species. Studies using fluorescent dye to keep track of the parasites found that while they initially settle randomly on the body of their host, as they grow, they move to specific body parts. In particular they congregate around the fish's fins where they will find potential mates (this invokes a mental image of parasite orgies happening on fish fins). And it doesn't take Neobenedenia long to get to that stage - they can reach sexual maturity and start pumping out eggs at 10 days old, and if no one else is around, as hermaphrodites, they can simply self-fertilise for at least 3 consecutive generation without suffering any ill effects.This makes them a formidable obstacle for any aquaculture system. But there are potential treatments under development on the horizon, ranging seaweed extracts that inhibit embryonic development, and cleaner shrimps which can eat up these pesky parasites and their eggs.

Photo of Austrolittorina antipodum by
Graham Bould
Some of you might recognise the name Katie O'Dwyer from a recent guest post. Well, for the last few years she has been working on her doctorate studying the diversity of parasites in periwinkles from New Zealand and Australia. While there has been a long history of research on parasites found in periwinkles in Europe, the perwinkles of the southern hemisphere have been mostly neglected despite, being one of the most common and abundant animals on the rocky shores. In her research, Katie examined two species of New Zealand perwinkles - Austrolittorina cincta and A. antipodum - the latter is also known as the banded periwinkle.

From these two snails alone, she discovered four new species of flukes, two of which are exclusively found in the banded periwinkle. She also examined the Australian periwinkle A. unifasciata (which confusingly is also called the banded periwinkle), in which she found four species of flukes, one of them happened to be Gorgocephalus sp., a species of parasite which is known from its adult form living in the gut of fish, but rest of life cycle and its other life stages were unknown prior to her discovery. These flukes do very nasty things to their snail hosts - causing them to lose their appetite and their gonads to shrivel away. They also compromise their ability to stay attached onto rocks and other surfaces, which is a big deal for snails living on the rocky shores. In mark-recapture studies, Katie found that infected snails were recaptured less often than their non-parasitised conspecifics, presumably because they were more likely to get swept off the rocks.

Fluke cysts in the foot of a clam
Sticking to seashells on the seashore, there was a talk by Master student Sorrel O'Connell-Milne (also from Otago University like Katie O'Dwyer) who is working on one of the parasite species that I studied during my PhD - a fluke call Curtuteria australis. This parasitic fluke has larvae that encyst in the foot of the clam Austrovenus stutchburyi, where it waits to be eaten by the final host which is the oystercatcher. When these parasites occur in sufficient numbers in the foot of these clams, they can affect the bivalves' ability to dig themselves into the sand, which makes them more vulnerable to predation. However, this also has other effects as the shells of the exposed clams act as habitats for other animals and can affect the biodiversity of the surrounding ecosystem.

Through a series of studies which included assessing the parasite load of clams from commercially harvested sites to those from unharvested area, as well as placing caged juvenile clams from different sites, Sorrel found that clams at site subjected to commercial harvesting had over one-third higher infection load than clams from unharvested sites. It possible that commercial harvesting decrease the density of clams, less individual around to soak up and "dilute" the pool of parasites in the environment. She also performed experimental infection of clams at various doses of C. australis and found that after 3 months of being exposed to C. australis, infected clams have reduced shell growth, body condition, and foot length. Considering the ecological role that these parasites can play through their bivalve hosts, these changes can have potentially cascading effects on the rest of the ecosystem.

Photo by NTNU
Museum of Natural history and Archeaology
One of the highlights of the conference for me was no doubt Haseeb Randhawa's talk about the parasites of the giant squid. He recently had an opportunity to dissect one of these giant mollusc for parasites, and it seems that while it is a predator in its own right, the giant squid also serves as a transmission vehicle for the larval stage of various parasites, particularly shark tapeworms. But the part that it plays in the transmission of these tapeworm larvae depends on the tapeworm species in question, and an individual squid can either be a transmission pathway or a dead end - depending on the size and age of the squid. Before they end up in the squid, the larvae of these marine tapeworms dwell in tiny crustaceans, which are consumed at various stage of the squid's life either directly or indirectly (through the squid's prey). The tapeworm then reach maturity in a shark's gut when it consumes an infected squid.

Throughout its life, the giant squid ends up acquiring a community of different tapeworm larvae, all of them go to different sharks, and ending up in the wrong host is a basically a death sentence for these tapeworm. So inevitable, success for one species can spell disaster for another. Haseeb found that there are at least four species of tapeworm which uses the giant squid as their ticket to the gut of their shark host - two of them infect skates, one infect porbeagle sharks, and one infect sleeper sharks. All these host species inhabit very different environments.

Giant squids start out life in more shallow waters, then moving to the open ocean as they grow into paralarvae. In such habitats, they are potential prey to skates (in the shallows) and porbeagle sharks (out in the open ocean), and presents tapeworms of such hosts an opportunity to complete their life cycle. But as the squid ages and moves into the deeper waters, the window of opportunity for those skate and porbeagle shark tapeworms closes. So as the giant squid matures, it literally sinks their chances of ever reaching their final host - while at the same time offers a glimmer of hope for another group of tapeworms - those that need to reach the deep dwelling sleeper sharks to complete their life cycle. The deep sea might be the final destination for the squid's life, but it is also the case for the tapeworms that parasitises sleeper sharks.

As a side note, I asked Haseeb if he also found any other parasites from the giant squid, in addition to tapeworm larvae. He replied that there were also some anisakid nematodes (which use marine mammals as a final host) and the larval stage of a fluke which infects sperm whales. But the role that giant squid plays in the life cycle of those parasites will have to be another story, another time...

Speaking of shark parasites, Part 2 of my Special Report on #NZASP15 will include more on shark parasites, the ups and down of parasite life cycles, networking in reptiles (and their parasites), and a re-examination of Toxoplasma gondii and its reputation for behavioural manipulation. Stay tuned!

June 26, 2015

Lysibia nana

Lysibia nana photo by Nina Fatouros
Used with permission
In order to live, a parasite must find its host. Whereas some parasites take a passive approach and simply wait for a chance encounter, many species are more proactive. In the case of parasitoid insects that have free-flying adults, they have various adaptations for tracking down their hosts. But what about the hyperparasites - parasites that infect other parasites? How do they find their host, which themselves are hidden within the body of a host animal? It seems as if they would need to have X-ray vision in order to complete their life cycle.

The parasite we are featuring today is Lysibia nana, a hyperparasitoid that infects Cotesia glomerata - the parasitoid wasp which lays its eggs inside caterpillars. It turns out that L. nana does not rely on superpowers like X-ray vision, but a far more parsimonious ability. To find out how L. nana finds a host, first of all, we have to ask; how does C. glomerata itself find its hosts? A few months ago, we featured a parasitoid fly that uses sound to track down its prey, but most parasitoid wasps use scent to sniff our their hosts. But this scent does not come directly from the host itself, but rather, the host's food.

When a plant comes under attack by herbivores like caterpillars, they emit volatile chemical signals call kairomones that acts like a dinner bell for parasitoid wasps, which have evolved to use those chemicals to guide them to their prey. Feeding by different species of caterpillars elicit different chemical emissions from the plant, which provides a signature of their presence and attract different species of parasitoids.

Parasitoid wasps are master body-snatchers, they don't just consume their hosts from within; while they are in residence they also change the caterpillar's physiology, altering its growth pattern and behaviour - so much so that on some levels the parasitised caterpillar can be considered as almost a different animal. But they have their own enemies in the form of hyperparasitoids like L. nana.

A research group in the Netherlands conducted a series of experiments to figure out how this hyperparasitoid tracks down its hidden prey. They first tested how wild cabbage plants responded when they come under attack by two different species of caterpillar - Pieris brassicae and P. rapae.
Dead caterpillar with Cotesia glomerata cocoons
Photo by Hectonichus
They found that two caterpillars induce very different blends of chemical volatiles from the plant. But it is a different story when those caterpillars are parasitised by C. glomerata. The physiological alteration that the parasitoid imposed on their host was reflected in how the caterpillar's food plant responded. Cotesia glomerata manipulated their hosts to such a degree that once parastisied, both P. brassicae and P. rapae elicited a far more similar blends of chemical emissions from the plant.

This is where the hyperparasitoid L. nana comes in. The researchers put some female hyperparasitoids in a Y-maze and exposed them to combinations of different volatile chemical released by; caterpillar-free plants, plants which had been chewed on by caterpillars, or plants which have been chewed on by parasitised caterpillars. They noticed that given the choice between the chemicals of plants damaged by parasitoid-free and parasitised caterpillars, the hyperparasitoids preferred overwhelming to go in the direction of the latter - regardless of what species the host caterpillar might be. To L. nana, whether those caterpillars had parasitoid babies onboard is far more important than their species identity, and they showed no clear preference for either caterpillar species as long as they were parasitised by C. glomerata.

The researchers also conducted a field-based study that corroborated the results from the behavioural experiment. They did so by attaching C. glomerata cocoons to some wild cabbage plants that they have grown in an experimental plot. Some of the plants had previously been munched on by parasitoid-free caterpillars, others by parasitised caterpillars. After 5 days, they checked the parasitoid wasp cocoons for signs of L. nana and found that cocoons on plants which have been chewed on by parasitised caterpillar attracted far more L. nana than those munched on by parasitoid-free-caterpillars

So while parasitoid wasps like C. glomerata may have masterful control over their host body's physiology, this also leaves a calling card to their own hyperparasitoids. For the hyperparasitoids, it's what's inside that counts.

Zhu, F., Broekgaarden, C., Weldegergis, B. T., Harvey, J. A., Vosman, B., Dicke, M., & Poelman, E. H. (2015). Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore‐induced plant volatiles. Molecular Ecology 24: 2886–2899.

P.S. I will be attending the New Zealand Society for Parasitology and Australian Society for Parasitology joint conference in Auckland, New Zealand. So watch for tweets with highlights from conference at my Twitter @The_Episiarch! All tweets related to that conference will have the #NZASP15 hashtag.

June 12, 2015

Coccipolipus hippodamiae

Today we feature a guest post by Katie O'Dwyer who recently completed her PhD at the Evolutionary and Ecological Parasitology group at Otago University. She has previously written for Parasite of the Day about  Phronima - a parasitic crustacean that turns gelatinous salps into floating zombies. This time she has written a story about why "Promiscuous ladybirds pay the price when it comes to parasites".

A pair of mating two-spot ladybirds (photo by Richard001)
For most of us when we hear any mention of sexually transmitted infections (STIs) we think of humans, herpes and the variety of public service announcements we see about practicing safe methods in order to avoid contracting STIs. However STIs are rife in the animal kingdom. They can be found in any animals that require internal fertilisation for reproduction. And it seems that one group which can really benefit from advice on safe methods to avoid STIs are the ladybirds.

Who would have known (well, probably some entomologists) that these beautiful beetles are highly promiscuous and not very choosy about who they mate with? This makes them an extremely efficient host for any sexually transmitted parasite. Today’s post is about a sexually transmitted mite Coccipolipus hippodamiae and its host - an European ladybird.

These mites are transmitted when ladybirds are mating and they migrate to the wing case (called elytra) of the beetles. Here they latch on using their mouthparts and feed on the hosts blood (known as haemolymph) before metamorphosing into adults. What quickly follows is the development of a large mite colony on a single ladybird. The presence of these mites can reduce the fertility and reproductive capacity of female ladybirds.

A female Coccipolipus hippodamiae mite with eggs.
Scale bar = 100 µm (photo from here)
There are some measures that can be taken when faced with high levels of STIs, such as switching the mating system to monogamy and being choosier when it comes to potential partners. However, studies have found no evidence for C. hippodamiae having any effects on mate choice in ladybirds. Luckily for the mites, female ladybirds are unable to detect if their male partners are infected.

However, there are other factors that limit the success of these parasites. Timing is an important aspect of STI transmission in this system. Ladybirds overwinter and refrain from mating regularly during this season. Following the period of overwintering, these highly promiscuous bugs travel across plants on a mating spree, hooking up indiscriminately, and triggering an epidemic of mite infections. A key aspect in this process is the overlap between generations.  In order for the mite population to be maintained mating must occur between consecutive generations of ladybirds. The mites have evolved to take advantage of those hosts with overlapping generations and unfortunately for the two-spot ladybird, Adalia bipunctata, it has one of the longest periods of overlap between generations. Therefore it is also the most common host for these mites.

These miniature mites have also adapted to infect other ladybird species with up to four species of European ladybirds in its repertoire of hosts. Interestingly, one of these ladybird species does not have an overlap in generations because a period of diapause is required during development, whereby one generation dies off before the next one metamorphoses into adults.  Luckily for the mite, these ladybirds appear free and easy when it comes to mating, even across different species. So even this ladybird species without overlapping generations can become reinfected during such hybrid mating sessions.

This picture gets even more complicated when the invasive Asian harlequin ladybird gets involved. This beetle has invaded the UK and is out-competing the native ladybirds (of which there are up to 46 species!). As a method of control some researchers have decided it might be a good idea to introduce the mites as a biological control agent. However, up to now, C. hippodamiae has not been found in ladybirds in the UK as they do not overlap in generations in the same way that continental European ladybirds do. This is currently an active area of research and not much is known about the effect the mites could have on the UK’s naïve ladybird hosts. In their struggle against the feisty harlequin ladybird, can a foe of European ladybirds become a friend of the UK’s native ladybirds? Only further research will tell…


Hurst, G.D.D., Sharpe, R.G., Broomfield, A.H., Walker, L.E., Majerus, T.M.O., Zakharov, I.A., Majerus, M.E.N. (1995) Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecological Entomology 20, 230-236

Webberley, K.M., Hurst, G.D.D., Husband, R.W., Schulenberg, J.H.G.V.D., Sloggett, J.J., Isham, V., Buszko, J., Majerus, M.E.N. (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. Journal of Animal Ecology 73, 1-10

Rhule, E.L., Majerus, M.E.N., Jiggins, F.M., Ware, R.L. (2010) Potential role of the sexually transmitted mite Coccipolipus hippodamiae in controlling populations of the invasive ladybird Harmonia axyridis. Biological Control 53, 243-247

Post written by Katie O'Dwyer

May 29, 2015

Mermis nigrescens

Photo by Haseeb Randhawa & Ken Miller here
New Zealand is a land known for its unique animals and plants, but over the centuries it has also become home to many introduced species which have become invasive and disruptive to its natural ecology. While many of the introduced species are recognisable larger animals such as pigs, possums, and rats, some of them tiny creepy-crawlies - insects and other invertebrates. And some of those have passengers living inside them which have largely been hidden out of sight

Meet Mermis nigrescens, a nematode worm which arrived in New Zealand inside European earwigs (Forficula auricularia). Mermis nigrescens is a species which had been known since 1842, and it is likely that it might have even been discovered earlier than that in 1766, but was mistakenly identified as Gordius - a genus of hairworm - which despite superficial resemblance and a similar life cycle, belongs to a different phylum. Its host, the European earwig, first arrived in New Zealand during the 19th century, but it was only recently noticed that these insects have also brought along a parasite from their original home range.

Photo of earwig host with M. nigrescens from this paper
Like other nematodes from the family Mermithidae, M. nigrescens are aquatic as adults and only parasitise earwigs during their juvenile stage. An earwig can be hosting anything from a single worm up to as many as seven of those parasite. When M. nigrescens reaches maturity, it needs to get into a water body to mate and reproduce. And if they're anything like the hairworms and other species of mermithids, it would commandeer the earwig and steer it to water, where the worm can evacuate its host xenomorph-style and leaves the now hollowed-out earwig to drown.

So how do we know this parasite is an introduced species and isn't one that the earwig had simply acquired in its new home?

Molecular analysis looking at three genetic markers from M. nigrescens showed that the closest relatives of these particular nematodes are found in Canada - M. nigrescens appears to be well-travelled, and is found all over the world. But it does not seem to be as abundant in Dunedin, New Zealand as seen elsewhere in world. In the population that was examined for this study, only 19 out of the 198 earwigs examined were infected with M. nigrescens, whereas a study in Tasmania, Australia found the parasite in half of the earwigs examined, and it was even more common in Ontario, Canada where infection prevalence reached 63%. It is currently unknown why M. nigrescens does not seem to be as abundant in New Zealand as it is elsewhere in the world, though it could just be something about this particular bunch of earwigs and that there are more heavily parasitised earwig populations elsewhere in New Zealand.

But where did the M. nigrescens population in New Zealand originate? While its closest living relatives are found in Canada, did it arrive to New Zealand from there? After all, the original home of M. nigrescens is Europe, so the Canadian population was not native to that region either. The missing piece of this puzzle is genetic sequences of M. nigrescens specimen from its original range in Europe, which might resolve where this newly discovered New Zealand population originated - from Europe or elsewhere. For all we known, this supposedly widespread species may in fact be composed of a complex of closely-related cryptic species, with each species found in a different region of the world.

Just goes to show that even in the common earwig, there are natural history secrets waiting to be revealed.

Presswell, B., S. Evans, R. Poulin, and F. Jorge. 2015. Morphological and molecular characterization of Mermis nigrescens Dujardin, 1842 (Nematoda: Mermithidae) parasitizing the introduced European earwig (Dermaptera: Forficulidae) in New Zealand. Journal of Helminthology 89: 267-27

May 15, 2015

Taenia serialis

Many parasite can cause health problems for their hosts, but aside from those that infect humans and domestic animals, it is not entirely clear just how much impact most parasites are having on the host population. Of course, the problems caused by parasites for a host goes beyond direct pathology; for social animals, parasitism can also affect how individuals interact within a group.

(A) Frodo the gelada and (B) the T. serialis larvae that spilled from her back
Photo from Fig 1 of the paper
In this post, we will be discussing a study which investigated the impact of a tapeworm on a population of gelada baboons (Theropithecus gelada) in Ethiopia. The tapeworm in question is Taenia serialis, which is related to some more well-known species of tapeworms include the beef tapeworm and the pork tapeworm. Despite being commonly used in first year biology textbook as a "typical" example of a tapeworm, Taenia is anything but typical in terms of its life cycle compared with most other tapeworms.

Like other parasites that have a complex life cycle, the larval stage dwells in an animal known as the intermediate host - this is where the parasite grows to a certain size before being eaten by a predatory animal which serves as the final host (definitive host), where it will mature into a sexually reproducing adult worm. Taenia does something different in its intermediate host - an adaptation found in the evolutionary play book of the digenean flukes and some other parasites. Instead of merely growing larger and await consumption by the final host, they asexually multiply inside the intermediate host - making many genetically identical copies of themselves and forming cysts which contain hundreds or even thousands of larval clones.

As you can imagine, having a slowly growing bag of worms lodge inside your body is not good for your health (it actually served as a plot device in an episode of House), but just how much does it impact a population of wild animals? The paper featured today is the result of a long term study stretching from January 2007 to June 2013 monitoring the health and demographic data of 16 gelada bands on the Guassa Plateau located on the western edge of the Great Rift Valley on the Ethiopian Highlands. The research group kept track of 348 individual geladas over the course of the six and a half year study, noting their health, reproductive status, and any birth or death. These monkeys are also commonly infected by a species of Taenia which uses the geladas as an intermediate host.

The final host for this parasite is most likely the Ethiopian Wolf (Canis simensis) - which shares the same habitat with the geladas. Even though this carnivore usually only hunt small mammals such as rodents, they are known to scavenge on gelada corpses - which is probably how they become infected with T. serialis. When geladas accidentally ingest tapeworm eggs which had come from the wolf's faece, the parasite proliferate in the monkey, forming cysts or bladdders which can become visible as protrusions on the skin. While the cysts are grotesque, this allows researchers to monitor infections in the monkeys without coming into direct contact them (which might affect their natural behaviour). But while the cysts are clearly recognisable on the gelada's skin, one cannot simply identify a parasite via skin cysts alone - a closer examination is necessary.

Fortuitously (for science anyway), during the course of their study they were able to obtain some parasite material for identification due to a serendipitous event. Some members of the research group noticed an adult female gelada they named Frodo had a large parasite cyst on her back. At some point, the cyst ruptured and spilled out a bunch of parasite larvae, enabling the researchers who were following Frodo at the time to collect some of the parasites for examination, and subsequently identify them as T. serialis. While this tapeworm is usually known to infect rabbits as an intermediate host, on the Ethiopian Highlands, they infect geladas.

Overall, the researchers found that one in six of the monkeys they monitored had at least one T. serialis cysts, and most of those afflicted were adults with one-third of the adult population showing signs of infection by the tapeworm at some point. Those infected monkeys are more than twice as likely to die than their uninfected comrades, and this tapeworm's impact extends beyond the individual directly infected with it. Infants born to tapeworm-infected mothers are twice as likely to die before their first birthday compared with infants that have mothers with no signs of infection, and infected female monkeys also experience a longer lag period between the birth of each offspring.

Male monkeys also lose out due to T. serialis infection - geladas are polygamous species that organise themselves into so-called one-male units (OMU), each consisting of a single male with a harem of females. The researchers observed that tapeworms infection compromises the male monkeys' ability to hang on to their harems and infected geladas are more likely to lose in a dispute with any new (uninfected) challenger(s) that appear on the scene.

The impact of parasites on most wildlife is not well-understood, and often their effects are not immediately visible without a sustained long-term ecological and demographic study. Even natural levels of infection can have profound impact on host population, as seen with the effects of T. serialis on geladas. Therefore when it comes to wildlife conservation, it important to be mindful of parasites and the hidden role they play on the stage of nature.

Nguyen, N. et al. (2015). Fitness impacts of tapeworm parasitism on wild gelada monkeys at Guassa, Ethiopia. American Journal of Primatology 77: 579-594.

April 26, 2015

Nepinnotheres novaezelandiae

Life as a pea crab seems pretty sweet, you spend most of your time sitting snug and protected within the armoured shelter of a shellfish, while your host's filtration current bring you a constant stream of oxygen and food - everything that a pea crab needs for a good life. Well, almost everything - because there's more to life than just being protected and fed. Much like other organisms pea crabs need to reproduce - that's how evolution works, and unlike many other living things, a pea crab cannot just clone itself.
Male Nepinnotheres novaezelandiae squeezing in between
the valves of a mussel. From video here.
So when it comes to reproduction, the balance of living the pea crab life tips from "pretty sweet" to "absolutely terrible" - especially if you are a male pea crab. For them, trying to find a mate is a harrowing challenge than none of us can possibly imagine. First of all, to reach a potential mate, you have to leave your host, which means you have to pass the gates that are the valves of the host mussel, without being caught in between them. At that stage, those valves that had offer such formidable protection for the pea crabs then become death traps, with about 13% of male crabs meeting their end at this molluscan gate - their bodies litter the mussel bed.

Once outside, the male pea crab faces even more challenges. These tiny crustaceans, which are more accustom to a cosy life inside a shellfish, have to cross the treacherous, open areas of the mussel bed, filled with horrible monsters (in the form of predators like fish, octopus, and larger crustaceans) for which an exposed pea crab is just a convenient snack. Furthermore, male crabs only make up 20% of the population despite the more or less equal sex ratio of immature pea crabs. The length that they have to go to just to find a mate probably has something to do with that...

Despite the odds, almost 90% of all female crabs in the population carry fertilised eggs, so some male crabs must be having successes - but how?

The researchers who conducted this study noticed that the male pea crabs always set out under the cover of darkness when they will be less likely to be spotted by predators, and also because mussels are more relaxed at night. From the researchers' perspective, this also means that all the experiments and observation of pea crab behaviour had to be done in the dark. So in addition to sea water tanks, they set up some infra-red cameras to capture footages of all this activity - like some kind of voyeuristic shellfish reality TV show.

So what would coax a male crab out of his cosy home? To find out, the researchers constructed a flow-through observation chamber lined with PVC tubes in which they placed pea crab-infected mussels. When they placed a mussel with a female crab upstream of one with a male pea crab, the male crab would exit their host 60% of the time, roused into action by something which seem to secreted by the mussel (or the female crab in the mussel) upstream.

Male Nepinnotheres novaezelandiae tickling the mantle edge
of a mussel. From videos here.
The crab then makes its way to the mussel where the female crab resides. Once there, the pea crab patiently tickles the mussel's mantle fringe with its legs to try and convince the bivalve to let it enter. This is also the reason why the male crab only do this at night, because a mussel's response to such tickling can be very different in daylight. Try the same trick during the day and the bivalves would slam shut, crushing the amorous crab between its valves. On average, the crab will spend over three hours fiddling away at the mussel to coax the shellfish into opening up.

Additionally, in a different flow-through seawater tank where the crabs were given more freedom to roam from one host to another, the researchers recorded how long it took for the male pea crab to leave its host and reach a mussel containing a female crab. The entire journey from exiting the original host mussel to reaching their final destination took seven hours on average, though this varies from a quick hour-and-a-half jolt, to an eighteen-and-a-half hour-long trek for one particularly unfortunate individual.

So when love (or at least lust) is in the water, the pea crab will give up the easy life, and risk life and limbs for an evening rendezvous.

Trottier, O., & Jeffs, A. G. (2015). Mate locating and access behaviour of the parasitic pea crab, Nepinnotheres novaezelandiae, an important parasite of the mussel Perna canaliculus. Parasite, 22: 13.

April 10, 2015

Edhazardia aedis

When two different parasites find themselves in a small host animal like a mosquito, there is only so much of the host to go around. So there is a pretty good chance that those co-occurring parasites are going to fight it out, and there's no guarantee that there will be a winner out of this conflict.
Photo of E. aedis spores from here

Edhazardia aedis is a microsporidian parasite that specialises on infecting Aedes aegypti - also known as the mosquito that can act as the main vector for a variety of viruses include those that causes degnue fever, yellow fever, and Chikungunya. Edhazardia aedis can spread through the mosquito population via two methods; (1) the parasite can proliferation throughout the mosquito's body until it ultimately overwhelms the host, which dies and dissolves into a cloud of infective spores, or (2) if an infected female mosquito survives the ordeal to adulthood and still manage to produce offspring, her mosquito babies will inherit E. aedis from her (gee, thanks a lot mum!).

But E. aedis can sometimes run into a competing species - Vavraia culicis. It is also a microsporidian, but unlike E. aedis, it is a generalist that can infect many different species of mosquitoes. It is also a mosquito-killer which has the same general modus operandi as E. aedis, where the parasite's spores are released when the host finally succumbs. This study found that mosquito larvae which have less access to food and are infected by both parasites tend to die earlier - and when the host dies, the spores are dispersed for both E. aedis and V. culicis - so everyone wins, right? Well not quite.

While host death does release the spores which allow them to infect more mosquito larvae, the parasites get more spores for their bucks by keeping their host alive for longer - so a host that ends up keeling over too early is not very cost effective. This applies to both E. aedis and V. culicis. Even before host death, the cost of co-infection starts manifesting itself. Regardless of whether the host dies sooner or later, both parasites produce less spores in co-infections. If E. aedis is sharing a host, it produces half as many spores as it would have if it had the host all to itself. But co-infection is even more costly for V. culicis, which manages to produce only a bit over a quarter of the spore it would have in single infections.

It is unknown how these two parasites duke it out in the mosquito, or why E. aedis has a competitive edge over V. culicis. Perhaps by being a specialist of A. aegypti, E. aedis has some sort of home ground advantage when it comes to getting the most out of its host. So it seems that some parasites just don't like sharing, and when it comes to living with others, sometimes it pays for a parasite to be a specialist.

Duncan, A. B., Agnew, P., Noel, V., & Michalakis, Y. (2015). The consequences of co-infections for parasite transmission in the mosquito Aedes aegypti. Journal of Animal Ecology 84: 498-508.

March 26, 2015

Emblemasoma erro

During summer the air is filled with the rattling ruckus of cicada songs. Male cicadas produce this summer choir using a pair of noise-making organs located in their abdomen, with the aim of getting attention from any prospective mates. But in some cases, they can also end up with some unwanted attention.

Top: Male Tibicen dorsatus cicada
Bottom: Female Embelmasoma erro fly
Photos from Figure 1 & 2 of this paper
The species we are featuring today is an "acoustically hunting" parasitoid fly - it eavesdrops on the male cicada's flirtatious serenading and uses it to home in on its target. This fly is commonly found on the Great Plains of North America and is a scourge to male cicadas, especially male Tibicen dorsatus.

Most of what is known about such acoustically hunting parasitoids are based on flies from the Tachinidae family - one of which targets crickets (I talked about how crickets on Hawaii evolved to become silent due to the presence of one such parasitoid fly here). But this fly belongs to a different family (Sarcophagidae). Only one species of Emblemasoma is well-studied - E. auditrix- and even though Emblemasoma is widely use in the study of insect hearing, not much is known about how they actually live out in the wild. Until now, the only information available on E. erro are based on two scientific papers - one published in 1981 and the other published in 2009. The paper we are featuring today provides some much-needed update on key aspects of this parasitoid's ecology and life history.

This paper reports on a series of field surveys and laboratory experiments that documented the parasitoid's occurrence, abundance, behaviour, and developmental cycle.

The field surveys were conducted at study sites located across Kansas and Colorado. The surveys found that a bit over a quarter of male cicadas were infected with E. erro larvae, and because of how the flies track down their host, almost all the infected cicadas were male - except for one very unlucky female cicada, which most probably got infected because she was responding to the call of a male, ran into a larvae-ladened E. erro that had the same idea, the latter decided that any cicada will do. Talk about a case of fatal attraction!

And it is indeed the sound of the male cicada's serenade that draws in those flies - a loudspeaker playing the recordings of cicada calls is sufficient to attract the attention of E. erro, but a female fly need more than that to commit to dropping off her precious offspring. In outdoor cage experiments where flies and cicadas were housed together and allowed to mingle freely, the researcher observed that even if an E. erro finds herself perched next to a cicada, she will only attack when the host makes any sudden movements. So E. erro uses two separate signals to track down its prey; an acoustic signal at long range in the form of the cicada's call to guide them in, and a visual signal at close range in the form of cicada movement to confirm the host's identity

Emblemasoma erro larva emerging from a cicada
From Figure 6 of this paper
Once she has confirmed her target, the female fly makes an attack run, and very quickly drops off between 1-6 maggots (usually 3) on the base of the cicada's wings. As soon as the maggots land, they immediately start burrowing between the segments and into the cicada's body. The maggots then start devouring its host alive from the inside. Depending on the temperature and clutch size, they take about 88 hours to reach a large enough size to start pupating. At the end of this period, the maggots use teeth-like "oral hooks" to chew their way to freedom, fall onto the soil below to become pupae, and leaving the cicada an empty husk.

So while the aim of the male cicada's singing is to attract the attention of female cicadas, some of them may instead end up getting attention from females of a very different species, and become reluctant incubators for the broods of some keen-eared, cicada-hunting flies.

Stucky, B. J. (2015). Infection behavior, life history, and host parasitism rates of Emblemasoma erro (Diptera: Sarcophagidae), an acoustically hunting parasitoid of the cicada Tibicen dorsatus (Hemiptera: Cicadidae). Zoological Studies, 54: 30.