"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

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!