Maritrema novaezealandensis (revisited)

This is the fourth and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by Sally Thorsteinsson on a study that investigated how an intertidal parasite with a complex life cycle might respond to global warming (you can read a previous post about toxic birds and their lice here, a post about bees protecting themselves against fungal parasites by lining their hives with resin here, and how an avian malaria parasite might make its bird host more attractive to mosquitoes here).

Paracalliope novizealandiae

Intertidal habitats are tough places to live: one minute you may be submersed, buffeted, and chilled by salt water, the next baking under a hot, drying sun. However, global warming is predicted to turn up the heat even more on those that inhabit these environments. The tidal flats on the South Island of New Zealand are the habitats of the parasite trematode Maritrema novaezealandensis and the three hosts necessary for it to complete its life cycle – mudsnail Zeacumantus subcarinatus, amphipod Paracalliope novizealandiae (a type of sandhopper-like crustacean) and gulls which are its final host (this life cycle is described in a previous Parasite of the Day blog post here).

Cercaria of
M. novaezealandensis

Trematodes are strongly influenced by the heat, and some studies have predicted that they will flourish with global warming and increase their impact on intertidal systems. However, parasites cannot be looked at in isolation, but considered as part of the ecosystem, which may also be temperature sensitive. For M. novaezealandensis itself, there may be a perk to global warming, as long as temperatures stay within its optimal range.

When the water in rock pools is comfortable for us to roll up our jeans and paddle (between 20 and 25 °C), M. novaezealandensis thrives. At present this happens during low tide on hot summer days and the warmth sparks the release of multitudes of cercariae (free-swimming trematode larvae) into the water from the bodies of their snail hosts, ready to drill their way into their next host, the amphipod. In such temperature, the cercariae survive for relatively long periods, are at their infective peak and develop well inside the amphipods. These conditions are expected to occur more often and for longer periods with global warming - not particularly good news for the host snails and amphipods of M. novaezealandensis  bombarded by increased numbers of this parasite and suffering death and destruction (particularly the amphipods) as a result.

But the heat gets all too much for M. novaezealandensis at temperatures greater than 30 °C when there are still many cercariae but they infect amphipods at lower rates and their lifespans are shortened. The amphipods also die at such heat, making it harder for the parasites to find their hosts and live in them long enough to develop. At present these extremes are rare, but the increase in high-temperature days as predicted would disrupt the parasite’s life cycle further and decrease the population of amphipods. As amphipods are an important food source for other animals, as well as the decomposers of the intertidal world, their demise can have widespread consequences.

Who knows what changes global warming will be bringing to the wider ecosystem; lab experiments, such as the one providing these results in this study, can only offer an indication. Further research into the effects of climate change on host-parasite systems will be important given the pivotal role of parasites and the complexity of the ecosystems that they are part of. Perhaps the behaviour of the snail, amphipod and gull hosts will also be affected by temperature changes, sea level rise or alterations in habitats and such selection pressure over generations of hosts and parasites will turn up the heat on evolution, resulting in offspring that may be quite differently to those that are alive today.

Reference
Studer, A., Thieltges, D. W., & Poulin, R. (2010). Parasites and global warming: Net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415: 11-22.

This post was written by Sally Thorsteinsson

Plasmodium relictum (revisited)

This is the third post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by David Rex Mitchell on a paper published just this year on how an avian malaria parasite might make its bird host more attractive to mosquitoes which are the parasite's vector (you can read a previous post about toxic birds and their lice here and a post about bees protecting themselves against fungal parasites by lining their hives with resin here).

Photo of Culex pipiens
by Joaquim Alves Gaspar

One of the aspects of parasites that people tend to find a little more disturbing is the idea that they can control the minds of other animals. Although this may seem like the stuff of science fiction, this is indeed sometimes the case. For those parasites that live inside other animals, there are often several stages to their lives and each of these stages may require the use of a different type of animal. This presents a challenge in getting from one animal to the next and so if a parasite can influence the behaviour of one animal in some way, making it easier to reach the next, this is incredibly advantageous.

Many parasites have evolved abilities to do just this. For example, some blood-sucking insects infected with certain parasites are known to bite more frequently than when uninfected, helping to spread the disease to more animals. This is seen in malaria-infected mosquitoes, tsetse flies infected with sleeping sickness, and plague-infected fleas. But is it possible that a parasite can also influence a healthy, uninfected animal’s behaviour? The paper featured today attempts to address this question. Researchers used a species of avian malaria (Plasmodium relictum - a parasite that has been previously covered on the blog by this post here) and its natural mosquito carrier (Culex pipiens) to find out if malaria-infected animals are more attractive to mosquitoes than healthy, uninfected animals. This species of malaria is spread among birds via its mosquito carriers and thus the researchers chose canaries to carry out the experiment.

Photo of canaries by 3268zauber

Pairs of canaries, one infected with the parasite and one uninfected, were exposed to uninfected mosquitoes to see which bird they would prefer to feed on. The mosquitoes mostly fed on only one animal per sitting, so the blood inside their bellies could be removed and the DNA analysed to determine which bird it fed upon. The experiment was carried out on the day the birds were injected with the parasite, as well as 10 days and 24 days after injection, so as to monitor any changes as the parasites matured inside them.

From this experiment the researchers discovered that, not only did the mosquitoes clearly prefer to feast on the malaria-infected canaries, but also this behaviour became more prominent as the malaria parasites mature within the canary and become capable of crossing into a mosquito. The researchers suggest that the malaria parasite influences the mosquito’s decision to feed on the infected animal, assisting its transfer to said mosquito – the next stage in its life-cycle. The mechanism used to achieve this has not yet been determined but the researchers suggest that the parasite may alter the odours that are emitted from the host animal, enticing the mosquitoes to choose its infected animal over other uninfected animals. If these odours can be identified and reproduced, they may prove very useful in control of malaria in the future, for example in mosquito traps.

So is this an example of crazy sci-fi mind-controlling by parasites? Ok, so mosquitoes may not exactly be renowned for their calculated decision making skills. But the results of this experiment were still able to show us how the malaria parasite can influence a healthy mosquito’s decisions, offering further insight into the awesome manipulative powers of parasites.

Reference
Cornet S, Nicot A, Rivero A, & Gandon S (2013) Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecology Letters 16: 323 – 329.

This post was written by David Rex Mitchell

Ascosphaera apis

This is the second post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by Karen McDonald on a paper published in 2008 on how bees use resin to protect their hive against fungal parasites (you can read the previous post about toxic birds and their lice here).

Animals have evolved many different strategies to fight parasite infections; from eating tough or poisonous leaves (which would normally never be chosen as part of their diet), dirt bathing, grooming themselves with plants that contain chemicals that kill parasites, living in hostile environments that parasites can't tolerate, to drinking toxic substances like alcohol to kill internal parasites. Animals in general are individuals and care only for their own personal well-being and so the parasite-ridding strategies animals use really only affect their own health and well-being. But bees, on the other hand, are different.

SEM photo of Ascosphaera apis sporeball from here

Bees are communal animals and each bee is an important part of the hive community. The article I am going to talk about today shows that bees don't act on a self-motivated level where they are only concerned with their own well-being, instead bees work only to improve and support the whole hive community. Wild bees always smother the inside of their nests with sticky plant resin and the reason for this was never really understood. Domesticated bees don't use much, if any resin at all. They have been selectively bred to not use it because the sticky resin makes opening the hive and removing the honey and combs very difficult. But domestic bees are also plagued by many, often destructive, parasites.

In 2008 researchers decided to document whether the amount of plant resin that domestic bees use in their hives has an effect on fungal parasite levels in that hive. Two groups of hives were set up; the first group of 12 had the inside of each box painted with thick resin to replicate the nests of wild bees, the second group of 11 boxes were only painted with the type and quantity of resin used by commercial apiaries. Bees from both groups were fed with pollen infected with Chalkbrood, which they ate and/or carried back to their hives.

Photo of chalkbrood-infect larvae from here

Chalkbrood (Ascosphaera apis) is a fungal infection of bee larvae, causing them to die and mummify in the nest (see photo on the right). Adult bees are not affected by the parasite but they do carry it in their bodies and drop spores throughout the nest infecting young bees. Normally, as mentioned above, infected animals are usually only concerned with their own well-being and so the researchers were interested in seeing whether the adults would react to the threat to the larvae or ignore the parasite menace because it did not affect them personally.

Within days, the bees immediately began collecting more resin for their nests. Normally, there are only a few bees in each hive that forage for resin, the majority forage for pollen or nectar. Bees do not eat resin; its only function is to line the nest, so not much energy is used by the hive community to collect it. But when the hive is under threat from a parasite like Chalkbrood, more bees begin to forage for resin and a lot of energy is used to find it.  The nests painted with resin, although infected at the same level, also had a reduced level of infection compared to the commercial standard nests, but the level of infection in all nests dropped as the amount of resin in the nest increased. The bees were using the resin as a form of  social immunity rather than self-immunity.

References:
Simone-Finstrom M.D., Spivak M., (2012) Increased Resin Collection after Parasite Challenge: A Case of Self-Medication in Honey Bees? PloS One, 7(3): e34601. Doi: 10.1371/journal.pone.0034601

This post was written by Karen McDonald

Toxic Birds Make For Sad Lice

It has been a while since we had a guest post at the Parasite of the Day blog (in fact the last guest-contributed post date back to May 2011), but in the next few weeks I will be bringing you a series of posts from guest contributors. Earlier this year, I ran my third year Evolutionary Parasitology unit (ZOOL329/529) for the first time. One of the assessments I set for the students who took that unit was for them to summarise a paper that they have read, and write it in the manner of a blog post, much like the ones you see on this and other blogs. 

I also told them that the best blog posts from the class will be 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 2013. To kick things off, here's a post by Bianca Boss-Bishop on a paper published in 1999 on toxic birds and their lice.

Photo by John Dumbacher from
the California Academy of Sciences

Birds are host to an impressive diversity of external parasites, from insects (including lice, fleas, bugs and flies) to mites, ticks and even fungi and bacteria. These parasitic organisms can have severe negative effects on host fitness. Therefore, it is not surprising that birds invest a lot of time engaged in behaviours such as grooming, preening, dusting and sunning in attempts to rid themselves of their ectoparasites. A handful of unique birds from the genus Pitohui have an interesting physiological adaptation that may assist in the fight against parasite infestation: feather toxins.

Yes, toxic birds. The six species of Pitohui, which are endemic to New Guinea have been found to carry toxin in their skin and plumage. These are the same potent toxins as those found in the skin of poison dart frogs (Phyllobates spp.) and are some of the most toxic natural substances known. The toxin present in the Pitohui is known as homobatrachotoxin and like all batrachotoxins is a neurotoxic steroidal alkaloid capable of depolarising nerve and muscle cell membranes. The level of toxins present in Pitohui tissue varies between species and geographic location. The most toxic species is the hooded pitohui (Pitohui dichrous), from which merely handling an individual can cause numbness, sneezing, and irritation of the eyes and sensitive mucous membranes. It has been hypothesised that the high proportions of toxin present in the Pitohui skin and feathers could provide the bird with a barrier from ectoparasites that live and feed on skin, feathers and subdermal blood supplies.
batrachotoxins

SEM photograph from phthiraptera.info

John Dumbacher, current curator and department chair of Ornithology and Mammology at the California Academy of Sciences was the first to test if the presence of toxins in Pitohui feathers and skin would deter or kill chewing lice (order Phthiraptera). In order to investigate this he conducted a series of choice and lifespan experiments. Dumbacher found that when individual lice in the laboratory were given a choice of two feathers (one toxic Pitohui feather and one non-toxic non-Pitohui feather) there was a statistically significant preference against feeding or resting on the toxic feathers. Lice exposed to the highly toxic feathers of P. dichrous rarely showed signs of eating, with many becoming immobile and inactive. In some cases the louse would simply drop off the toxic feather. In a natural setting, immobility and lower feeding rates reduces the damaging effect of the lice and may even allow the birds to more easily remove or dislodge the parasites mechanically by preening or flying. Since this part of the study showed that the lice exhibited an active choice against the naturally toxic Pitohui feathers we can conclude that homobatrachotoxin has the potential to act as a repellent against these parasites.

Dumbacher also determined that the natural levels of homobatrachotoxin in Pitohui feathers greatly increased louse mortality. The results of the lifespan experiments showed that the mean lifespan of lice exposed to feathers of either high or low level toxicity was half that of those on nontoxic feathers. Interestingly, the mean lifespan of the lice on the toxic feathers was similar even though the toxin levels in P. ferrugineus are ten times lower than P. dichrous. Therefore, Pitohui feathers with lower toxin levels may not have been potent enough to repel lice during the choice experiments but were as effective in increasing louse mortality as the highly toxic feathers. Increased mortality in lice could have many benefits for the host. Less time spent on the host will reduce the negative effect of each individual louse.

One observation from the study was that non-toxic feathers showed obvious damage from lice feeding. This may be due to the extended life span offering additional feeding time, or the lice simply find nontoxic feathers more palatable. Further investigations may provide insight into additional  benefits, for example whether or not the potent toxin is able to reduce louse fecundity. If mating in lice is decreased then subsequent generations of lice are also reduced. Smaller populations would cause less irritation to the host and also be less visible to potential mates. Additionally, less ectoparasites would reduce time spent mechanically removing them and more time to invest in other activities. The results of Dumbacher's study suggest that the naturally occurring homobatrachotoxin found in the skin and feathers of the Pitohui repels and kills lice. The presence of a powerful toxin in skin and feathers has the potential to create a formidable barrier and protect the bird against infestation from ectoparasites.

Reference:
Dumbacher, J. P. (1999). Evolution of toxicity in Pitohuis: I. effects of homobatrachotoxin on chewing lice (order: Phthiraptera). The Auk, 116: 957-963.

This post was written by Bianca Boss-Bishop

Tetrabothrius bassani

It has been known for some time that intestinal parasites such as tapeworms can accumulate high concentrations of heavy metals, acting as a sink for such substances in the host's body. Back in 2010 a study on shark tapeworms accumulating heavy metals was featured on this blog, but most of such studies comparing the concentration of heavy metals in the host's organs with that of their parasites have been conducted on fish and fewer studies have looked at the heavy metal concentrations of intestinal parasites in birds and in particular seabirds, which form an important part of the marine ecosystem.

Photo of Tetrabothrius scolex (attachment organ)
from this paper

In the study we are featuring today, researchers tested the concentration of various heavy metals in the organs of twenty-three Northern Gannets from the central coast of Portugal. The birds had died when they were tangled up in fishing gear from commercial fishing boats, but they were otherwise in good health before they ended up on the wrong end of some fishing nets. They all had stomachs full of fish and the only parasite found in their intestines was the tapeworm we are featuring today - Tetrabothrius bassani. There are a number of different species in the Tetrabothrius genus, some species like T. bassani parasitise seabirds such as gannets and albatrosses, while other are found in whales - for example, I wrote a post a few years ago about some tapeworms I found in the gut of a beaked whale, which you can read about here.

For this study, the researchers collected at least one T. bassani from each gannet and took tissue samples from the bird's liver, kidney and pectoral muscle to measure the concentration of different heavy metals. They found that, on average, T. bassani accumulated twelve times as much cadmium as the gannet's pectoral muscles. Furthermore the tapeworms had seven to ten times more lead than the seabird's kidneys and liver. Since these worms seem to act like sponges that soak up and concentrate heavy metals, such substances would reach detectable level in the tapeworms well before they became noticeable in the host's own tissues. Because of that, these parasites can possibly serve as early warning indicators for the presence of pollutants in the environment.

Reference:
Mendes, P., Eira, C., Vingada, J., Miquel, J., & Torres, J. (2013). The system Tetrabothrius bassani (Tetrabothriidae)/Morus bassanus (Sulidae) as a bioindicator of marine heavy metal pollution. Acta Parasitologica, 58: 21-25.

Flamingolepis liguloides

The parasite that features prominently in the study we are looking at today is a tapeworm that lives in flamingoes - something that you might have already guessed by the parasite's genus name. The larval stage of the tapeworm Flamingolepis liguloides lives inside brine shrimps, which happen to be a major part of the flamingo's diet. Previous research has found that this parasite is capable of altering the behaviour of the shrimp as well as their colour and fat content.

Photo of F. liguloides larvae from the paper

In this new study, a team of scientists looked at the frequency of larval F. liguloides (and other tapeworms) in two brine shrimp species found in Mediterranean wetlands - Artemia parthenogenetica and Artemia salina - and how they related to the abundance of birds, the final hosts for those tapeworms. As the name indicates, A. parthenogenetica reproduces asexually (without mating), while A. salina is a more conventional sexually reproducing species.

Flamingolepis liguloides is not the only species of tapeworm infecting those shrimps, in fact each Artemia species harbours nine different tapeworm species each for a total of ten different tapeworms (both species of shrimps share a number of tapeworms in common). But F. liguloides is by far the most dominant, probably because flamingoes also happen to be the most numerous and long-lived birds in the area - the researchers estimated that flamingoes represented almost ninety percent of the bird biomass at those wetlands. Despite its dominance, F. liguloides does not seem to push aside the other tapeworms; the brine shrimps often harbour multiple species of tapeworms and the different parasites don't seem to get in each other's way. The fact that they have so many different species of parasites is also an indicator of the wide variety of birds that frequently visited the area. The Odiel marshes, where the scientists collected the asexual brine shrimps, is home for up to twenty thousand shorebirds during migration periods.

Photo of brine shrimps by Hans Hillewaert via Wikipedia

There were some seasonal patterns in infection prevalence. For the asexual brine shrimp, it ranged from a low of four percent to almost half the population being infected, whereas the parasite prevalence in sexual brine shrimps was consistently high, with tapeworms being found in over a quarter to almost three quarters of the shrimp throughout the year. The researchers found that such seasonal changes in the prevalence of some (but not all) of the tapeworms were associated with changes in abundance of the bird hosts. However, the scientists suggested that the consistently high tapeworm abundance in A. salinawas due to the areas they studied being protected areas that harbour thousands of birds, especially flamingoes, which flock there in huge numbers as their wetland habitats are destroyed elsewhere.

The high abundance of tapeworm infections simply reflects a high abundance in the bird hosts that harbour the adult worm that produces eggs that infect the brine shrimps. Therefore, bird watchers should perhaps be thankful for the presence of shrimps heavily infected by a wide variety of parasitic worms!

Reference:
Sánchez, Marta I., et al. (2013) "High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts." Parasitology Research 112: 1913-1923.

Himasthla elongata

Photo taken by and used
with permission from Kirill V. Galaktionov

Today's post is bit of a trip down nostalgia lane for me, as the experimental model used in the study we are featuring today is a host-parasite combination similar to one I worked on for somes years during my PhD and postdoc - bivalves and flukes (specifically flukes from a family called the Echinostomatidae - identifiable by their fetching array of collar spines). Much like a parasite that I worked on (Curtuteria australis), Himasthla elongata encysts in the foot muscle of its host and transforms into a stage called the metacercaria (see left photo). But whereas C. australis infects cockles on the mudflats of New Zealand, H. elongata infects mussels on the rock shores of the White Sea.

By embedding itself in the mussel's foot, this parasite hinders the mollusc's ability to move and produce the all-important byssus threads that anchor them to rocks or other substrates. If it becomes infected with too many H. elongata, the mussel loses its ability to use its foot and its survival becomes compromised. Thus this parasite selects for the evolution of mussels that are resistant against it, resulting in a coevolution arms race between the mussels and H. elongata.

To find out how parasites and mussels fare against each other and the role that genetic variants in both the parasite and host population play in coevolution, a group of Russian researchers conducted a series of parasite survival studies and experimental infections. First of all, they did an in vitro experiment where they exposed the infective larval stage of H. elongata (called cercariae) to the blood of different mussels. This was followed by an experimental infection study where they exposed some of those same "blood donor" mussels to H. elongata larvae and measured how well they were they at resisting the parasite.

Photo taken by and
used with permission
from Kirill V. Galaktionov

The researchers obtained parasite-free mussels from an experimental aquaculture farm to act both as blood donors and infection targets for H. elongata cercariae, while the parasites themselves came from infected periwinkles that the researchers collected from an intertidal inlet. These periwinkles harboured the asexual proliferative stages of H. elongata which produce cercariae (see photo on the right). Because H. elongata undergoes asexual multiplication in the periwinkle host, the researchers were able to obtain multiple genetically-identical (clones, essentially) cercariae from each infected snail and test them against a group of genetically-varied mussels.

The researchers paired up 51 different H. elongata clonal lines to blood samples from 161 randomly selected mussels for a total 764 parasite versus host blood combinations* (!). They found that a handful of mussels had blood that killed every single cercaria that came in contact with it and another handful had blood where all the cercariae survived and successfully turn into metacercariae. It seem that H. elongata is adapted specifically to surviving contact with mussel blood (just that it seems that some are better adapted than others), because when they tried to incubate H. elongata cercariae in the blood of the soft-shell clam (Mya arenaria), all the cercariae died within an hour or two.

In a follow-up experiment, they selected 39 of those mussels that had previously served as "blood donors"and exposed each to one of twelve H. elongata clones that were used in the in vitro experiment and found that the results of the in vitro experiment were pretty good indicators of the outcome of those experimental exposures - mussels with blood that killed all the H. elongata they came in contact with were also better than most at fighting off infection by the parasitic fluke. The rest of the mussels were fairly vulnerable to H. elongata and a small handful offered almost no resistance. The larger mussels were generally better at fighting off the parasites with just a little over a quarter of the H. elongata cercariae getting through, while more than half of the cercariae successfully established in the smaller mussels, regardless of the host or parasite genotype.

The parasites themselves also varied in their effectiveness at infecting mussels. Most of the H. elongata clones were fairly good at it, there were a few "superstars" that were especially effective at becoming metacercariae in mussels, while there were also a few "duds" that were hopeless, regardless of which particular mussel they were up against.

Other host-parasite coevolution arms races operate under so-called "gene-for-gene"-type interaction. Examples of which include the bacterial parasite Pasteuria ramosa in waterfleas where a specific parasite strain is most successful at infecting a specific host strain, or the arms race between parasitoid wasps and aphids' protective symbionts where you have wasp lines that can overcome most of aphid protective symbiont strains out there, but remain vulnerable to one specific strain of the symbiont.

What those Russian scientists found with the mussel-Himasthla elongata system does not seem as absolute. Instead, we see variation in overall performance in the population of both host and parasite: there are parasites that ranged from being super effective at what they do, all the way down to complete duds and everything in between. They in turn are going up against mussels with varied level of resistance against them, and how much of a fight those bivalves put up can also be affected by the age and/or body size of the host. However, what it does have in common with those "gene-for-gene"-type coevolutionary systems is that there is a genetic component to either infectivity or resistance, and none of the host are completely resistant to all parasites, just as not all the parasites are completely effective at infecting the available hosts.

Reference:
Levakin, I. A., Losev, E. A., Nikolaev, K. E., & Galaktionov, K. V. (2013). In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology, 87: 180-188.

*because there was simply not enough blood and cercariae to go around, not every H. elongata clone was exposed to the blood from every mussel

Urogasilus brasiliensis

While most people who have some passing familiarity with copepods would know them as tiny zooplankton crustaceans, a large number of them are actually parasitic. In fact, about a third of all known species of copepods are parasites and with about 13000 known species of copepods in total, that is a lot of parasitic species. These parasitic copepods infect a wide variety of aquatic animals and come in all kinds of weird shapes.

Photo composed from Fig 4 and Fig 5 of the paper

Naturally, many of them are fish parasites as fish are such an abundant and diverse group of aquatic animals. But while most parasitic copepods of fish usually infect the skin or gills of their host, today's parasite stands out from the crowd as it inhabits the fish's urinary bladder and is the first parasitic copepod ever known to live in that organ.

Now that is not to say that a fish's bladder is a parasite-free zone - far from it. You wouldn't think that an organ that gets periodically filled up with urine and metabolic waste would be prime real estate, but there are all kinds of parasites that call it home ranging from single-cell eukaryotic parasites, to myxozoans, parasitic flatworms like monogeneans and digenean flukes - some of them are even found exclusively in the urinary bladder. However it is an unusual habitat for a parasitic copepod seeing how, as mentioned above, most live on the fish's skin or gills

Today's featured parasite, Urogasilus brasiliensis, is a newly described species that has been found in some freshwater fish living in the Cristalino River, a tributary of the Araguaia River in Brazil. The known hosts to this parasite include the tiger fish and two species of peacock bass. Much like other parasites that infect many different species of hosts, some hosts are just better than others and that is the case for U. brasiliensis too. This copepod tends be more common in the tiger fish and grows to a larger size in that host, indicating that it is possibly a better host for the parasite than the peacock bass. But while U. brasilensis is not particularly picky about what species of fish it infects, it is picky about where it lives within that fish - it is always found in the bladder.

Living in the urinary bladder does present some physiological challenges - as mentioned above, it is an organ that regularly alternates between being empty and being full of urine. Such periodic shifts in the concentration of fluid surrounding U. brasiliensis would cause severe osmotic stress like those experienced by animals that regularly migrate between freshwater and marine habitats. Presumably U. brasiliensis has overcome this particular obstacle and in doing so has been able to colonise an otherwise fairly vacant niche not occupied by other parasitic copepods.

Urogasilus brasiliensis is one of the few parasitic copepod that has evolved into an endoparasite (internal parasite) as opposed to being an ectoparasite (external parasite). But it is not alone - a few other species of copepods have also evolved to conquer that frontier, some of which we have featured on this blog such as one that lives in the cephalic canal of fish in Australia and another species lives in the rectum of rockfish.

Reference:
Rosim DF, Boxshall GA, Ceccarelli PS. (2013) A novel microhabitat for parasitic copepods: A new genus of Ergasilidae (Copepoda: Cyclopoida) from the urinary bladder of a freshwater fish. Parasitology International 62: 347-354

Cyrtosomum penneri

The Atractidae is a family of nematodes (roundworms) that are found in the intestines or lungs of various vertebrate animals. Instead of producing eggs, the adults produce larvae that are ready to infect as soon as they leave their mother's womb. While it is well-known that a host already parasitised by an atractid nematode can infect themselves again thanks to the infective larvae, it was not entirely clear how this parasite get passed between different hosts.

Photo taken by Charles R. Bursery
Used with permission from Gerrut Norval

For the paper we are looking at today, a team of scientists studied a species of atractid nematode that infects lizards - Cyrtosomum penneri - and conducted a series of experiments to figure out how this parasite is transmitted in Brown Anoles. They did this by administering larval worms in a number of different ways to lizards that they had previously de-wormed with anti-parasite drugs. To ensure that they could tell afterwards if the worms they found in the anoles were the ones they administered, the scientists labelled them with a fluorescent dye (the same type as the ones I used in experimental infections to track larval flukes in bivalves: see here and here)

The larvae of many parasitic nematodes infect their hosts through being accidentally swallowed, usually while their hosts are feeding (this is commonly how mammalian herbivores like sheep, cattle, and horses become infected). However, when these scientists tried to do the same with C. penneri larvae by pippetting larval worms down the lizards' throats, none of the larvae were successful in establishing in the host.

Instead, they found the feces of anoles that had been fed parasite larvae were full of dead worms - presumably they were killed by gastric acid. Indeed, the environment in which C. penneri is usually found, down in the lower intestine, is pretty benign comparing with the acidic milieu of the stomach. But when they pipetted larval C. penneri into the cloaca of the lizard, it worked every time. Instead of having a separate opening, lizards have a cloaca - a common opening for their intestinal, urinary, and reproductive tracts. When lizards mate, they bring their cloacae together - and this is when C. penneri gets transmitted.

Yes, that's right - C. penneri is a sexually transmitted infection.

In the mating trials run by those scientists, male lizards infected with the nematode passed it on to the female they mated with every single time, whereas the female lizard only passed the STI to the male in seven out of the ten trials they ran. In addition to anoles, C. penneri is also found in a few other lizard species such as the Mediterranean House Gecko and Eastern Fence Lizard. But while it infects those other lizards in addition to the Brown Anole, for some reason it does not appear to parasitise the Carolina Anole... which means that it would be interesting to consider what happens to the parasite when something like what you see at this link happens...

Reference:
Langford, G. J., Willobee, B. A., & Isidoro, L. F. (2013). Transmission, host specificity, and seasonal occurrence of Cyrtosomum penneri (Nematoda: Atractidae) in lizards from Florida. Journal of Parasitology 99: 241-246

Prosorhynchoides borealis

The study we are featuring today is one of the more difficult, yet under-appreciated type of studies in ecological parasitology; working out the life cycle of a multi-host parasite. Piecing together a parasite's life cycle is like conducting a forensic investigation into nature, which requires a lot of persistence and hard work gathering clues and putting together a picture from widely scattered jigsaw pieces. It is difficult enough working out a life cycle when the parasite in question lives in a relatively accessible habitat such as a lake or an estuary, but today's parasite, Prosorhynchoides borealis, is a fluke with a life-cycle that takes place far from shore in the sea off the southern coast of Iceland.

Image from Fig 2a of the paper

We start this journey in a tiny clam (Abra prismatica) that lives buried in mud and sandy seabeds at depths of 15–164 metres in the sea off South Iceland. Prosorhynchoides borealis uses the clam for the asexual stage of its life cycle, and by that I mean it turns the clam into a little parasite factory that pumps out free-swimming larvae called cercariae.

The researchers found that clams that are below a size threshold of 11 mm appear to be free of this parasite, but once they grow above that size, infection rates steadily increase and almost half the clams above 11 mm in size are infected. This resembles a pattern that has previously been found for other bivalve parasites (for example see this study and this study). The asexual stages of the P. borealis are made up of interconnected, branching modules that extend throughout the clam's body like aggressive roots (see the picture above), invading various internal organs to draw out nutrients to fuel the production of hundreds of cercariae.

Extending from the back of each cercaria are a pair of long filaments that can reach more than six times the length of the cercaria itself (see the picture below). When they are released into the water, those filaments unfurl and fully extend and the cercaria resembles a "V" as it floats in the water. While it can't swim, it can use its tail to hang passively in the water, carried along by the current. In related species, scientists have observed the cercariae attaching to each other by the end of those extended filaments so that together they form a floating "net of cercariae".

Image from Fig 2b, 2c of the paper

And why would they want to turn themselves into a miniature drift net? All the better to get tangled up in the gills of the parasite's next host - an unsuspecting fish cruising by in the wrong place at the wrong time. The next hosts of P. borealis are fish from the Gadidae family, which are also known as codfish. Once it gets under the skin of a cod, it migrates to the nerves and the brain cavity. There it grows and transforms into a stage called a metacercaria. But this is not even the parasite's final form; it needs to be eaten by an even larger fish to complete its life cycle.

Gadids like cod, haddock, whiting, and pollock are generally fairly large fish, so if that is not the final destination for P. borealis, then the last host must be a pretty voracious predators that can eat a whole cod for lunch. Enter the monkfish Lophius piscatorius.

Lophius piscatorius is a fish with a big mouth, big appetite and indiscriminate taste, and that suits P. borealis just fine. A monkfish has no trouble when it comes to eating a fairly sizeable cod as you can see in this video. In fact, it has little hesitation when it comes to dining on a lot of things, including the occasional sea bird. And it is in the intestine of this fish that the adult stage of P. borealis spends the rest of its life, nestled in a nutrient-filled highway of muscle and laying eggs that are carried out into the sea with the rest of the host's...waste traffic, where it can then go on to infect clams and begin the cycle anew.

So if you have ever seen an unfortunate cod ambushed by a well-hidden monkfish, then what you just saw was not just a cod being eaten by a big ugly fish with an alarmingly large mouth, you have also just witnessed another few dozen P. borealis completing their life cycle.

Reference:
Eydal, M., Freeman, M. A., Kristmundsson, A., Bambir, S. H., Jonsson, P. M., & Helgason, S. (2013). Prosorhynchoides borealis Bartoli, Gibson & Bray, 2006 (Digenea: Bucephalidae) cercariae from Abra prismatica (Mollusca: Bivalvia) in Icelandic waters. Journal of Helminthology 87: 34-41