Ismaila sp.

Those who have been reading this blog for a while might recall that this time last year, I featured some guest posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class. Well, it is happening again for this year! For those who are unaware of this, 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, 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 2014. To kick things off, here's a post by Courtney Waters on a paper published in 2002 that documented the diversity of parasitic copepods that live inside sea slugs off the coast of Chile (see also this post from June this year).

Picture of infected sea slug from the paper

Bright colourful sea slugs are every diver’s ultimate find. Imagine getting up close to it with that macro lens and... wait, what's that protruding from the slug's side? They appear to be the egg sacs of an endoparasitic copepod - small crustaceans, which parasitises the insides of these soft‐bodied molluscs. The aim of the study I am writing about for this post was to expand existing knowledge about these endoparasites, particularly the genus Ismaila from the family Splanchnotrophidae. This particular genus is characterised by the presence of a pair of well-developed first appendages which are absent in related genera.

The six year study was based mainly in Chilean waters where different sea slug species were collected and examined for parasite infection. This was done simply by examining the sea slug externally without dissection as the egg sacs of the adult parasite protrude conspicuously from the abdominal wall of the host (see the accompanied figure). Over 2000 specimens from 47 species of sea slug were examined in such a manner and only 8 species of slugs were found to be parasitised by those copepods. These parasites are very host specific and each parasite species is only found in one host species. The overall infection rate was 13% which is the highest infection prevalence documented. Fortunately, these parasites only like the soft innards of our mollusc friends - otherwise I would not be so jealous of the scuba divers who were doing the collecting!


Obvious differences were seen between the infection rates of different host species, with some parasitised more than others. For example, in several species of hosts, only one individual was observed to be infected, whereas for other species the infection rate was almost 90%. The infection frequencies for two of the main sea slug host species did not vary much between years and seasons, though this would need to be verified with further studies. An additional result of the study was information on the evolution of these parasites. The disjunct distribution of the copepods along with their host groups suggest that these parasites had evolved from an ancestor that was not very host-specific, but as different populations became isolated, they evolved to be very specific to their hosts. This resulted in scattered pockets of area with high parasite abundance. As for why they have not spread out to wherever appropriate hosts are available, this is likely due to other life-cycle requirements of the parasite which are currently unknown.

In summary, the study found 4 new species of host for splanchnotrophid copepods, taking the world total to 47 host species (at least as of 2002 when this paper was published), with 12 of which being found in Chilean waters and 9 of them being host to copepods in the Ismaila genus. This means the waters of Chile have over a quarter of all known splanchnotrophid species. Additionally, the percentage of infected sea slug in Chile is ten times higher than anywhere else in the world - a fact that, if I was a sea slug in those waters, would probably give me the chills...

Reference:
Schrödl, M. (2002). Heavy infestation by endoparasitic copepod crustaceans (Poecilostomatoida: Splanchnotrophidae) in Chilean opisthobranch gastropods, with aspects of splanchnotrophid evolution. Organisms Diversity & Evolution, 2: 19-26.

This post was written by Courtney Waters

Ismaila belciki

Photo of infected Janolus fuscus
used with permission from Jeff Goddard

If you ever find yourself down by the sea, you may come across some very flamboyant sea slugs call nudibranchs. But beneath their colourful exterior, some of them are harbouring a dark secret in the form of a very strange looking parasite. These parasites live hidden inside the main body cavity of their molluscan host, so if you are unfamiliar with this particular critter, you might not even notice it. The main thing that gives away their presence are a pair of egg sacs poking out of the sea slug (see photo on the right). Those egg sacs belong to a parasite call Ismaila belciki - it is a crustacean, though it looks more like one of Cthulhu's lovechild or something out of Men In Black.

Ismaila and other copepods of the Splanchnotrophidae family are specialist parasites of sea slugs and they can get pretty big in comparison with their host, taking up substantial room and resources. Ismaila belciki infects Janolus fuscus, a nudibranch found along the west coast of North America from Alaska to California, as well as the shores of northern Japan. In some areas, such as Coos Bay, Oregon where the study we are featuring today took place, up to 80% of the slugs are infected with this odd creature. Having such a big parasite sitting in the middle of slug's body soaking up nutrient obviously carries some kind of cost - but just how much?

Photo of a female Ismaila belciki with an
embraced dwarf male front and centre.
Photo by and used with permission
from Maya Wolf

A pair of researchers from University of Oregon decided to find out just how costly this parasite is to its host. They compared the growth, survival, and reproductive capacity of infected and uninfected J. fuscus, and measured how much resources the parasite takes up.

While I. belciki did not seem to interfere with sea slug's growth, infected slugs do have a lower survival rate. Additionally, they have shrunken gonads that are only capable of producing about half as many eggs as healthy slugs. But the reproductive capacity of those afflicted sea slug suffers not just in terms of quantity, but in quality as well. In addition to producing fewer eggs, infected slugs also produced eggs that were smaller, and the baby slugs that hatch out of them also have lower survival rates.

So it seems I. belciki can be very harmful indeed, but it cause even greater harm if the parasite itself is breeding. The researchers noted that I. belciki bearing developing egg sacs exert a greater toll on the host than egg-free parasites. A female I. belciki is an egg-laying machine that can churn out over 88000 embryos per month and all the expenses for that are paid for by the host. To fuel the development of its eggs, I. belciki draws from the same pool of resources that the host normally use for its own egg production. Slugs with brooding I. belciki produce even fewer eggs than those that are "just" stuck with an egg-free parasite.

It is as if the sea slug is a factory that has been retooled from solely making slug babies into one which now has to divert some of its attention and raw material to making parasite babies too, via a proxy in the form of a female I. belciki. Given that Janolus fuscus usually only live for five months, by shorten their lives and severely reducing their reproductive capacity, I. belciki might actually be putting a natural check on the population growth of these flamboyant nudibranchs.

Reference:
Wolf, M., & Young, C. M. (2014). Impacts of an endoparasitic copepod, Ismaila belciki, on the reproduction, growth and survivorship of its nudibranch host, Janolus fuscus. International Journal for Parasitology 44: 391-401.

P.S. I will be attending the annual Australian Society for Parasitology annual conference in Canberra, Australia between 30th June to 3rd July. So watch for tweets about highlights from conference at my Twitter @The_Episiarch! Meanwhile, I have written a article for The Conversation about the crab-castrating barnacle Sacculina carcini - you can read it here.

Anilocra nemipteri

Photo from Figure 1 of the paper

The parasite in the study being featured today makes a living riding around on the top of a fish's head and occasionally gnawing on its face. It is in the same family as the infamous tongue-biter, the Cymothoidae, though technically this one is more of a face-hugger.

Anilocra nemipteri is found on the Great Barrier Reef of Australia and it makes a living by hitching a ride (and feeds) from the bridled monocle bream, Scolopsis bilineata. It is a pretty common parasite - in some areas, up to 30 percent of monocle bream carry one of these crustaceans on their head like a nasty blood-sucking beret that stay attached for years.

As you can see from the photo, A. nemipteri is a fairly big parasites comparing with the size of the fish (in some case they can reach as almost one-third the length of the host fish!), and having a parasite of that size hanging off your face is going to be quite a drag - literally. That is bad news for a little fish like the monocle bream that needs to make a quick getaway from any hungry predators on the reef. So just how much of a drag is A. nemipteri? A related species - Anilocra apogonae - which clings to the cardinal fish (Cheilodipterus quinquelineatus) is known to cause their host to swim slower and have lower endurance. Does the same apply for A. nemipteri and the monocle bream?

To find out, scientists compared how quickly the fish can respond to an attack and their Flight Initiation Distance (FID) in both a laboratory setting and in the field. The FID is the distance from a predator at which an animal decides to flee - risk-takers have a shorter FID. They divided the monocle bream into three different groups: parasite-free fish, fish carrying an A. nemipteri, infected fish which just had their parasite removed.

Photo from Figure 1 of the paper

The research team simulated an attack by a bird (with a weighted PVC pipe) on fish in specially-designed experimental tanks and filmed the response to measure the fish's reaction time to the attack. Even though one would think all that face-gnawing from A. nemipteri would have weakened their host, and not to mention the body of the parasite itself causing significant drag, the escape performance of parasitised fish was not all that different from unparasitised - they reacted and got away from the attack just as quickly as their unburdened buddies. In the field experiment, the scientists donned snorkelling gear and tried to approach any monocle breams they spotted and measured how close they could get to the fish before they fled. There, they found parasitised fish have a slightly shorter FID than parasite-free fish, but not significantly so.

Fish that are infected by A. nemipteri are smaller than uninfected ones, and it just so happen that smaller fish tend to allow predators to get closer to them before fleeing. But whether this is due to the parasite is another matter. Are parasitised fish smaller because their growth have been stunt by A. nemipteri? Or does this face-hugger simply prefer smaller fish because larger and older fish might have built up an immunity to it?

Though it may seem less exciting when we find a parasite doesn't cause much behavioural changes in its host, it is vital to our understanding of host-parasite relationships. Perhaps it means the host is able to compensate for the presence of the parasite. Also it is not clear what the long term cost of having A. nemipteri might be over the life time of the fish. It is also important to treat such a case in its context. Unlike other parasite which have a complex life-cycle and depend upon its host getting eaten by a predator to reach maturity, A. nemipteri is an external parasite that simply sticks to a host and stay for life - if the parasitised fish is eaten by a predator, it'll go down with the host like a bit of garnish and be digested too.

So it is probably just as well that A. nemipteri is not too much of a drag to have around.

Reference:
Binning, S. A., Barnes, J. I., Davies, J. N., Backwell, P. R., Keogh, J. S., & Roche, D. G. (2014). Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Animal Behaviour 93: 1-7.

Loxothylacus panopei

Photo by Inken Kruse via the Hare Lab

Some parasites can manipulate their host's behaviour in very spectacular ways, but there are also other parasites that change their host's habits in more subtle manners. While such alteration to the host can seem fairly minor, they can still result in some very profound impact on the rest of the ecosystem.

There is a group of parasitic barnacles call Rhizocephala (the most well-known species is Sacculina carcini) that are capable of castrating their host, turning them into unwitting babysitters that nurture the parasites' brood. The infected crab display some very obvious changes to their behaviour, and in some cases, their appearance. But the study we are featuring today shows that apart from turning them into doting mothers for the parasite's babies, these barnacles can also alter the crab's behaviour in less obvious ways that have ramifications for other marine inhabitants.

The flatback mud crab (Eurypanopeus depressus) lives in estuaries on the coast of South Carolina and it is infected by a species of rhizocephalan call Loxothylacus panopei. In addition to doing the usual host castrating and commandeering trick, L. panopei also changes how this crab responds to potential prey. Usually, the mud crab has an omnivorous diet, dining on algae as well as worms, smaller crustaceans, and sponges. Sometimes they may also have a crack at more armoured prey like mussels. But crabs that are infected with L. panopei lose their appetite for such shell-covered fares.

When researchers offered uninfected crabs with piles of mussels, the crabs acted like they were at an all-you-can-eat seafood buffet and ate as much as they can - the more mussels the researchers presented them with, the more they ate. But no matter how many mussels they offered to crabs that were infected with L. panopei, they simply eat one and call it a day. The parasitised crabs also took longer to get their act together and this seems to be related to the size of the crab's parasite - the larger the parasite has grown, the longer the crab takes to start digging into a mussel.

Based on a field survey of the estuary where the study took place, the researcher concluded that about a fifth of the crab at that location were infected with L. panopei. Given the effects that L. panopei has on their crab's appetite for shellfish, it seems that the mussels might have an unlikely ally in the form a parasitic barnacle. The finding of this study share some parallel to another paper that we featured on this blog earlier this year, on the muscle-wasting parasite that infects a predatory shrimp and curb its otherwise ravenous appetite.

Ecosystems are made up of complicated networks of biological interactions and parasites can mediate predator-prey interactions in different, and sometimes conflicting ways. While some parasites can make prey animals more vulnerable or accessible to predators, there are other like L. panopei that may be reducing the appetite of the said predators. The subtle interplay of such parasite-mediated interactions are often overlooked or ignored, but their effects on the ecosystem are certainly there if you know what to look for.

Reference:
Toscano, B. J., Newsome, B., & Griffen, B. D. (2014). Parasite modification of predator functional response. Oecologia 175: 345-352.

Cucumispora dikerogammari

Invasive species can be very disruptive - cane toads, rabbits, water hyacinth, and zebra mussels are just a few well-known examples of species that have been introduced to areas outside of their original geographic range and have caused extensive ecological disruption in their new home. One of the hypotheses for why some introduced species become so successful when they arrive at a new region is called the "enemy release hypothesis". In their new home, introduced species run amok as they are no longer hounded by their usual foes that would otherwise keep their population in check.

Top: A heavily infected amphipod
Bottom: Spores of C. dikerogammari
Photo from here

Dikerogammarus villosus is an amphipod (a little, shrimp-like crustacean) from the Ponto-Caspian that has invaded western and central Europe, and is now also found in the United Kingdom. They might only grow up to a little over an inch long, but they are voracious little predators that eat everything smaller than themselves, including each other. Released from their usual predators and parasites, D. villosus rips through the freshwater life of its new neighbourhood. But they have not completely escaped from their past foes; one parasite has managed to come along for the ride, and it is a microsporidian called Cucumispora dikerogammari.

As far as the parasite goes, Cucumispora dikerogammari is a pretty nasty one. It invades the host's muscles, reproduces prolifically and eventually kills the host by overwhelming it with sheer numbers. There is some concern that this parasite can spill over into the native invertebrates and add insult to injury to the local stream life. But on another hand, a new study shows that this parasite might be one of the few things holding back this voracious invasive amphipod from causing even more destruction.

A group of scientists from France conducted a study to looked at how C. dikerogammari affects the activity levels and appetite of D. villosus. They observed the behaviour of both infected and uninfected amhipods in a water-filled glass tube and noticed that amphipods at a late stage of infection that are visibly "filled to the brim" with parasite spores are actually more active than healthy amphipods or those that are not visibly parasitised because they are at a much earlier stage of the infection.

Close-up of a C. dikerogammari spore from here

Furthermore, they also presented amphipods with midge larvae (also known to some as "bloodworms") to see how many they ate. Both infected and uninfected D. villosus pounced on those insect larvae, but the heavily infected amphipods ate far less than the healthy ones. For whatever reason, this parasite seems to cause D. villosus to lose its appetite, and given this crustacean's reputation of eating everything that it can get its claws around, this may have significant ecological ramifications. It could mean that C. dikerogammari may be subtly reducing the impact these amphipods have on the areas where they have been introduced.

But why would heavily-infected D. villosus, which would have much of their muscle mass already converted to parasite spores by C. dikerogammari, be more active? Well, it could just be an odd manifestation of the disease, but if it is, it is certainly a useful one for this parasite - as it depends upon cannibalism for transmission to new hosts. Dikerogammarus villosus are rather homely creatures and usually prefer to stay under a shelter and wait for potential prey to wander by. By getting their host out and about, C. dikerogammari might increase the chances that its host will either run into one of its cannibalistic buddies, or die out in the open where it can be scavenged by other D. villosus.

It seems that for this little invasive amphipod, no matter how far you go, you can never really run away from your past (foes).

Reference:
Bacela-Spychalska, K., Rigaud, T., & Wattier, R. A. (2013). A co-invasive microsporidian parasite that reduces the predatory behaviour of its host Dikerogammarus villosus (Crustacea, Amphipoda). Parasitology 141: 254-258.

Phronima sp.

Today's guest post is by Katie O'Dwyer, a PhD student currently at University of Otago in the Evolutionary and Ecological Parasitology research group. In one of my conference reports last year, I mentioned some of the research that she is currently conducting on parasitic flukes that live in periwinkles. She has provided us with a post about a parasite that she came across while walking along a beach in New Zealand.

Phronima and its salp barrel.
Photo by Katie O'Dwyer, used here with permission

After recently finding some salps containing the amphipod Phronima, washed up on a beach in New Zealand, I decided this was a worthy group to compose a blog about. It helped too that I was already interested in this group of crustaceans, having assisted with some work on them in Ireland. Read on for some interesting information on this little studied group of parasitic organisms…

Imagine a parasite which can create its own mobile nursery for its young, a parasite which is thought to be the inspiration behind the chestbusting xenomorph in the popular movie Alien. Well imagine no more! Introducing Phronima, the pram bug. These amphipods are members of the Phronimidae, a group of ten species of hyperiid amphipod, which occur in the water column throughout the open ocean. This sets them apart from their close relatives, which typically inhabit the benthic environment of the seafloor. So what has allowed this particular family to adapt to the pelagic or open water environment?

Those adorable little babies!
Photo by Katie O'Dwyer, used here with permission

Enter salps. What is a salp? Salps are gelatinous zooplankton which drift throughout our oceans. They may occur singly or in huge chains composed of individual salps linked together. Phronima is equipped with impressive front claws and with these they attach to an individual salp and carve away its insides until it forms a barrel. Phronima then climbs inside and sails the sea from inside a gelatinous barrel, collecting food from the water column. A number of questions may now come to mind regarding this symbiosis; has Phronima killed its host, which suggests that it is a parasitoid rather than a parasite, and why does it carry this barrel around as it must be pretty energetically expensive, right?

Well, as mentioned, these organisms live in the open ocean which presents several challenges to collecting samples for answering these questions. However, some dedicated researchers have indeed managed to study these fascinating creatures on the rare occasion that such an opportunity arises. From their research they have found that the salp in fact still contains live cells, although it hardly resembles a salp anymore with just a barrel of tissue remaining. The presence of live cells means that the barrel maintains its structure and that is important for Phronima to have a sturdy home. As the barrel barely resembles a live salp any longer, Phronima should really be considered as parasitoids rather than parasites.

Do a barrel roll!
Photo by Katie O'Dwyer, used here with permission

As for the energy involved in carrying around this barrel, the barrel provides a larger structure than the amphipod itself and this enables the Phronima to be more buoyant in the water column. However, some energy is still required to carry around this jelly barrel. Overall energy usage by Phronima is higher than that of benthic amphipods but on the lower spectrum compared with other pelagic or open water amphipods. This suggests that Phronima have indeed adapted to a unique niche which enables them to travel in the water column with their young and access new food resources without this behaviour being too energetically costly.

One unusual finding in the research thus far is that male Phronima are also found in barrels. If Phronima is known as the pram bug, which suggests the barrel is important for carrying offspring, then why should males carry a barrel too? Could they use it as part of some mating strategy, where they pass the barrel on to the female they mate with? Due to the difficulties associated with studying organisms that dwell in the open ocean many questions remain unanswered and this leaves us ever more curious and fascinated by creatures such as Phronima.

References:

Hirose, E., Aoki, M. N., & Nishikawa, J. (2005). Still alive? Fine structure of the barrels made by Phronima (Crustacea: Amphipoda). Journal of the Marine Biological Association of the United Kingdom 85: 1435-1439.

Bishop, R. E., & Geiger, S. P. (2006). Phronima energetics: is there a bonus to the barrel? Crustaceana 79: 1059-1070.

This post was written by Katie O'Dwyer.

Choniomyzon inflatus

Photo of C. inflatus from the paper

I guess you could say that the parasite we are featuring today is a "balloon animal" and indeed its name refers to that property. According to the paper that described and named this copepod - Choniomyzon inflatus - "The specific name of the new species is a reference to its swollen prosome, which resembles a balloon."

But you won't be finding this odd little crustacean at any kid's party, instead it is usually attached to the egg masses of smooth fan lobsters (Ibacus novemdentatus) on the coast of western Japan. It is the third species from the genus Choniomyzon to have ever been described. The other two known species are C. panuliri, which are found on spiny lobsters from India, the British Solomon Islands and the Great Barrier Reef, and C. libiniae, which live on spider crabs from São Sebastião Island, Brazil. All three species attach themselves to the external eggs masses of their respective hosts.

SEM photo of C.inflatus
from the paper

So why do they look like a miniature hopper ball toy? Well, that relates to where they live and what they feed on. Chioniomyzon inflatus belongs to a family of copepods called the Nicothoidae and the reason they do this Humpty Dumpty impersonation is so that they can insinuate themselves amidst the eggs masses of larger crustaceans.

Normally the host crustaceans would remove any foreign particles or organisms that get caught up in their brood pouch or egg mass, but by disguising themselves as an egg, C. inflatus and their relatives can stay there undisturbed. And while the appearance seems comical to us, it is seriously bad news for its host because nicothoid copepods are egg-eaters - they have a syringe-like mouthpart with which they puncture their host's eggs and suck out their contents.

So C. inflatus masquerades as just another egg in the brood to avoid being expelled meanwhile munching on the actual eggs around it. This strategy is rather reminiscent of another creature that we featured during the first year of the Parasite of the Day blog - the cuckoo catfish which hides its eggs amongst that of mouth-brooding cichlids. You can read more about the cuckoo catfish here.

Reference:
Wakabayashi, K., Otake, S., Tanaka, Y., & Nagasawa, K. (2013). Choniomyzon inflatus n. sp.(Crustacea: Copepoda: Nicothoidae) associated with Ibacus novemdentatus (Crustacea: Decapoda: Scyllaridae) from Japanese waters. Systematic parasitology 84: 157-165.

Tracheliastes polycolpus

Photo of adult T. polycolpus from here

Tracheliastes polycolpus is a parasitic copepod that lives on freshwater fish and does so by attaching to the fins of its host, grazing on mucus and epithelial cells. While T. polycolpus can infect a handful of different freshwater fishes, it is primarily found on the beaked dace (Leuciscus burdigalensis). When they occur in large numbers, their feeding activities can severely erode the fins of their hosts, so much that in some fish the fins are gnawed down to mere nubs (see the photo below of a heavily parasitised dace, with outlines showing the missing fin tissue).

So when it gets crowded on this parasite's usual, preferred host, some T. polycolpus find a home elsewhere and start parasitising other species of fish living in the same area. Even though T. polycolpus is considered to be a host generalist and can infect multiple species of fish, not all fish are considered equally habitable for this parasite and it does have a predilection for certain species over others. So what determines which other fish end up acquiring these parasitic copepods?

A group of scientists from France conducted a study looking at T. polycolpus population on freshwater fish in two French rivers, focusing on the 10 most abundant fish species in those rivers. Of the fish that they examined, eight of them were cyprinids (the family of fish that include dace, roach, and carp) while the two remaining species were the stone loach and brown trout.

Photo of parasitised dace with missing fin tissue from this paper

Only cyrpinids were found to be infected with T. polycolpus and of those only four species (dace, nase, gudgeon, minnows) were found to be consistently infected across both study sites. It turns out that next to the beaked dace, the second most preferred host for T. polycolpus is Parachondrostoma toxostoma, also known as South-west European Nase. After the beaked dace, it was the most commonly infected fish, especially in the Viaur river where there was generally higher abundance of the parasite.

It just so happens that out of all the fishes in those rivers, the nase is most similar to the dace in terms of its general body size, feeding style and habitat, making it the ideal second choice for T. polycolpus. On the flip side, it seems that minnow is the worst host for T. polycolpus - it hosted the least parasites out of the four fish species that were found with T. polycolpus and the parasites that were found on minnows were smaller and produced less eggs than those found on the other fish species. This is probably due to the minnow being a smaller fish than the beaked dace or the nase, so it does not produce as much mucus for T. polycolpus to graze on.

So even when generalist parasites do infect other hosts, they prefer some familiarity. The more similar you are (physiologically and/or ecologically) to the parasite's preferred host, the more likely that you will be next in line to get infected should the parasite's preferred host become too heavily parasitised.

But here's an added to layer to this story which you might want to consider - the South-west European nase is actually listed as a vulnerable species - its population has declined by at least 30% in the past 10 years due to habitat destruction and hybridisation with introduced species, so if the number of nase continues to decline, what does this mean for T. polycolpus? Would this result in increased parasite pressure on other fish species as they find themselves soaking up the "excess" T. polycolpus? Or will the the beaked dace experience even more exacerbated pathology as T. polycolpus are left with less alternative hosts to infect?

Reference:
Lootvoet, A., Blanchet, S., Gevrey, M., Buisson, L., Tudesque, L., & Loot, G. (2013). Patterns and processes of alternative host use in a generalist parasite: insights from a natural host–parasite interaction. Functional Ecology 27: 1403-1414

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

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.

Hyperia curticephala

C. plocamia photo by
Rubén Arturo Guzmán Pittman

Generally speaking, jellyfish are not very appetising as food. They are composed mostly of water and armed with batteries of nasty stinging cells. Both of those characteristics together they make an unfulfilling and potentially painful meal. Nevertheless, they are fed upon by large pelagic fishes, and there are even some marine animals such as sea turtles that can live on a diet composed entirely of sea jellies. For those lacking the stomach for such squishy and venomous prey, there is still a way for them to obtain nutritional benefits from jellyfishes - and the parasite we are featuring today provides one such pathway.

The study we are looking at today focuses on a little parasitic crustacean that belongs to a group known as the Hyperiidea. They are amphipods that have evolved to live inside gelatinous animals of the open ocean. In the case of Hyperia curticephala, it dwells within the bell of the medusa Chrysaora plocamia - a rather large jellyfish that can grow up to a metre (a bit over 3 feet) in diameter.

H. curticephala image from here

Like other hyperiids, individuals of H. curticephala feed on the jellies that they live in. In turn, they can also provide food for those that feed on them. An avid consumer of these little crustaceans is the palm ruff (Seriolella violacea) - a fish that can grow to about 65 cm (about 2 feet) long. The palm ruff is one of a number of fish that are known to be "medusafish" as they are often found in close association with medusa jellyfishes.

When scientists examined the stomach contents of small (about 6-10 cm / 2-4 inches long) palm ruffs, they found them to be packed full of H. curticephala and nothing else. As they grew larger, the fish started having a more varied diet, but hyperiids still make up for over 97% of their prey. The amount of H. curticephala in the stomach of palm ruffs reaches a peak in February, just as the parasite also reaches very high abundances in the medusa when some individual C. plocamia can be infected with over a thousand amphipods (which in turn provides a floating banquet for any hungry palm ruff). The abundance of H. curticephala also reaches a high during November, but this was not reflected in the stomach content of the fish - so why is that? The scientists suggested that during this season, most of the medusae available are still quite small and while collectively they might be harbouring a high abundance of H. curticephala, because of their smaller bell size they are inaccessible to the palm ruff (which needs to get in or under the medusa's bell to reach the hyperiids). But by February, the medusae have grown to sufficient size that the fish are able to swim inside the jellyfish's bell to peck at the hyperiids.

Smaller fish can easily swim inside the jellyfish to feed on the parasites and are often found loitering within the host medusa (which also provides them with protection). Larger juveniles cannot enter the bell and have to settle for pecking off parasites, which happens to be in more accessible positions. In this manner, the palm ruffs act as cleaners for C. plocamia, protecting the jellyfish from the parasitic H. curticephala rather like cleaner wrasses that eat ectoparasites off coral reef fishes.

Reference:
Riascos, J.M., Vergara, M., Fajardo, J., Villegas, V., Pacheco, A.S. (2012) The role of hyperiid parasites as a trophic link between jellyfish and fishes. Journal of Fish Biology 81:1686–1695

Bolbosoma balaenae

Image from Figure 1 of the paper

Today's parasite is an acanthocephalan (also known as a thorny-headed worm) and its name should be a clue to what it infects - baleen whales. And what do most baleen whales eat? Krill - lots and LOTS of it. The authors of the study I am writing about in this post found Bolbosoma balaenae larvae infecting krill that were caught during a plankton trawl off the coast of Ría de Vigo, Spain in the NW Iberian Peninsula.

The krill serve as hosts for larval B. balanae and from there, they proceed to infect the next host of their life-cycle, which as mentioned above, are baleen whales where they develop into adult worms. Acanthocephalans as a whole generally only have two hosts in their life-cycle - a small arthropod intermediate host where the larval worm resides, and the vertebrate definitive host where the adult lives and reproduces. But many of the thorny-headed worms that infect marine mammals add another host into the life-cycle between the crustacean host and the vertebrate host - this extra host is known as a paratenic host. The paratenic host is different from the intermediate host, and here's why.

For parasites with complex, multi-host life-cycles, the intermediate host is an obligate component for successful completion of the cycle. It is where the larval parasites gather resources to undergo development into the next stage, and at the same time, the intermediate host also serves as a mean of transporting the larvae into the definitive host (usually by getting itself eaten by the said host). It is in the definitive host where the parasite reaches sexual maturity. In contrast, a paratenic host serves only as a transport, and while the parasite has to infect an intermediate host to complete its life-cycle, infecting the paratenic host is optional. Seeing how the parasite can technically go through its life without ever hopping inside the paratenic host, why do it at all?

Image from Figure 1 of the paper

In the case of other acanthocephalans that infect marine mammals (such as Corynosoma cetaceum), if they are accidentally ingested by their marine mammal hosts while still inside the tiny crustacean intermediate hosts, they will still reach adulthood. But because the chances of that happening is negligibly slim compared to the likelihood of the crustacean host being eaten by a fish, which itself is then eaten by the said marine mammal, incorporating a paratenic host greatly enhances its chances of completing its life-cycle.

However, all this is unnecessary for B. balaenae, as their next host - fin whales and minke whales - do in fact feed on those tiny crustaceans. The authors of this study found that the infection prevalence of B. balaenae in krill is very low - only one in every thousand krill was infected with B. balaenae. But considering that a fin whale gulps down about 10 kg (22 lb) worth of krill with every mouthful and eats about 1800 kg (4000 lb) of those little crustaceans each day,  they can easily pick a few hundred worms very quickly even though the infection level is relatively low in krill.

Just like another acanthocephalan we have previously featured on this blog, Acanthocephalus dirus, instead of simply shedding eggs that are released into the environment with the host's faeces, the female worm actually leaves the gut once she is filled with fertilised eggs (see this paper). So even though the whale is constantly being infected with new worms with every mouthful, there is also a constant turnover in the population in the form of mature female worms exiting the host.

Reference:
Gregori, M., Aznar, F.J., Abollo, E., Roura, Á., González, Á.F. and Pascual, S. (2012) Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Diseases of Aquatic Organisms 99: 37-47.

Metschnikowia bicuspidata

If you are a regular reader of this blog, at some point you would have read about the concept of coevolutionary arms races between hosts and parasites (see this for example). Previously, we have featured Pasteuria ramosa - a bacterial parasite of the waterflea Daphnia. Pasteuria ramosa is very picky about its host - specific strains are compatible only with specific host genetic lines, and as we have talked about in that previous post, this parasite is very harmful. Because of how virulent P. ramosa is to waterfleas and because the resistance by the host is dependent upon being the lucky genotype that is not compatible with whatever strain of the parasite which is most common at the time, this sets up an ideal situation for a Red Queen-style evolutionary arms race (and it is one that has been going on for long time).

Uninfected (top right) and
infected waterflea (lower left)
Photo by Meghan Duffy

But in some areas where P. ramosa is found, it also co-occurs with a different parasite - the one that we are featuring today: Metschnikowia bicuspidata. It is a yeast that also infects Daphnia (other fungal parasites also named Metschnikowia biscuspidata have been reported to cause disease in shrimps, crabs, even fish - but it is more likely that they are similar-looking fungi that have been lumped together). The study we are looking at today was conducted by a collaborative group of three researchers who wanted to find out what happens when waterfleas are confronted by both parasites.

Under such circumstances, will the presence of M. bicuspidata exacerbate the existing arms race between Daphnia and P. ramosa, or will it simply get in the way? If resistance for P. ramosa is also associated with resistance to M. bicuspidata, then it means Daphnia has a general mechanism for resisting both parasites. This scenario will simply select for general parasite resistance in the Daphnia population, reducing the level of genetic variation in the population (the raw material for ongoing Red Queen-style evolutionary arms race). On another hand, if Daphnia resistant to P. ramosa are negatively associated with resistance to M. bicuspidata, then it means resistance for one parasite will come at the cost to another - this trade-off in defending against two different parasites sets up an additional selective pressure that can potentially accelerate the arms race.

There are a number of key differences between the two parasites. While P. ramosa reduces the reproductive capacity of the host more than M. bicuspidata, the latter kills the host quicker. Metschnikowia bicuspidata is extremely lethal, killing infected waterfleas within 2-3 weeks of infection (whereas waterfleas can live up to 5-7 weeks after being infected by P. ramosa). The fungus releases its spores after the waterflea dies, and those infective spores can even survive passage through a fish's gut if their host Daphnia is eaten.

And unlike P. ramosa, infection success of M. bicuspidata depends not so much on encountering a host with the right genes, but through sheer persistence - the more often a waterflea is exposed to M. bicuspidata spores, the more likely that they become infected. This difference also manifests in the nature of outbreaks caused by the two parasites. Outbreaks of P. ramosa tend to be rarer and more limited, especially in genetically diverse populations, whereas M. biscuspidata is more prone to massive outbreaks that spread widely across the whole population. Even though it is not as discriminate about host genotype as P. ramosa, it is not as if M. bicuspidata does not influence the evolution of its host. But the way it affects host evolution is different to that of P. ramosa - instead of selecting for specific genotypes, it influences how much the waterfleas allocate their resources into either reproduction or parasite resistance.

In this study, the researchers found that different genetic lines of waterfleas varied considerably in their resistance to M. bicuspidata, but a waterflea's resistance to the fungal parasite did not in turn predict how well it also resisted P. ramosa. Instead, as found in previous studies, infection success of different P. ramosa strains depended upon the specific combination of host genotype and parasite genotype. This indicates that waterfleas have very different ways of resisting the two parasites, and that resistance to one does not lend protection to the other, but at the same time, nor does protection against one parasite increases a waterflea's vulnerability to the other.

Therefore, as far as the Red Queen arms race between waterfleas and P.ramosa is concerned, even though M. bicuspidata looms as a significant threat to the waterflea population, it is unlikely to significantly alter the coevolutionary dynamics between Daphnia and P. ramosa.

Reference:
Auld SKJR, Hall SR, Duffy MA (2012) Epidemiology of a Daphnia-Multiparasite System and Its Implications for the Red Queen. PLoS ONE 7(6): e39564. doi:10.1371/journal.pone.0039564

Mysidobdella californiensis

Photo taken from Figure 3 of the paper

Marine leeches are commonly known to feed on various vertebrate hosts - mainly fish and sea turtles. However, today's parasite stands out from the pack by associating itself with an arthropod. Instead of fish or turtles, Mysidobdella californiensis sticks its sucker onto mysid shrimps. Mysids are also known as opossum shrimps because the females have a little brood pouch (called a marsupium) in which they carry developing young.

The discovery of Mysidobdella californiensis actually occurred rather serendipitously. Back in the summer and fall of 2010, an unprecedentedly huge swarm of mysid shrimp appeared off the central Californian coast. Some of those shrimps got sucked into the water clarification system at the Bodega Marine Laboratory. With all this shrimp in the system, the lab staff began collecting them opportunistically for fish food. But then, they started noticing these little leeches attached to the shrimps, so they made a concerted effort to collect the shrimps directly from the water clarifier, and examine them under the microscope.

What they found were tiny leeches about 1.5 cm (a bit above half an inch) long. Approximately one in every six shrimp were found to have leeches on them, and each infected shrimp was carrying between one to three leeches. Seeing as this is a new species, at this stage very little is known about its biology except what can be inferred based on what we know of a related species - M. borealis - which has been studied in slightly more details. It is unclear whether M. californiensis (and related species) merely hitch-hike on the shrimp and use it to carry them to potential hosts, or if they in fact feed on the shrimp. In laboratory trials on M. borealis, the leeches refused to feed on any of the fishes that they were presented with, and none of the leeches were found to have fish blood cells in their gut. It is possible that Mysidobdella as a genus specialise in feeding on mysid shrimps. If that is indeed the case, then Mysidobdella would be the only marine leech known to feed on the blood of invertebrates rather than vertebrates. However, mysid blood has yet to be found in the gut of these leeches, so at least at this point, the diet of M. californiensis remains a mystery.

Reference:
Burreson, E.M., Kim, B. and Passarelli, J.K. (2012) A New Species of Mysidobdella (Hirudinida: Piscicolidae) from Mysids along the California Coast. Journal of Parasitology 98: 341-343.

Acanthocephalus rhinensis

image from figure 1 of the paper

The study which forms the basis of today's post features an acanthocephalan - also known as a thorny-headed worm - which lives in the intestine of European eels in Lake Piediluco in central Italy. Acanthocephalans spend their adult lives like tapeworms, clinging to the wall of their host's intestine, and absorbing nutrients from the pre-digested gut content. But unlike tapeworms, which mostly use suckers and small hooks to cling to the intestinal wall, an acanthocephalan has a formidable bit of armament which puts the tapeworms to shame. As its name indicates, at the front of the acanthocephalan is a hook-laden proboscis (see the picture on the right) to stab into the intestinal wall and firmly anchor themselves in place.

In Lake Piediluco, some eels were found to be infected with up to 350 Acanthocephalus rhinensis, though most eels had fewer than 50 worms. The eels become infected through eating little shrimp-like crustaceans called amphipods. The amphipods live mostly amongst the aquatic vegetation at the edge of the lake, and they are parasitised by the larval stage of A. rhinensis. If you thought the idea of having dozens of prickly-headed worms clinging to your intestinal wall with their nightmarish probosces is bad, A. rhinensis is downright brutal to the amphipod host.

image from figure 3 of the paper

The larval worm (called a cystacanth) occupies a large part of the little crustacean's body (see picture on the left), displacing many of its internal organs. About one in ten amphipods at Lake Piediluco are infected with A. rhinensis, and each amphipod had one or two worms inside them (probably because there wouldn't be much room for more). Acanthocephalus rhinensis imposes a massive burden on the little crustaceans - infected females can only successfully produce half as many eggs as uninfected females.

Armed with that formidable anchor, you would think that A. rhinensis would be able to establish itself in the gut of just about any fish it finds itself in. But it appears to be remarkably faithful to eels, which are the only fish found to have A. rhinensis in their intestines. Perhaps there are other immunological or ecological reasons that prevent this species from successfully infecting other fish.

In addition to establishing the life-cycle of A. rhinesis, another discovery made by the researchers actually served to amend an existing error in the scientific literature. In the original description of A. rhinensis, which was made based on nine specimens, this species is supposed to have a distinctive band of orange-brown (think spray-on tan) pigment just behind their proboscis, a feature that apparently distinguishes it from all the other Acanthocephalus species. However, the researchers who wrote this paper examined a total of over a thousand worms and not a single one had the supposed distinguishing band. But what gave those worms that orange-brown collar? The researchers suggested that this was caused by discolouration from being jammed so deeply into the intestinal wall that the worms inadvertently absorbed pigment from host's intestinal vessel which gave them a distinctive tinge just behind their proboscis.

So in addition to working out the life-cycle of A. rhinensis, this study also served to clarify old mistakes, which will help out any future researchers who work on this species.

Reference:
Dezfuli, B.S., Lui, A., Squerzanti, S., Lorenzoni, M. and Shinn, A.P. (2012) Confirmation of the hosts involved in the life cycle of an acanthocephalan parasite of Anguilla anguilla (L.) from Lake Piediluco and its effect on the reproductive potential of its amphipod intermediate host. Parasitology Research 11: 2137-2143.

Acanthocephalus dirus

The word parasite has a lot of connotations associated with it, and "maternal" is certainly not one of them. To most people, the term "freeloader" comes to mind (hopefully, this blog will show you that parasitism is actually a very challenging way of life). They also have a reputation as being pretty lousy parents. In most textbooks, parasites are usually considered as "r-strategists" - which produce many, many offspring and don't take good care of them (as opposed to a K-strategist which produces fewer offspring, but invest a lot into parental care - like an elephant). But not all parasites are bad parents, and today, I am going to tell you about a study on a maternal parasite which sacrifices everything (literally) for her offspring.

Acanthocephalus dirus has a reproductive strategy that is unusual for its group - the acanthocephalans or the thorny-headed worms (Acantho = "thorns", Cephala = "head"). In fact it is unusual compared to most intestinal parasites. Unlike some tapeworms, which profligately cast off segments (each containing hundreds of eggs) into the wilderness with abandonment, A. dirus has rather different approach. The impetus that spurred on this piece of research were two separate observations: (1) fish that are infected with A. dirus do not have any worm eggs in their feces (unlike most animals infected with intestinal parasites) and (2) perfectly healthy and intact female worms were often expelled from the definitive host. What the researchers found was that instead of simply laying eggs that are expelled from the worm and from the host, a female A. dirus actually retains her eggs until she become completely bloated with them - at which point she exits gracefully from the host fish's digestive tract. Some readers might recall a nematode that has a similar reproductive strategy, and that both lineages have evolved such a reproductive strategy independently. So why has A. dirus evolved such an extreme strategy instead of just laying eggs normally like other thorny-head worms?

One reason could be that A. dirus infects creek chub - which, as its name indicates - lives in flowing creeks. The chub acquire the worm through eating infected isopods in the stream (the picture shows the light-coloured infected isopod on the right, and the darker uninfected individual on the left), which become infected when they ingest worm eggs resting on the creek bed. Acanthocephalan eggs tend to float - so if the eggs are simply expelled into the environment, they would get washed away downstream and deposited where the isopods do not occur. Whereas with A. dirus, the worm's own body can act like a weight belt which would carry the eggs down to the sediment layer, so by the time the worm herself decays, the eggs are already in the sediment where isopods can pick them up.

Furthermore, laboratory tests showed that isopods like to eat egg-filled female worms as much as their usual food - leaf litter - and the worm body itself actually enhances the infection success of the eggs. Researchers found that when exposed to fresh eggs alone, fewer than one in four isopods became infected, whereas when exposed to gravid females, over 80% became infected (natural infection comes somewhere in between those at about 60%). By making the ultimate maternal sacrifice, A. dirus gives her offspring the best possible start in life.

Image from figure in: Seidenberg (1973) Journal of Parasitology 59: 957-962

Reference:

Kopp, D.A., Elke, D.A., Caddigan, S.C., Raj, A., Rodriguez, L., Young, M.L. and Sparkes, T.C. (2011) Dispersal in the acanthocephalan Acanthocephalus dirus. Journal of Parasitology 97: 101-105

Ascarophis sp.

When I saw the reports of giant amphipods being dragged up from the Kermadec Trench off the coast of New Zealand, my immediate thought was "I wonder what parasites it has?" This promoted me to do a write-up of a paper I've read recently, which is about a parasite that infects amphipods - admittedly those that are more modestly sized. Today, we are featuring a study on Ascarophis, a nematode worm that infects an intertidal amphipod (Gammarus deubeni) in Passamaquoddy Bay, New Brunswick, Canada. Compared with related species this worm has evolved to live the simple life(-cycle), and avoids the complications that come with having a complex life-cycle.

Previously on this blog, we have featured parasites that have evolved to take short-cuts with their complicated life-cycles. When a particular host is absent, such parasites may opt to ditch that host from their life-cycle, and switch up their developmental schedule. This is the case with the fluke Coitocaecum parvum. However, while C. parvum can switch between different life-cycles depending on circumstances, Ascarophis has completely abandoned that altogether, and has evolved to make things simpler by completing its entire life-cycle within its amphipod host. Usually, parasites with complex life-cycles use different hosts for different functions - i.e., one host might merely serve as a transport and/or resources for temporary development, whereas another acts as a mating ground and/or habitat in which it reaches maturity. So how can Ascarophis get so much functionality out of a tiny little crustacean?

Nematodes normally go through 4 larval stages (L1-L4) before becoming a sexual mature "fifth stage" worm (L5). The end of each larval stage is accompanied by a molt (rather like insects). In related nematodes that have retained their complex life-cycle, the L3 worms (which are ready to infect the next host) live encapsulated in the first host, while the L4-L5 live in the digestive tract of the final host. What the researchers found with the Ascarophis they collected from New Brunswick is that L1 and L2 worms were found in the muscle tissue, and upon reaching L3 the worms begin to migrate into the body cavity where they complete their development into adulthood and start producing eggs. Now compare this with Ascarophis from the White and Baltic Seas, which also infect amphipods, but uses a species of sculpin as their final host. Those fish acquire their infection by eating amphipods infected with L3 stage nematode, and the worms develop into adults in the fish's gut.

In effect, the Ascarophis from New Brunswick gets the most out of its little crustacean host by using different parts of the amphipod's body as surrogates for different hosts - instead of being transmitted to a different host, it simply moves to occupy a different part whose function is close enough to its needs for it to complete its development. Unlike the C. parvum, it appears that Ascarophis has abandoned the fish host altogether, and has committed itself to using the amphipod as the sole host for its entire life-cycle. Even though the Ascarophis found in the White and Baltic Seas have retained their complex life-cycle, researchers of this study suggested that they are the same species as the worms they looked at, but the New Brunswick variant has simply adapted to local condition and evolved a different life-cycle. However, it must be noted that the researchers have come to this conclusion based on the worm's morphology and as we have seen before, appearance can be deceptive with nematodes.

Through all that, this plucky little New Brunswick parasite faces one last problem - getting its eggs out of its crustacean host. For worms that live in inside a fish's gut, passing eggs out into the environment is a pretty straightforward affair - the eggs simply get washed out with the poop. But there is no exit in the body cavity of an amphipod, so how is a worm supposed to cast its eggs out into the environment? Well, this thrifty nematode simply waits for the host to die, and as the body disintegrates, the eggs are released as well. Of course, it helps that these amphipods have a tendency to cannibalise the rotting bodies of their fallen comrades - this presents the perfect opportunity for the parasite to infect a new batch of hosts - yet another reason to not gnaw on any random corpses you may come across.

Image modified from figure in the paper

Reference:

Appy, R.G. and Butterworth, E.W. (2011) Development of Ascarophis sp. (Nematoda: Cystidicolidae) to maturity in Gammarus deubeni (Amphipoda). Journal of Parasitology 97: 1035-1048.

Pasteuria ramosa

Parasitic infections can severely debilitate the host in many ways, sometimes this manifests itself as the loss of some, or even all, of the host's reproductive ability. Evolutionary speaking, an organism that cannot reproduce is as good as dead. However, it's not entirely clear who (if anyone) is benefiting from this outcome - is it; (1) a survival strategy by the host to temporarily free up resources to compensate for the parasite's presence? Or is it (2) an adaptive strategy by the parasites to divert as many resources as possible to themselves without compromising the host's ability for self-maintenance and survival? Or is it (3) merely an unintended side-effect of infection? Of course, (1) and (2) are not mutually exclusive, and in the case of (3), even if it had started out as an unintended side-effect of infection, if host castration resulted in higher reproductive fitness for the parasite, then that trait will be positively selected for and become part of the its repertoire of host-exploitation strategies.

Waterfleas (Daphnia) are infected by all manner of parasites (we featured one of them during the early days of the blog: Caullerya mesnili) ; most of them are pretty nasty - they often end up castrating and/or killing the host. Pasteuria ramosa is no different - it is a spore-forming bacterium that infects waterfleas, makes them bloated, darkening their body (see the right waterflea in the photo) and castrates them in the process. While it was previously thought that any waterfleas infected by P. ramosa were permanently castrated, it turns out that some lucky Daphnia can actually recover from their infection.

So do these little crustaceans adjust their reproductive output in response to the parasites and is castration a way for them to compensate for a (potentially) temporary hiccup in their baby-making ability? To find out, a team of scientists from Norway set out to see just who benefits the most from host castration. Their logic is that if it is an adaptive strategy by the parasite, then we should see higher spore output from a permanently castrated host. Whereas, if castration is an adaptive coping mechanism by the waterflea, then there should be a jump in reproduction upon the onset of infection as the waterflea tries to make as many baby Daphnia as possible before P. ramosa put a stop to it, then store up reserves during the infection to "wait it out".

To correct for any potential sex differences (there are many documented case of sex-bias in parasitism), these scientists used only female waterfleas for the experiment. During the course of the study, about half the waterfleas they infected with P. ramosa managed to regain their reproductive capacity. In those lucky ones, the parasite produced many fewer spores than in waterfleas that had been permanently castrated. So evidently, P. ramosa benefits from having permanently castrated hosts. But what about the waterfleas themselves? Were they able to compensate by adjusting their reproductive output in the parasite's presence?

The scientists found that by far, the strongest predictor for the lifetime reproductive output of a parasitised waterflea is the age at which it becomes infected - the later that it became infected, the more time it had to churn out babies before it came down with a severe case of P. ramosa. So it's pretty much a case of "use it or lose it". They did not find evidence to suggest the waterfleas made any effort to increase their reproductive output before they are castrated by their parasites. This is unlike other systems where parasite-castration occurs. In trematode-snail systems, the infected snails are less likely to recover from their infection. The strategy which has evolved among snails in areas with high parasite prevalence is to reach sexual maturity as quickly as possible (For example: see this study) so they can eke as many baby snails as they can before they inevitably become infected and be taken over by squirming body snatchers.

It should be noted that the waterfleas used in the experiment were from Southern Finland, whereas the parasites were isolated from a pond in Northern Germany. So perhaps the reproductive strategy of the Daphnia population used in that experiment has evolved in response to their local parasite(s) population instead. Other studies have found waterfleas to be locked in a close evolutionary race with their parasites across space and time, so the outcome of any host-parasite interaction will be dependent on the genetic identity of both host and parasite.

Image credit: Jensen et al./PLoS Biology

Reference:
Magerøy, J.H., Grepperud, E.J. and Jensen, K.H. (2011) Who benefits from reduced reproduction in parasitized hosts? An experimental test using the Pasteuria ramosa-Daphnia magna system. Parasitology 138: 1910-1915