Confluaria podicipina

Most of the time, being infected with parasites is costly to the host in some way. But sometimes there might be circumstance when the presence of parasites might be a good thing. For brine shrimps (known to most as "sea monkeys"), it seems like tapeworm larvae might be a worthwhile accessory - admittedly one that turns you bright red and make you more likely to be eaten by a bird.

Photo of infected (red) and uninfected (transparent) brine shrimps
From Fig 1 of the paper

The study being featured today were based on a population of brine shrimps living at salt marshes in southwestern Spain which are infected by nine different species of tapeworm larvae. The most common species are Flamingolepis liguloides (which have previously been featured on this blog here) and Confluaria podicipina. At the site where the scientists conducted this study, about two-thirds of the brine shrimps were infected with either F. liguloides or C. podicipina, and about a third of them are unlucky enough to be simultaneous infected by both species (alongside a bunch of other less common species).

All these parasites are using the shrimps as a temporary vehicle for getting into final host where they can mature into adult worms, and for that to happen, the shrimp needs to be eaten by a bird. However, in the environment that these shrimps dwell in, tapeworms like C. podicipina can convey some unexpected benefits. It seems that shrimps infected with tapeworms are more resistant towards arsenic.

Previously, we have featured a study on how tapeworms can act as a sink for heavy metal in seabirds soaking up the toxin before they get absorbed into the host's tissue. But that study was on adult tapeworms living in the gut of a bird host. Though they are also tapeworms, the physiological interaction between an adult tapeworm in the gut of a vertebrate host is very different to that of a larval tapeworm residing inside a small arthropod.

Flamigolepis liguloides cysticerocoid (larger one on the left) and Confluaria podicipina cysticercoid (indicated by arrows)
From Fig 2 of the paper

In this case, the tapeworm larvae increased the level of various fatty substances - C. podicipina increases triglyceride level, while F. liguloides increase the amount of lipid in the host. Together, these fatty droplets help soak up any arsenic in the brine shrimp. Additionally, the tapeworms also help the shrimp sequester carotenoid which enhances the shrimp's capacity to produce antioxidant enzymes which mops up harmful free radicals, and help the shrimp deal with the presence of arsenic in their bodies.

Whereas F. liguloides seems to be present in high numbers all the time, C. podicipina only appear in April. This might be related to the seasonal movement of their final host - which are flamingos in the case of F. liguloides, but for C. podicipina, the final hosts are grebes, which only visit the lake during certain time of year. Indeed, that was the finding of a previous study which has been featured on this blog.

Additionally, it seems that the brine shrimps are better at handling arsenic in May when they are mostly only infected with F. liguloides. So why is that the case? Well, it could be that (1) C. podicipina is not as good at helping their host deal with arsenic, (2) it is harmful to the host in other ways that offset their detoxification effects, and (3) it only appears during the warmer months when the brine shrimp's overall resistance to arsenic is lower anyway, so it simply coincided with their appearance.

Of course, neither F. liguloides and C. podicipina are doing this as some kind of favour to the host - C. podicipina and its fellow tapeworm larvae are doing this for their own benefit. They are manipulating host physiology to make the host a more suitable shelter and vehicle for reaching the final host - increasing the fat content of the host makes it a cosier site for development, and increasing the carotenoid level makes the shrimp bright red and stand out more to the bird host. But it just so happens that all these changes also have a side effect of benefiting the shrimp, even if temporarily, before they end up between the beaks of a bird

Reference:
Sánchez, M. I., Pons, I., Martínez-Haro, M., Taggart, M. A., Lenormand, T., & Green, A. J. (2016). When Parasites are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps. PLOS Pathogen 12(3): e1005459.

Trichobilharzia szidati

If you have ever gone for a swim in a lake and later found your arms and legs covered in red itchy welts resembling mosquito bites, it is quite likely that you have encounter parasites related to the one being featured today. Trichobilharzia szidati is an avian blood fluke, and it has relatives living all over the world in both freshwater and marine environments. While they usually infect waterbirds like duck, they are not very good at telling birds apart from humans. To them, any warm-blooded terrestrial vertebrate animal is fair game, which is rather unfortunate for both humans and flukes alike - more so for them than us. As a result of this encounter, we end up covered in intensely itchy spots, but getting under the skin of a human means immediate death for such flukes.

Cercaria of Trichobilharzia regenti, a species related to T. szidati
Scale bar = 200 μm. Photo from this paper

So why is that the case? Blood flukes are masterful molecular mimics - they are able to disguise themselves with proteins that resembles the host's own molecules, allowing them to stealthily sneak pass the host's immune system. But Trichobilharzia szidati and similar avian blood flukes have evolved to bypass the immune system of birds, and when it encounters a mammalian immune systems like ours - all bets are off. Our immune system takes immediate action against this intruder with extreme prejudice, which results in an inflammatory reaction that manifest itself as "duck itch" or "swimmer's itch".

But aside from getting inside the circulatory systems of ducks or giving us a nasty itch, it seems that trematode larvae like those of T.szidati are also making a contribution to the environment which usually get overlooked.

As a part of their lifecycle, parasitic flukes turn snails into parasite factories - churning out a continuous stream of free-swimming parasite larvae called cercariae, which in the case of T. szidati is the stage that infects birds and cause us temporary grief. But most of these cercariae don't actually end up infecting a bird or getting (and dying) under the skin of an unsuspecting human swimmer. The majority of them end up entering the food web as food for a range of other animals. To aquatic insects and fish, the swimming parasite larvae is simply another tasty morsel. Alternatively, the cercariae simply use up their limited energy reserves and expire, becoming food for all manner of scavengers and detritivores. So how much food is being provided by these tiny parasite larvae?

In the study being featured today, scientists collected some T. szidati-infected snails from a fish pond in Czech Republic and made daily observations on the amount of cercariae they were pumping into the environment. The noticed that most cercariae came streaming out upon first light in the morning, in order to coincide with the daily routine of the bird host, then dwindled as the day went by. But throughout the day, it adds to to hundreds and thousands of larvae.

When they conducted the first set of observations in April, they found that on average infected snails were releasing about 1000 cercariae per day, with a maximum of over 4500. However, when they made another series of observation again in September, the average daily output was ten times that of the snails they studied in April, with a maximum output of almost 30000 cercariae per snail per day. It is worth noting that while they made four sets of observations for the April sample, only one set was conducted during September, which means the sample could have be skewed by an unusual sample. Additionally, the snails in the September sample were larger than those from April, and larger hosts are usually able to produce more parasite larvae. But these are the kind of seasonal and individual variations which would have exist in the natural environment anyway.

Since each infect snails are releasing thousands of cercariae per day, though they are microscopic, those contributions really adds up. Based on the numbers they obtained from the study, the research estimated that over its lifetime, an infected snail produce as much as its own body mass (or more) in the form of T. szidati larvae. Therefore, in a large fish pond with a relatively low infection prevalence such as 5%, the infected snails would be contributing about a 500 kilograms of biomass per year in the form of T. szidati cercariae. But in some location where almost half the snails are infected at any given period, the yearly output of all these snails can add to to 4.65 tons of parasite larvae, which weighs as much as an Asian elephant.

Trichobilharzia szidati and other avian blood flukes do not exist in isolation - the snails they infect can also host an entire communities of other flukes species, some of which have been recorded to churn out even more cercariae than T. szidati. When you put them together, they provide quite a substantial food source for all the aquatic organisms that they share the environment with. These parasitic flukes are the unseen elephant(s) in the pond.

Reference:
Soldánová, M., Selbach, C., & Sures, B. (2016). The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis. PloS One 11: e0149678.