Parasites in food webs

Food webs are a biological concept taught to students starting early in grade school. On the surface they’re fairly straight-forward; clear and concise introductions to the circle of life. But what about parasites? Have you ever wondered what a food web might look like if you included all of the parasitic worms that affected those animals? Turns out it’s rather tricky, even to say what level of a food web a parasite might fit in, which is one of the most basic pieces of information in the web. So tricky in fact, that scientists that study this sort of thing have only recently begun to include parasites in their models of ecosystems. Here’s a nice quote from a 2008 review article on the subject:

“Think ‘food web’ and the African Savannah may come to mind. Even children recognize that zebras eat grass and lions eat zebras. Less obvious, however, are the 54 or more consumers that eat lions, which include lions themselves, leopards, hyenas and a notable diversity of infectious agents (or parasites): two arthropods, two bacteria, 31 helminths, six protozoans and 10 viruses (Nunn & Altizer 2005).”

So food webs can be very complex. The article then goes on to discuss some of the far-reaching implications of such a web:

“The strong impacts of some infectious agents in food webs have been apparent for over a hundred years. After 1889, the introduced rinderpest virus rapidly reduced the ungulates [hoofed animals] of the African Savannahs to 20% of their original abundance (Sinclair 1979). Without prey, carnivores starved and their populations declined. Freed from grazing, the grass grew tall, which increased the frequency of fire and, in turn, reduced resources for tree-feeding species such giraffes (Sinclair 1979).”

So parasites can affect an ecosystem in surprising ways. The effects get more complicated when you consider that many parasites affect more than host during their life cycles. This can make it very difficult to include a parasite into a food web, and even to classify its trophic level. It’s easy to say that grass is a producer at level 1 of the food web, that a herbivore like a zebra is at level 2, and that a lion is at level 3. But what about a parasite that infects a snail (also level 2) before moving on to infect the lion? It gets its energy from the snail initially, so you might start it at level 3, but the parasite then moves on to get energy from the lion, which would put it at level 4. Now, that’s not uncommon for animal, and food webs can handle these kind of complex links. However, what if the parasite lives in the gut of the lion, feeding on whatever the lion eats? In that situation you might want to say it is a level 3, as technically both it and the lion are feeding on zebra meat. As you can see, it can start to get messy, and there isn’t any rule that works for all parasites. To illustrate that, here’s an example from (Lafferty 2008) of a simple food web with and without a couple of parasites:

pic1

Here, we have a 5 organism food web, with 1 base (B), 2 grazers (G1 and G2), and 2 predators (C1 and C2). The left figure shows the interactions in that web, while the right figure shows what happens if you add in 1 parasite (P), and 1 hyperparasite (HP; a parasite that infects the other parasite). The parasite itself is represented by 3 circles in a box, indicating that it has 3 distinct stages in its life cycle, and the box is ‘L’ shaped because one of those stages is at level 3, and the other 2 are at level 4. The new arrows in the right figure indicate that the adult form of this parasite lives inside animal C1, where it releases eggs. Those eggs move out of C1 and become stage 1 larvae (L1), where they are sometimes eaten by G1 (probably accidentally because they’re present on the grass). If they survive they become stage 2 larvae (L2), at which point they infect animal G2. That animal is sometimes eaten by C1, and if that happens the parasite infects C1 where it becomes an adult and starts releasing eggs all over again.

So that’s the kind of complexity we see on a simple example food web. Here’s what it looks like on a real food web in 3D, where the red balls are the animals and the yellow are various parasites:

pic3

But that’s not all! Not only do the different stages in the life cycle of a parasite all come with their own (large) set of interactions in a web, but those different stages can also have a dramatic impact on an animal beyond just feeding on it. It is not uncommon for a parasite to change the behaviour of its host to suit its own needs. There is a common fluke (a certain kind of parasitic worm) that resides in the brain of a fish in Californian estuaries. To complete its life cycle and start producing eggs, that fluke needs to end up in a bird, which happens if the fish is eaten by a bird. To make sure this happens reliably, the fluke changes the behaviour of the fish drastically enough that it becomes 10-30 times more likely to be eaten by a bird. So not only is the fluke preying on the fish by taking energy, it’s also helping other animals to prey on the fish. Sort of doubling up on the predation. So what trophic level is that fluke? How do we represent its impact on a food web?

Sometimes the modification of the host goes beyond just behaviour; as an example let’s look at the frankly horrific phenomenon of parasitic castration. There is a different kind of rather insidious fluke that infects snails in the same Californian estuaries. Once it gets into the snail, the fluke starts taking over and replacing its reproductive tissue, so that eventually nearly half of the snail’s body actually consists of parasite tissue that does nothing but produce parasite eggs. This zombified snail still acts like a regular snail, except that it no longer cares about reproduction, not spending any time or energy looking for mates. The image below from (Lafferty & Kuris 2009) shows a snail with its shell removed that has been infected with the fluke Himasthia rhigedana. The overall shape is the same as a regular snail, where the reproductive organs would be in the spiralling bit on the left. However in this particular snail, that entire portion of the body has been eaten by the fluke (the entire blotchy red/grey bit) which has grown into the same shape so it fits in the snail’s shell.

pic2

Told you it was horrific. Now you may think this would be unquestionably bad for the snail, but surprisingly enough the infection may actually cause the snail to grow larger and/or to live longer! So this parasite is sort of killing the snail, in the sense that it can no longer produce new snails, yet at the same time helping it to be a better snail, as it now spends more of its time eating and growing, and can still be eaten by predators. How can we include all of this in a food web?

Like I said, tricky. And those are just a few of the reasons that parasites have historically not been included in food webs, especially those taught in schools. Incredibly interesting organisms, with some of the most complex and diverse life cycles that we know of. Aren’t helminths cool?

— Posted by Dave Curran

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