National Geographic

Parasites outweigh top predators and castrators do best of all

To a science-fiction filmmaker, the concept of being controlled by unseen forces is creative gold, but for the rest of us, it’s a fairly unsettling prospect. But like it or not, it’s clear that parasites – creatures that live off (and often control) the bodies of others – are an integral part of the world we live in and carry an influence that far exceeds their small size.

Now, a painstaking survey of the residents of river estuaries shows that parasites do indeed punch above their weight, and they aren’t slouches in that department either. Despite their tiny size, their combined mass eclipsed that of the top predators in the area and their influence extended wider still. It’s a parasite’s world and we’re just living in it.

Over five years, Armand Kuris and Ryan Hechinger from the University of California, Santa Barbara led an exhaustive census of life in three Californian estuaries. At 69 different sites, they assessed almost 200 species of free-living animals, from high-flying birds to burrowing shrimps, as well as the 138 species of parasites hitching a lifestyle on their bodies.

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Using a wonderfully old-school combo of nets, binoculars, meshes, sieves and scales, the team collected samples of the estuaries’ inhabitants and dissected over 17,000 individual animals. Their bodies were dissected and their parasites removed, classified and weighed.

Massive flukes

Snails, crabs and bivalves (hinged shellfish) made up the bulk of the local fauna but every single animal group living in the estuaries was infected with parasites of some description. On average, these freeloaders made up about 2% of the weight of their hosts. That may not seem like much, but it’s about ten times more than previous estimates; it was always assumed that parasites, being very small, would weigh next-to-nothing despite their weighty influence. Now, we know that isn’t true.

Tapeworms and parasitic crustaceans were very common, but lording over all of them were the trematodes or flukes. This group of parasitic worms alone weighed as much as the local fish and outweighed the birds – the local top predators – by three to nine times. Pound for pound, the estuaries were home to more parasite tissue than bird tissue.

Kuris and Hechinger also found that some parasites use particularly successful strategies. The dominant group castrated their hosts by infecting and shutting down their reproductive systems. Castrators are the ultimate body-snatchers for their neutered hosts have zero chance of passing their genes down to the next generation. In effect, their usurped bodies become living shells for the parasites’ own genes – a superb example of Richard Dawkin’s “extended phenotypes“.

Of the many strategies used by local parasites, this was the most successful, so much so that the combined weight of castrated bivalves, snails, shrimps and crabs was almost the equal of their fertile peers. Remember that these were the most common animal groups around, and take a second to reflect on that sobering statistic. It means that a massive proportion of the flesh in the estuaries is under parasite control.

Ex-snails

Take the California horn snail, Cerithidea californica. It’s the most abundant single species in area that Kuris and Hechinger studied and it’s infected by 18 species of trematode. Almost all of the largest snails were castrated and on average, 22% of an infected snail’s body was made up of parasites. The snails had been converted into trematode factories. In the pictures above, you can see that the snail’s orange testes (left) have become corrupted by trematodes (right).  

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Every day, the infected snails released a swarm of cercariae – a part of the trematode’s life cycle that swims with a tadpole-like tail. Each of these lives for just a day, but the snails discharge so many into the water that the combined weight of the cercariae alone also dwarfs the mass of local birds by three to ten times. The snail’s tale illustrates that parasites have influence far beyond their already considerable weight. They may have the substantial combined mass of larger animals, but because they don’t need to move or forage, they also enjoy the high productivity typically enjoyed by microscopic organisms.

Kuris and Hechinger admit that they only looked at one specific ecosystem, but they believe that their estimates will apply elsewhere and that they are, if anything, too conservative.  If they are right, no consideration of food webs or ecology would be complete without taking the power of the local parasites into account.  

Reference: Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., Dobson, A.P., Dunham, E.J., Fredensborg, B.L., Huspeni, T.C., Lorda, J., Mababa, L., Mancini, F.T., Mora, A.B., Pickering, M., Talhouk, N.L., Torchin, M.E., Lafferty, K.D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454(7203), 515-518. DOI: 10.1038/nature06970

Photos by Todd Huspeni and Kevin Lafferty

There are 20 Comments. Add Yours.

  1. drb
    July 25, 2008

    Can you clarify regarding the advantage to the parasite of neutering the host? In the short term, the advantage is apparent. However, if the host cannot reproduce, it would seem that the long term survival strategy of the castrators must be compromised as well. Or am I missing something?

  2. Carl Zimmer
    July 25, 2008

    These parasites aren’t passed down from parent to offspring. They move from snails to fish and birds, where they lay eggs that can infect more snails. So there’s no long-term benefit to sparing your host’s sex life.

  3. Wilson
    July 25, 2008

    It’s a parasite’s world and we’re just living in it.

    Funny, I thought we humans were the biggest ones of all!

  4. Jon D
    July 25, 2008

    This post had great timing!
    I just finished reading Carl Zimmer’s Parasite Rex about 2 weeks ago. Thoroughly enjoyed it by the way! It was deeply disturbing to learn how extensively parasites influence nature!
    Now that influence is looking even greater. There’s just no escaping them. Indeed, when they form such a large chunk of the animal and plant kingdoms (in numbers and now in weight), you have to start thinking that without them and the strategies and mechanisms plants and animals have had to evolve to combat them, we possibly wouldnt have such wonderful diversity!

  5. Ed Yong
    July 25, 2008

    *Everyone* should go and read Parasite Rex. It has a pride of place on my shelf of favourite science books. Also, for the parasitophiles out there, I’m pretty keen on parasite research both here and on the old WordPress site.

  6. HolfordWatch
    July 25, 2008

    The 1st photograph is so beautiful – it gives me a fresh appreciation for Dale Chihuly’s ocean forms.
    Parasites are horribly fascinating and Zimmer’s book is excellent. I’m interested by the way in which expts. with hookworms and whippleworms keep popping up as a way to investigate damping the more severe forms of asthma or Crohn’s Disease.

  7. subramanyam.a
    July 25, 2008

    It is sad thing(truth)to accept. But parasites really rule the world. I have ordered a copy of Parasite Rex. Curious(afraid also) to know more about them.

  8. Ian Tindale
    July 26, 2008

    If parasites not only occupy their hosts, but also to a certain extent actually control them, I think it’s worth proposing a question:
    Do we know of any parasites that themselves are subject to other parasites, that in turn control them also? And so on.

  9. Ed Yong
    July 26, 2008

    Ooh, good question Ian, and the answer is yes. A very large number of wasps lay their eggs in the bodies of other animals, which are then eaten alive by the grubs. These species are called ‘parasitoids’ but a subgroup of them are ‘hyperparasitoids’ – they lay their eggs on the eggs/larvae of other parasitoids. As far as I’m aware, this can extend to three layers – wasps parasitising parasites, which parastise other parasites, which parasitise a poor, hapless host.
    It’s all very meta.

  10. Ian Tindale
    July 26, 2008

    One thing that has bothered me all day about this. We, as humans, in civilised 2008, tend to think of this in a fairly polarised manner, along the lines of ‘those parasitic bastards are evil, why don’t they leave the poor hosts alone, I wouldn’t like to be controlled by wasp larvae or fungi, so I’m sure those poor buggers don’t either”. All in all, an empathic response which probably concludes in drawing a line down some branch of the taxonomy of life and sweeping a chunk of it into the ‘evil’ end of the workbench. It might involve thinking about ‘rights’ that a living being might be assumed to have. It might also conclude in thinking how lucky we are that our minds aren’t controlled by an external agent. (?)
    But hang on, from a purely economics point of view, the hosts have created or are presenting an opportunity. What else is variety to do but to eventually exploit it? In terms of computer security, if you develop a system and leave a hole open that becomes exploited eventually by mischievous hackers, whose fault is that? The next version improves upon this vulnerability, of course, and the cat and mouse game goes on.
    So parasites aren’t evil really, they’re exploiting an opportunity that’s been handed to them on a plate. This has further implications. It could imply that the desired, the designed, the evolved, the final form of any particular life form at its present state in nature has an ‘ideal’ that more or less corresponds to it’s genetic blueprint. But parasites take this raw material further, utilising to produce a modified version, a custom job, overclocking and adding blue LEDs and extra fans and speed stripes and chrome.
    Does this mean that the original organism has had its intent violated? Does this get us into the territory where we have to define intent in the first place? Parasites touch our nerve because we have an imbalanced tendency to wish everything in our enlightenment age was steeped in equality. Therefore we applaud at ‘symbiotic’ relationships, thinking what good fellows they are, and on the other hand, we frown on ‘parasitic’ relationships because they seem to hint at slavery or serfdom or other forms of exploitation that involve lack of freedom.

  11. Jon D
    July 27, 2008

    QUOTE: It might also conclude in thinking how lucky we are that our minds aren’t controlled by an external agent. (?)
    Toxoplasma gondii, a parasite carried by cats infects somewhere between 30-80% of the world’s population. It infects the brains of mammals, and its effect on rats makes them less afraid of cats, which obviously makes them easier to eat and thus pass the parasite on.
    Although more research on humans is needed, the effects suggested thus far are various changes in personality and delayed reaction times.
    The rest of your comment was very interesting – There is often a fine line between symbiotic and parasitic relationships – I’m obviously talking here about parasites that dont kill their hosts. eg would you call the bacteria living in your guts parasites or symbiotes? On its own, I expect bacteria would generally be a parasite, and of course some introduced strains can kill you. But the microbes in our guts break down carbohydrates and make some of the vitamins and amino acids our bodies need. (Microcosm – another really good Carl Zimmer book!!)

  12. Ed Yong
    July 27, 2008

    I’ve blogged about Toxoplasma affecting human culture before.

    As Jon pointed out, there is certainly a fine line between symbiosis and parasitism, and just last month, two papers came out that illustrated this nicely. I actually planned to do a two-part post on this recently, but failed to due to lack of time. So consider this a mini-write-up.

    The first concerns corals and the symbiotic algae that provide them with energy through photosynthesis. It’s a classic example of symbiosis. One group of algae called Symbiodium had 8 different genetically distinct groups and there’s new evidence that one of these (A) is actually a parasite. Corals that carry the A algae tend to have poor health and the algae provide them with less carbon than the more common C type.

    The second paper showed that a parasitic mite could actually be more of a symbiont. The mites suck the blood of a parasitoid wasp, but they also defend it from other hyperparasitoids (see my previous comment). The mites attack the hyperparasitoid larva and the more of them they are, the greater their chances of killing it. This benefit is so great that the host wasps have apparently evolved small structures on their backs to house the mites, even though they lose blood in the process.

    So we have a symbiote that’s actually a parasite and a parasite that’s actually beneficial in the grand scheme of things. It’s definitely ludicrous to label parasites as evil, and I personally think they are quite beautiful (despite the reflexive wincing they can induce).

  13. Jon D
    July 27, 2008

    QUOTE: I’ve blogged about Toxoplasma affecting human culture before.
    I actually read that post last year when I first heard about Toxoplasma, before before I started reading your blog regularly here!
    Parasites are very cool! Botfly larvae give me nightmares though

  14. subramanyam.a
    July 28, 2008

    these parasites are not passed on from parents to offspring. ok. But if the parasites take an upperhand and
    infect all snails and castrate them,where will the parasites find new hosts?. One more doubt. I read that some
    parasite infected fish easily offer themselves to birds. The birds actually take these fishes, because they can find them easily and save precious energy, even though they have to rear and pass on these parasites. Is this another kind of symbiosis?.

  15. Ian Tindale
    July 28, 2008

    Is all of this really nothing more than highly sophisticated tool use by the parasite? The parasitic fungi is deploying an insect as a tool that will relocate it – it’s now not a moth, but a vehicle.
    But does the host (and this we’ll probably never know) still “think” in an ‘acceptable’ and functional manner? Does the host know that it is under such control, and does it realise that the reason it does certain things is not because it decided to but because another agent wanted it to (or was evolved to want it to). I mean, it obviously must know something’s amiss, but it might not attribute the behavioural outcomes to the physical effects.
    It might be possible that they live a perfectly functional (but not normal and probably not optimally comfortable) life, where they understand everything they do to be their own impulses and stimuli (assuming we can extrapolate that they might ‘understand’ their own experiential world model in any depth at all. Probably – they can’t be that stupid, they’ve been around since before the dinosaurs, and after).
    The more I think about it, the more I think there’s a network-topology style intersection of disciplines waiting to produce innovative research, here:
    Bring together this area of parasites and “controlled host behaviour that achieves an end”.
    Match up with those studying behavioural deviancy in human cultures, where discussions of what makes a person a ‘bad’ person or criminal or insane often traverse a continuum with ‘environmental’ at one end and ‘hereditary’ at the other.
    It’d be interesting (frightening? disempowering? enlightening?) to discover, for example, that much antisocial behavioural aberration in individuals was really not our fault after all. The weevil made me do it.

  16. Richard
    July 29, 2008

    Could you explain the “extended phenotypes” in this context? I can understand a gene affecting behaviour to encourage a parasite if this affects your competition or predators more than you. But emasculating the host seems so obviously detrimental to the host’s DNA that I’d have assumed there’d be a massive evolutionary advantage to developing ways of stopping or slowing parasite infection.
    Or have I just misunderstood and you’re referring to “extended phenotypes” purely from the point of view of the parasite. So disabling the host’s reproduction isn’t a primary aim of the parasite, just a side effect- it’s evolved because it makes the host even more efficient as a factory?
    The sort of parasitic load you’re talking about for these snails seems to large I’d have assumed that it would seriously affect their competitiveness, both within and intra species. Even if evolving increased immunity is too tricky I’d intuitively expect tactics like shorter life spans (reducing competition with your offspring when you can’t reproduce). What’s the point in continuing to live when all you can do is poo you’re own killer?
    Though I guess the parasite might try to extend your life, but now we’re getting a bit too complicated…

  17. Ian Tindale
    July 30, 2008

    Or, it could be as it is in humans, where it is often said that men think of sex every x minutes (depending where you read it). The ‘thinking of sex’ might be a primary driver in most species, and removal of the presence of this controller may leave a free slot into which to insert a foreign control mechanism. This may lead to the question of whether the sex drive is a ‘high level’ driver or ‘primal’, as is often assumed. Religious beliefs frequently assign human sex drives to the ‘animal’ parts of our make up. Maybe it might turn out that sex drive is in fact a high-level, if not top-level control construct, and that all mating animals are driven by it. Take away this libido and you have a fully developed machine or tool that you can re-purpose to your own ends. Not taking it away may result in your control mechanism having to fight with the powerful libido all the time. Who knows. Just a minute, I’ve got to think about sex again – back in a while.

  18. Ed Yong
    July 30, 2008

    Subramanyam – It’s unlikely that the relationship between the parasites and the snails would ever become so extreme that the parasites make themselves extinct. If they infect too many snails, there will be fewer hosts around and the parasite population should fall. As this happens, the snails should recover allowing for another boom in parasites and so on. That and the fact that some snails will probably be better than others at fending off parasites – after all, only half of them were infected. The thing with the birds isn’t a symbiosis because the parasites don’t do the birds any favours once they’re actually in their bodies.
    Ian – I think you’re jumping the gun in assuming that the snails have self-awareness. That’s actually a surprisingly complex mental trait and one that few animals have. Have a look at this Wikipedia entry for a short primer and some links.
    Richard – The *snail* is the *parasite’s* extended phenotype. Because the snail can’t reproduce, it’s evolutionarily irrelevant. To the parasite, the snail is the equivalent of a dam to a beaver or an anthill to an ant or a skyscraper to a human.

  19. Jon D
    July 31, 2008

    This discussion is getting quite long! very interesting one too.
    To address why the snail populations dont drop to dangerously low levels, I remember reading in Parasite Rex that one of the strategies snails use to combat parasites is switching between sexual and asexual reproduction, depending on whether there are a lot of parasites around at the time.
    When they reproduce asexually, genetic variation is low since there are only a limited number of strains of snail, so parasites are able to evolve ways of getting around the snails’ immune systems quickly.
    When there are lots of parasites around, sexual reproduction allows for more genetic diversity, so its difficult for parasites that specialize in specific strains to invade the population.

  20. Nathan Myers
    August 14, 2008

    I cannot help but post this link, given the context.
    http://www.partiallyclips.com/index.php?id=1165

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