Are superspreaders also superreceivers?

For simplicity, we often assume that all hosts have an equal probability of becoming infected by and transmitting parasites and pathogens. But of course, we know that it isn’t how real systems work. For instance, in real systems, hosts vary in their propensity to become infected by pathogens, and that variation is one probable cause of the parasite ecology “law” that macroparasites are aggregately distributed among hosts. We call hosts that are highly susceptible to a given pathogen “superreceivers,” and hosts that are highly likely to transmit a pathogen are “superspreaders.”

Here’s a question for you to ponder: are superspreaders usually superreceivers and/or are superreceivers usually superspreaders? For instance, sex workers are at high risk for contracting HIV (=superreceivers) because they frequently change sex partners, and they’re also highly likely to spread HIV (=superspreader), if they have it, in comparison to the average person. In that case, the superreceivers are also superspreaders. When that happens, we might predict really explosive epidemics whenever “patient zero” is a superreceiver+superspreader, because R0 will be very, very high.

But consider the Tasmanian devil example that I posted about recently. Tasmanian devils that bite lots of individuals are highly likely to contract Tasmanian devil facial tumor disease; they’re superreceivers. But being bitten by an infected individual doesn’t seem to transmit the infectious cancer to the receiving host, so devils that bite frequently don’t transmit any more frequently than devils that don’t bite frequently. Therefore, the superreceivers in that system aren’t superspreaders.

Now let’s talk about a really cool system that I somehow haven’t blogged about yet. House finches are hosts for an emerging bacterial pathogen (Mycoplasma gallisepticum – Mg) that jumped from poultry into house finches in the 1990s. This pathogen causes conjunctivitis in the house finches – a symptom you don’t often think about in wildlife! In a really neat recent paper, Adelman et al. (2015) showed that birds that spent more time on bird feeders were more likely to become infected by (superreceivers) and transmit (superspreaders) Mg. This is a really cool example of a pathogen that appears to be transmitted by “fomites”: inanimate objects that the pathogen can survive on when off the host.

We probably don’t have enough examples in the literature to determine whether superspreaders are usually superreceivers or to look for generalities in systems where this occurs. But we’re accumulating more examples all the time! Stay tuned.

…if academics were at higher risk of developing conjunctivitis when they sought out free food, I’d have some very squinty-eyed colleagues.



Adelman, J.S., S.C. Moyers, D.R. Farine, and D.M. Hawley. 2015. Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird. Proc Biol Sci. 282(1815): 20151429.

The parasite ecology papers that got away: Part III

Today is the final installment of the parasite ecology papers that got away – back to regular posts next week!

Relationship highs and lows in coral reefs

This year, I blogged about the context dependent nature of symbioses a lot (e.g., here and here). If you’re into that sort of thing, check out these papers about the context dependent nature of coral-fish relationships and coral- zooxanthellae relationships. You’ll also get to see some really cool work regarding partner control; are zooxanthellae coral slaves?

Chase, T.J., M. S. Pratchett, S. P. W. Walker, and M. O. Hoogenboom. Small‑scale environmental variation influences whether coral‑dwelling fish promote or impede coral growth. Oecologia 176:1009–1022.

Cunning, R., N. Vaughan, P. Gillette, T.R. Capol, J.L. Mate, and A.C. Baker. 2015. Dynamic regulation of partner abundance mediates response of reef coral symbioses to environmental change. Ecology 96:1411–1420

Wooldridge, S.A. 2010. Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? BioEssays 32(7): 615-625.

Parasitic castrators

Some parasites sterilize or castrate their hosts. But often this sterilization isn’t 100% effective. Why not? And what does that mean for host-parasite ecology?

Tarnita, C.E., T.M. Palmer, and R.M. Pringle. 2014. Colonisation and competition dynamics can explain incomplete sterilisation parasitism in ant–plant symbioses. Ecology Letters 17: 1290-1298.

Parasites on predators

What happens when predators are infected by parasites? One possibility is that they’ll become lethargic, with totally altered functional responses. Just imagine the ecological implications!

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

The parasite ecology papers that got away: Part II

There are a lot of papers that I wish I could cover on this blog. (My “To Blog” folder currently has 58 awesome papers sitting in it, just waiting to be cartoonified and posted.) Unfortunately, I only have enough time to churn out one blog post per week, and I’d like to spend those 52 posts per year on newly minted papers so that I’m staying up-to-date on the field. So, for a few weeks, I’m going to turn this blog into a dumping ground for the recent parasite ecology papers that I wish I could cover in lots of detail. I’m sure you’ll find something of interest if you look through these gems!

Fishing out marine parasites?

A while back, Wood et al. (2010) published a neat Ecology Letters paper about the potential impacts of fishing on fish parasites. Then last year, Wood et al. (2014) published some survey work showing that parasite distributions in fished and unfished locations are, in fact, different. If you’ve ever wondered how anthropogenic disturbances affect parasites, this is a great place to start looking! (Also, I previously wrote a post about the impacts of fishing on a different, wicked cool marine parasite system.)

Wood, C.L., K.D. Lafferty, and F. Micheli. 2010. Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecology Letters 13: 761-775.

Wood, C.L., S.A. Sandin, B. Zgliczynski, A. Sofia Guerra, and F. Micheli. 2014. Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance. Ecology 95(7): 1929-1946.

Oh, and if you like those papers, you should check out this one!

Wood, C.L., et al. 2015. Productivity and fishing pressure drive variability in fish parasite assemblages of the Line Islands, equatorial Pacific. Ecology 96(5): 1383-1398.

Interesting Open Questions in Disease Ecology and Evolution

I think I’ve blogged about this paper before, but it’s one that is worth revisiting, even if you’ve already read it! Lively et al. (2014) published some “interesting open questions” in disease ecology and evolution that came up at the 2013 Am Nat symposium. My personal favorite – if you’re wondering – is, “What Is the Role of Host Microbiota in Shaping Disease Ecology and Evolution?”

Lively, C.M., J.C. de Roode, M.A. Duffy, A.L. Graham, and B. Koskella. 2014.  Interesting Open Questions in Disease Ecology and Evolution. The American Naturalist 184: S1-S8.

It’s a predator–eat–parasite world

I really, really, reallyreally, really, really like reading about predators that eat parasites. So here’s a paper about that.

Orlofske, S.A., R.C. Jadin, and P.T.J. Johnson. 2015. It’s a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178(2): 537-547.

The parasite ecology papers that got away: Part I

There are a lot of papers that I wish I could cover on this blog. (My “To Blog” folder currently has 58 awesome papers sitting in it, just waiting to be cartoonified and posted.) Unfortunately, I only have enough time to churn out one blog post per week, and I’d like to spend those 52 posts per year on newly minted papers so that I’m staying up-to-date on the field. So, for a few weeks, I’m going to turn this blog into a dumping ground for the recent parasite ecology papers that I wish I could cover in lots of detail. I’m sure you’ll find something of interest if you look through these gems!

Symbiont invasions

I’ve previously covered ant-plant symbioses in several posts (here and here and here) because I think they’re amazing! I mean, trees defended from hungry elephants by armies of teeny ants? That’s just good cinema! But what happens in the sequel when foreign ant armies storm in and take over the native ants’ trees?

Riginos, C., M.A. Karande, D.I. Rubenstein, and T.M. Palmer. 2015. Disruption of a protective ant–plant mutualism by an invasive ant increases elephant damage to savanna trees. Ecology 96(3): 654–661.

The early parasite gets the host

In free-living ecological communities, we know that the first species to show up at a site to start reproducing and changing the habitat is often in a better position to outcompete subsequent species to arrive (=priority effects). Is that true for parasites and/or other symbionts?

Hoverman, J.T., B.J. Hoye, and P.T.J. Johnson. 2013. Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173:1471–1480.

Hosts are all unique, special snowflakes

We’ve talked about why heterogeneity in susceptibility to pathogen infection is important to disease dynamics on this blog before. Did I mention that the same principles apply in human pathogen systems? (Bonus: this is a pretty math paper!)

Camacho, A., et al. 2011. Explaining rapid reinfections in multiplewave influenza outbreaks: Tristan da Cunha 1971 epidemic as a case study. Proc. R. Soc. B 278: 3635–3643.

And heterogeneity in host infection rates leads to aggregated parasite distributions

Relatedly, variation in infection rates should lead to aggregation of parasites among hosts. Check out this really cool experimental study that manipulated heterogeneity in infection risk and observed resulting changes in parasite aggregation.

Johnson, P.T.J., and J.T. Hoverman. 2014. Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. Journal of Animal Ecology 83: 1103–1112.

The coextinction of parasites, commensals, and mutualists – a call for more natural history studies!

By definition, mutualists, commensals, and parasites (hereafter “affiliates” in this post) depend on their hosts for resources or services. Therefore, if a host species goes extinct, the affiliates associated with that host may go extinct, too. And in fact, coextinction events like this should be as common as – or even more common than – extinctions of hosts, because we know that every host species has many mutualists, commensals, and parasites. Just think about the mites living in your eyebrows, the bacteria living in your intestines, and that one time that you had lice in third grade. If humans disappeared, all of those affiliate species might also go extinct!

Of course, you might not believe in the intrinsic value of all species; you might be wondering why you should care if some tiny species that you’ve never heard of goes extinct. Extinctions of mutualistic species – such as the gut microbes that help you digest food and the pollinators that keep our agricultural systems running – have obvious implications for our economy and health. But parasites, too, play important roles in our lives. For instance, they regulate populations of wildlife host species, and they may prevent you from having allergic reactions to things that you shouldn’t be allergic to. And of course, species exist in intricate webs of interactions, and by accidentally (or purposely!) adding or removing species from ecosystems, we have often learned that one species can have huge impacts on ecological communities.

So, coextinctions of affiliates are important, and these coextinctions should be common. That means that we have documented tons of these coextinction events, right? Actually, we haven’t! There are very few examples of documented coextinctions (Dunn 2009, Colwell et al. 2012), and some of those are not entirely open and shut cases. But why?

Say that you document the extinction of a particular host species: Host A. Should every affiliate associated with Host A also go extinct? Because some affiliates likely use multiple host species, some of the affiliates of Host A probably survived on other host species. Also, even an affiliate that historically only used Host A might be able to continue existing if it can switch to a new host species. For instance, maybe Host B, a close relative of Host A, is a suitable alternative host.

Now imagine that you’re trying to document affiliate coextinctions as Host A disappears. What evidence might you use to figure out which affiliates have also disappeared? There might be published accounts of some of the affiliates of Host A, but there are very few host species (if any) for which every affiliate species has been documented. Therefore, the loss of one host species means that several unnamed and undescribed invertebrate species will be lost before ever being documented by humans. Even if you had a perfect list of every affiliate species, it might be really difficult to confirm whether each affiliate was now extinct. That’s because we rarely (if ever) have perfect lists of every host species used by a given affiliate species. So, if one affiliate species frequently uses three host species, but you think it is a specialist on Host A, you might think the affiliate has gone extinct, only to find it happily hanging out on Hosts B and C when you survey those species three decades later.

To summarize, we predict many coextinctions of affiliates to occur as hosts go extinct, but we have hardly documented any such coextinctions. It may be that that affiliate species are much less vulnerable than we expect due to the use of multiple host species or host species switching as a primary host goes extinct, and/or it may be that we are just very poorly equipped to observe and document these coexinctions. Clearly, if we’re going to get better estimates of affiliate coextinction rates, we need more data! Specifically, we need:

  • Better understanding of the natural histories of these systems. We need complete lists of affiliates for each host species, complete lists of host species for each affiliate species, preserved specimens of affiliates for genetic identification, and information on the strengths of the interactions between each affiliate and host species.
  • Better estimates of how frequently affiliates shift host species, and whether jumps to new host species are associated with declines in the availability of the current species. In other words, how often do we expect affiliates to sink with the ship versus swimming to safety? (For further reading about this, see Kiers et al. 2010.)

(It’s been too long since my last pirate worm cartoon….)


Some related reading:

Conservation – save the parasites along with the hosts?

Are pubic lice going extinct?


Colwell, R.K., R.R. Dunn, N.C. Harris, and D.J. Futuyme. 2012. Coextinction and Persistence of Dependent Species in a Changing World. Annual Review of Ecology Evolution and Systematics 43: 183-203.

Dunn, R.R., N.C. Harris, R.K. Colwell, L.P. Koh, and N.S. Sodhi. 2009. The sixth mass coextinction: are most endangered species parasites and mutualists? Proc. R. Soc. B 276: 3037–3045.

Kiers, E.T., T.M. Palmer, A.R. Ives, J.F. Bruno, and J.L. Bronstein. 2010. Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13(12): 1459-1474.

What’s new with the dilution effect?

To say that the dilution effect is a hot topic in disease ecology would be an understatement. For instance, the posts that I wrote in 2013 about the dilution effect debates are some of the most frequently accessed posts on this blog. Since those debates, the dilution effect literature has been pouring in, and I thought I would compile some of the most notable papers (in my opinion) that I haven’t covered yet in one post.

But first: is there still a debate? Or have we all come to an agreement?

I’ve been putting off posts about the dilution effect for some time now, because I find the tone of some of the literature to be tedious. I tried to humorously represent how cutthroat the literature has been with my mortal kombat cartoons in my previous posts, but that might have unintentionally come off as me being antagonistic instead of just being silly. I think the tone has calmed down a little now, but we still have some distance to cover before people agree on what kinds of systems we expect to find the dilution effect in and at what spatial scales we might observe the dilution effect in those systems. But that’s completely understandable, because this is ecology, where the answer to all questions is, “Well, it depends….” :P In the meantime, it has been really neat to see (1) the recent compilations of data and (2) the frameworks that have been proposed to explain where and when we will see a given diversity-disease relationship and/or the relative strengths of mechanisms underpinning the diversity-disease relationships in some systems. For instance:

Civetello, D.J., J. Cohen, H. Fatima, et al. 2014. Biodiversity inhibits parasites: Broad evidence for the dilution effect. PNAS 112(28): 8667–8671.

One of the most talked about recent diversity-disease papers is this meta-analysis by Civetello et al. (2014). Looking across 202 effect sizes and 61 parasite species, they found strong support for a broad-scale, negative relationship between diversity and focal host disease risk. Very surprisingly, the strength of this relationship didn’t vary according to whether the pathogen infected only wildlife or wildlife and humans, whether the pathogen was a micro or macro parasite, whether the pathogen had a simple or complex life cycle, whether the pathogen was a specialist or generalist… or basically any other predictor variable. This is surprising because theory predicts that the diversity-disease relationships that we observe should depend on characteristics of the host-pathogen system, like whether transmission is density or frequency dependent and whether host species are added additively or substitutively to the system. But as Civetello et al. (2014) explain, this broad negative relationship between diversity and disease doesn’t tell us about the mechanisms underpinning that relationship, so we really need to start digging into the mechanisms.

Strauss, A.T., D.J. Civetello, C.E. Caceres, and S.R. Hall. 2015. Success, failure and ambiguity of the dilution effect among competitors. Ecology Letters 18(9): 919-926.

Speaking of mechanisms, Strauss et al. (2015) demonstrate how a really neat framework can give rise to amplification, neutral, and dilution effects. They suggest that by taking into account the focal host’s ability to spread the disease (R0), the competitive ability of the focal host (R*), and the ability of dilutor hosts to vacuum up parasites (encounter dilution), we can determine which diversity-disease outcome should occur. For instance, when focal hosts are strong competitors and the R0 is high, dilutors won’t be able to suppress focal host populations or vacuum up enough parasites to have an effect, so we won’t see a dilution effect. This is cool stuff!

Wood, C.L., K.D. Lafferty, G. Deleo, H.S. Young, P.J. Hudson, and A.M. Kuris. 2014. Does biodiversity protect humans against infectious disease? Ecology 95:817–832.

How often do we expect a negative relationship between host diversity and infection risk for human pathogens, in particular? Wood et al. (2014) considered the ecology/epidemiology of 69 human pathogens and determined whether human infection should increase or decrease with animal diversity based on existing diversity-disease theory. For instance, for pathogens that are directly transmitted among humans and don’t use any wildlife/environment reservoirs, wildlife diversity shouldn’t play a role in pathogen transmission. Wood et al. (2014) concluded that the dilution effect is not expected to occur for the majority of the most important human pathogens, and “there will be winners and losers in environments subject to anthropogenic change.”

Johnson, P.T.J., R.S. Ostfeld, and F. Keesing. In press. Frontiers in research on biodiversity and disease. Ecology Letters.

This paper starts out with an overview of the history of the dilution effect literature, including the dilution effect debates, and some background on how the dilution effect hypothesis fits into existing community ecology theory. Then the authors suggest some future directions for field studies, experiments, and models aimed at understanding the diversity-disease literature.

The future…

Finally, I just want to point out that my experience at ESA 2015 suggests that there is a lot more cool diversity-disease work in the pipeline. If you missed those talks, this is a good place to start perusing.

One Model to Rule Them All?

A common topic on this blog has been how to classify the different types of natural enemies. Where do we draw the line between predators, parasites, micropredators, parasitoids, etc.? What characteristics do we look for to determine which type of enemy we’re looking at? In a previous post, I showed you a classification scheme that used four criteria to divide up the predators, parasites, and parasitoids: (1) “Does the enemy attack more than one victim?” (2) “Does the enemy eliminate victim fitness?” (3) “Does the enemy require the death of the victim?” and (4) “Does the enemy cause intensity-dependent pathology?” In a later post, I talked about a classification scheme that extended this concept from considering only natural enemies to including other types of symbionts, such as mutualists. In that classification scheme, there were only two criteria: (1) the relative duration of the association and (2) the effects of the symbiont (predator, parasite, mutualist, etc.) on the fitness of other partner.

So, how many criteria do we need? To answer this question, we really need a precise way to categorize each type of natural enemy. And nothing gives a precise definition like an elegant mathematical expression! But if you’ve done any mathematical modeling of enemy-victim interactions, you know that there are tons of models out there: multiple predator-prey models, multiple parasite-host models, multiple parasitoid-host models, etc. And it can be tricky to figure out how these models relate to each other.  At least, it used to be tricky! Last week, Lafferty et al. (2015) published a general consumer-resource model that can be simplified to produce any specific enemy-victim model that you want. And they have a neat little program that can do the algebra for you! (At least, Kevin showed that program at ESA 2015. I didn’t see a link to it in the article.)

Now that we can define all of the natural enemy types using a common mathematical model, what criteria do we use to differentiate between the types? The first criterion is whether the enemy can try again if it has a failed attack (“predators”: autotrophs, detrivores, scavengers, predators, social predators, and micropredators) or whether one failed attack results in natural enemy death (“parasites”: parasitoids, parasitic castrators, macroparasites, microparasites, and decomposers. The decomposer thing is blowing my mind.) The second criterion is how many victims each enemy attacks at a given life stage (predators attack many victims, but parasites attack one victim), which is similar to the relative duration of association, and the third criterion is how the enemy affects the victim’s fitness (predators kill their victims, micropredators do not kill their victims). Those second and third criteria are similar to the previous classification scheme used by Lafferty and Kuris (2002), but the first criterion is a new one. And I’m not sure if Lafferty et al. (2015) would argue that we don’t need the intensity-dependent fitness cost criteria, or not. So it looks like we need three or four criteria. Cool stuff!


Lafferty, K.D., G. DeLeo, C.J. Briggs, A.P. Dobson, T. Gross, and A.M. Kuris. 2015. A general consumer-resource population model. Science 349 (6250): 854-857.