We should conserve general parasite biodiversity, because parasites play important roles in ecosystems. However, we should also do our best to control invasive or emerging parasite species that have large, negative impacts on species and ecosystems. One such parasite is Batrachochytrium dendrobatidis, a fungal parasite that causes chytridiomycosis in amphibians. There is some debate regarding how many amphibian species have been impacted by the global spread of the chytrid fungus. But no matter how you slice it, chytrid fungus has devastated amphibian communities globally, causing many declines and many extinctions. As amphibians disappeared, what happened to ecosystems?

In a recent paper, Zipkin et al. (2020) found that snake communities in Panama shifted after chyrid spread through the amphibian community. Comparing hundreds of transect surveys before and after chytrid invaded, they found that after chytrid invasion, there were fewer snake species and the snake community was more homogenous. Several snake species also had reduced body condition, on average. All of this makes sense, because many tropical snakes eat adult amphibians or amphibian eggs, and thus amphibian declines might have decreased prey availability. As a person who enjoys canned soup and using toilet paper, I feel a strong affinity for these tropical snakes and their pandemic-induced resource shortages.

We often focus on the key results of projects, without taking the time to truly appreciate the methods that yielded these results. So I just want to take a moment to appreciate the hard work and careful analyses in this study by Zipkin et al. (2020). Ecologists rarely have enough data from before parasite invasion to document how ecosystems change from before to after invasion, so the hundreds of before surveys in this project are especially valuable. Zipkin et al. (2020) also dealt with a tricky problem in their analyses; many snake species are very rare and hard to detect. For example, 12 out of 36 snake species that they observed were only observed a single time! Knowing that this uncertainty was important to incorporate, Zipkin et al. (2020) used a great Bayesian analysis to quantify not just how much the snake community changed, but also how confident they could be in their results, given snake rarity. If you want to read all about it, check out their paper, which is available as a PDF on researchgate!      

Reference:

E. F. Zipkin, G. V. DiRenzo, J. M. Ray, S. Rossman, K. R. Lips, Tropical snake diversity collapses after widespread amphibian loss. Science. 367, 814–816 (2020).

Since schools have closed across the country and world, parents and teachers are looking for learning activities that students can do at home. So I’m posting an easy experiment for Grades 3-6 that uses HEXBUGs, popular robot toys, to explore why we’re doing social distancing during the coronavirus pandemic. This activity could be modified for other grade levels. For instance, you could add in more replicates of each “treatment group” (number of robots), and then have students calculate and plot the means of each treatment group. Or you could have them use a line to predict how many contacts would occur for 10 or 20 robots—more than they probably own. Have fun!

ContactRateLab_K-12 <-PDF link

In the past week, my social media feeds – which encompass many people who love bats and support conservation – have been increasingly full of pleas and demands for the media to stop villainizing bats for the 2019-nCov outbreak. I can understand this sentiment; I certainly do not want mobs of people with torches and pitchforks to go out and cull bat colonies to try to protect human health. In fact, even in cases where the transmission of a deadly virus to people is ongoing, like transmission of rabies from vampire bats to people in Peru, killing a bunch of bats doesn’t necessarily reduce human risk; it might even increase it, due to complex disease dynamics! So the sentiment to be careful with how we portray the threats that bat-borne viruses pose for public health in news articles is one that I can support.

HOWEVER, today these social media posts contain a new element: a blog post by a famous bat conservation biologist, Merlin Tuttle, who argues that we have no reason to implicate bats in the 2019-nCov outbreak, and that researchers who are trying to find this virus and other viruses in bats are just in it for the easy research and grant money, because virus spillover from bats to people is very rare and not worth studying:

“…Compared to snakes or other animals, they [bats] are by far the easiest to quickly capture and process, have few defenders, and are already widely feared. Associating bats with rare, little-known viruses provides tempting opportunities for quick publication, big grants, and career advancement¹⁴_.

Nevertheless, history does not support this bias. The great pandemics have come from birds, rodents or primates, not bats¹⁵. In truth, bats have one of our planet’s finest records of living safely with humans^2,14.”

If you have been a long-term follower of this blog, you’ll know that I have never once criticized a paper or focused on the negatives, because I generally find that to be unproductive. But this is not Merlin’s first wildly irresponsible post that pits the general public against researchers by misrepresenting the scientific literature, and I fear that this one could have real negative impacts. So in this space, I want to provide some resources to people interested in bat conservation to learn more about how viral spillover events (like this coronavirus epidemic) and bat conservation are related.

Let’s start with some general information about spillover of viruses from bats. There is no question that bats are reservoirs for many viruses that cause serious human illnesses.  These include viruses like SARS, rabies, and some paramyxoviruses like the Hendra and Nipah viruses.  Because these viruses are such a big deal, there has been a lot of recent attention to bats and their potential as reservoirs for high-impact emerging zoonotic viruses. This work has shown that bat species do seem to be reservoirs for a disproportionate number of viruses, on average, in comparison to species in other taxonomic groups, like rodents. And there might be several reasons why bats have so many viruses but can live with them without being sick. Bats are reservoirs for many coronaviruses and similar viruses (e.g., SARS), so it is highly like that the 2019-nCov has a bat reservoir.

Bats can infect people with these viruses in many different ways. For instance, people can become infected by the rabies virus when they are bitten by a bat or when they contact bodily fluids from bats. People could also become infected by batborne viruses by handling bats or consuming bats, or by consuming things that bats defecated on/in (as in the palm sap and Nipah example). And finally, bats can infect other wildlife or domesticated species, and people can become infected by contacting/consuming those other species. We do not know which transmission route led to spillover from bats to people for this coronavirus, but in general, wildlife markets (for consumption or pet trade) do bring together bats, other wildlife, and people in unnatural ways, and there is a lot of potential for spillover from bats to people in these settings.

Viral spillover from bats is a real threat to global human health and has serious impacts on global economies, so we should be doing everything we can to neutralize those threats. One of the best ways to do that is by advancing global bat conservation. In particular, if we can keep bats in their undisturbed, natural habitats, we can minimize the chances of bat to human transmission. This isn’t as easy as saying, “Stop eating bats!” The global community needs to make a real effort to ensure that in places with high bat diversity (and thus high bat virus diversity), people are empowered to conserve bat habitats and bats because they have enough to eat, don’t need to cut down forests for fuel, etc.

If you have helpful resources for learning more about spillover of viruses from bats and how to use these spillover events as opportunities to advance local and global support for bat conservation, please leave them in the comments!

The February reading group paper was “Extreme Competence: Keystone Hosts of Infections”. If you’ve been following the blog for awhile, you probably know that this is a topic near and dear to my heart; I’ve often mused about superspreaders, superreceivers (here and here), and other types of “super hosts”. In fact, I think about this so often that I’ve started to get a bit bored with wondering why some individuals in a host population or some host species are really good at passing on their parasites. As Martin et al. (2019) point out, the superspreader idea is pretty sexy and superspreaders might be especially conspicuous, so it seems like everyone is looking for them and talking about them. But not me. My new quest is to figure out what makes a host “bad”.

In my hunt for bad boys (most of which cannot be discussed in a public venue), I worked on an idea that wasn’t brought up in the Martin et al. (2019) paper: other symbionts can make hosts super bad for parasites. That’s right, folks. Without a substantial Twitter discussion to guide this post, y’all are being subjected to a story from my dissertation. BRACE YOURSELVES.

On almost every continent on this planet, there are freshwater snails, and it seems like all of those snail species are at least sometimes infested by little ectosymbiotic oligochaete worms, called Chaetogaster limnaei. Chaetogaster are fascinating for several reasons, but their claim to fame in the literature is their diet: they’ll eat anything that fits in their mouths, including trematode parasites. From a snail’s perspective, this is awesome, because they gain at least some protection from being infected by trematode eggs, miracidia, and cercariae. In fact, after an absolutely abhorrent amount of pipetting – which caused by left thumb to grow a muscle as big as an egg – I found that the more Chaetogaster a snail had, the less likely the snail was to get infected by free-swimming trematode larvae. (And because Chaetogaster rapidly asexually reproduce, the more free-swimming trematode larvae a snail is exposed to, the more Chaetogaster it suddenly has, meaning that snails in risky waters get increased parasite defenses!)

Snails with many Chaetogaster are not a good target for trematodes, in the same way that a hotdog stand surrounded by hungry lions isn’t a good target restaurant for buying your lunch. But this probably isn’t particularly inconvenient for trematodes, because just just like most hotdog stands aren’t surrounded by hungry lions, most snails don’t have many Chaetogaster. As I’ve blogged about before, Chaetogaster are aggregately distributed amongst snail hosts, such that most snails have 0 or 1 worms, and just a few snails have many worms. Therefore, just a few snails are what we might call “super bad hosts”.

As Martin et al. (2019) point out, we know that 20% of hosts are typically responsible for 80% of parasite transmission. That 20% contains the superspreaders that we’re all so excited about. But my dissertation work shows something else: ~20% of hosts are “super bad hosts” that might be acting as superdiluters, with Chaetogaster literally sucking up the trematode population. This is interesting because Chaetogaster is just one defensive symbiont species in a world full of hosts covered in symbionts that eat parasites. Defensive symbionts are probably affecting host competence in many, many systems, so these interactions might be a good place to look as we start carefully quantifying variation in host competence within populations.

Finally, since we’re talking about symbiosis today, I’ll leave you with some advice: this year’s March Mammal Madness has an ENTIRE LINEUP of symbioses, including ants + aphids and Bornean bats + pitcher plants. Obviously, one of these will be the 2019 champion. Go fill out your brackets accordingly!

When I first sat down to write this post, I thought that I’d start with a quick definition of the term Neglected Tropical Disease (NTD). I thought I knew what an NTD was – I even study a few! – so I was surprised when a definition didn’t immediately pop into my head. And I wasn’t alone. Several people who read our January Parasite Ecology Reading Group Paper also wondered how we decide which human infectious diseases should be considered NTDs.

If you’re like us, you probably thought about Googling it; surely WHO, CDC, etc. have some sort of NTD definition? They sort of do. But while major health organizations all use generally similar verbiage on their websites and in their reports, none of them seem to have a particularly precise definition. It would be hard to use their definitions to decide whether a given human infectious disease was an NTD or not.

What we seem to have instead of a precise definition is the World Health Organization’s list of 18 NTDs. And what an ecologically interesting list it is! There are viruses, bacteria, protozoa, and helminths. There are parasites with vectorborne transmission, fecal-oral transmission, and environmental transmission. Such diversity! In fact, at first glance, the NTDs seem to have little in common. And at second glance, the list seems oddly short. For instance, this article shared by Valentin Greigert asks why hepatitis E, which kills 70,000 pregnant women a year, doesn’t make the list.

The crux of the issue seems to be deciding who is neglecting NTDs. Is it politicians? Is it researchers? Funding agencies? Drug developers? Rich nations? This is a difficult question to answer, because it requires quantifying how much attention different human infectious diseases are receiving.

To figure out which diseases are or are not neglected by research, Furuse (2018) counted the number of publications (i.e., one metric of research effort) for 52 human infectious diseases, to see if NTDs are studied less than non-NTDs. They found that relative to their disease burdens, only a few NTDs are understudied. The only NTDs that were considered understudied relative to their global burdens were lymphatic filariasis, trichuriasis, ascariasis, onchocerciasis, hookworm disease, and trematodiasis. And, as the above article suggested would be the case, some diseases that are not on the accepted list of 18 NTDs had relatively high burdens and relatively few published studies, like paratyphoid fever. (To see the full list, go check out the paper.)

Over on Twitter, there was some interesting discussion about why some diseases had relatively many or few research papers relative to their burdens. In general, it was hard to guess, and Furuse (2018) notes that the reasons are potentially unique to each disease. And thus our conversation kept circling back to whether and how this burden-adjusted research intensity method could be useful in identifying and controlling NTDs. My personal ponderings have been about which types of research papers could be most indicative of neglect vs. attention. For instance, many NTDs already have effective and relatively cheap control methods that are sufficiently deployed in rich nations but not in poor nations, like water sanitation, so we might not need much research on ways to interrupt transmission for those NTDs. Instead, we might need research on where/when those controllable NTDs exist or the best ways to deploy control operations. And thus only some types of research are highly relevant for any given NTD? Anyways, there is a lot to ponder about this neat analysis. You should give it a read and share your thoughts with us!

In closing, I’ll leave you with this description – not a definition – of NTDs. Maybe one day I’ll be able to amend this post with a precise definition. 

Neglected Tropical Diseases…

…are diseases that affect poor populations that lack basic requirements like clean water, sanitation, education opportunities, and access to affordable healthcare. If you don’t study infectious diseases and you aren’t poor, you probably haven’t heard of more than four of the 18 NTDs in the figure below, despite the fact that they affect billions of people.

…trap people in a disease–poverty cycle. No matter how hard they work or how much economic assistance they receive, populations afflicted by NTDs will remain impoverished without disease control efforts because their disease burdens continue to result in lost economic mobility.

…disproportionally affect tropical and subtropical nations because poverty (i.e., people making less than $1 USD per day) is prevalent in “the global south”. But NTDs aren’t restricted to the the tropics. For instance, it is difficult to estimate NTD burdens, but NTDs are thought to affect thousands to millions of people in the United States.

…tend to be chronic diseases that cause substantial human morbidity, rather than mortality, but several of NTDs do cause substantial mortality, especially in children.

…can often be prevented/controlled/treated using existing, effective, and relatively cheap methods, such as education and water sanitation, but not always. When control methods are lacking, NTDs are often neglected by drug research and development efforts, because it isn’t usually profitable to develop drugs for people who won’t be able to pay for them.

…lack public and political visibility and discourse because they affect people with limited economic and political power, they are associated with stigma/shame, and/or they don’t have high, news-worthy mortality rates like HIV/AIDs, tuberculosis, and malaria.

Figure taken from here:

Yesterday, as I was swabbing an eastern small-footed bat for the first time, I noticed something startling: it’s ears were orange! I was alarmed, because under UV light, orange spots show regions of the bat that are infected by the white-nose syndrome fungus. But when I looked at my nearby colleague, he was not holding the UV flashlight. Confused, but excited, I whispered to him (you always whisper when you’re around hibernating bats), “This bat has orange ears!”

He was totally unphased. Apparently Myotis leibii pretty much always have ectoparasitic mites, which are orange. I’m so intrigued by these mites, but my lit searching has yet to answer my many questions: why do so many M. leibii have them? Do other species not have mites because they rarely cuddle with M. leibii during hibernation? And, most importantly, are the mites parasites, commensals, or mutualists? It might seem safe to assume that the mites are parasites, but these two awesome stories have taught me to be cautious:

(1) Even groups with parasitic origins can contain species that aren’t parasites. The New Zealand bat fly (Mystacinobia zelandica) is a good example of this. You should read this whole fascinating story about the people who discovered that the New Zealand bat fly doesn’t suck bat blood, like related genera in other places, but rather lives in social groups that feed on bat guano (Holloway 1976). M. zelandica only hang out on bats when they’re catching rides to roosts.

(As a side note, one of the people quoted in that article is Ricardo Palma – a retired, Honorary Research Associate at the Museum of New Zealand Te Papa Tongarewa – who has the best automated email response I’ve ever seen:

“I will be happy to deal with your message, but only if it refers to parasitic lice (Phthiraptera) or to ornithological nomenclature.”

I cannot wait until I get to that part of my career.)

(2) Bird mites aren’t parasites. I’ll give you a minute…

…

…

Yeah, I was shocked, too! In what I imagine was incredibly painstaking work, Doña et al. (2018) found that the tiny guts of bird mites didn’t contain bird blood or feathers. Instead, they contained bird uropygial gland oil, fungi, and bacteria; mites are little cleaner symbionts! This probably explains why a large correlational study found that in most bird species, there were positive relationships between mite loads on birds and birds’ body condition. Unlike parasites, mites seem to have a net beneficial effect on their hosts (Galván et al. 2012).

This all reminds me of why I started writing this post in the first place: I wanted to ponder whether we look for relationships between symbionts and host body condition too often or not often enough. The examples that I’ve given so far suggest that we might not quantify how symbionts affect their hosts often enough, because we often assume that all symbionts are parasites until someone comes along and demonstrates otherwise. On the other hand, looking for correlations between symbiont loads and host body condition is probably not a great way to quantify how symbionts affect hosts, especially when the correlations are from a cross-sectional survey at just one time point. These correlational studies might be suboptimal and even misleading for many reasons:

1. Symbiont loads today might not noticeably affect host condition until some point in the future, so time-lagged correlations might be more appropriate.
2. Body condition metrics are alluring – wouldn’t it be great to measure one or two things and know how healthy or evolutionarily fit an animal is? – but studies often find that our favorite body condition metrics predict little to nothing about host fitness.
3. As always, correlation doesn’t imply causation. Instead of symbionts decreasing host body condition, it might be that hosts with low body condition are more likely to acquire parasites or that a shared driver affects both body condition and parasite load.

I also worry that many correlational studies between symbiont loads and host body condition occur as afterthoughts. Now that I’ve switched to study vertebrates, I can relate to this. If you can only catch a few individuals (because they’re rare, or because IACUC said so, or because they’re hard to catch), you want to measure everything that you can about each individual, especially anything that might tell you about that animal’s future health and fitness (things you probably won’t get to measure later). Over the years, you accumulate tons of parasite data this way, even if you weren’t originally interested in parasites, so you decide to analyze it, and maybe publish it if you find that parasites decrease host body condition. Maybe this scenario isn’t as common as I think it is, but there is a publication bias in the literature: we’re less likely to publish positive relationships between symbiont loads and host body condition (Sánchez et al. 2018).

In conclusion, I think that we don’t quantify the effects of symbionts on their hosts often enough, and that when we do, we often do it in a suboptimal way. If we really want to quantify these effects, we should (1) figure out what the symbionts eat (is it the host or something else?), and (2) experimentally manipulate symbiont loads and quantify host fitness (rather than body condition) – otherwise, we should put a lot more caveats in our discussion sections. If you’re interested in more details about parasite loads and host body condition that I didn’t cover here, check out this recent meta-analysis by Sánchez et al. (2018)!

References: 

Doña, J., H. Proctor, D. Serrano, K. P. Johnson, A. O. Oploo, J. C. Huguet‐Tapia, M. S. Ascunce, and R. Jovani. 2018. Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy. Molecular Ecology.

Galván, I., E. Aguilera, F. Atiénzar, E. Barba, G. Blanco, J. L. Cantó, V. Cortés, Ó. Frías, I. Kovács, L. Meléndez, A. P. Møller, J. S. Monrós, P. L. Pap, R. Piculo, J. C. Senar, D. Serrano, J. L. Tella, C. I. Vágási, M. Vögeli, and R. Jovani. 2012. Feather mites (Acari: Astigmata) and body condition of their avian hosts: a large correlative study. Journal of Avian Biology 43:273–279.

Holloway, B. A. 1976. A new bat‐fly family from New Zealand (Diptera: Mystacinobiidae). New Zealand Journal of Zoology 3:279–301.

Sánchez, C. A., D. J. Becker, C. S. Teitelbaum, P. Barriga, L. M. Brown, A. A. Majewska, R. J. Hall, and S. Altizer. 2018. On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. Ecology Letters 21:1869–1884.

Happy Thanksgiving, Everyone! The origins of this holiday aside, I find it worthwhile to spend a day feasting and reflecting on all of the things that I’m thankful for. This year, one of those things is my new postdoc position studying white-nose syndrome (WNS). I’ve blogged about WNS before (e.g., here and here), but I’ve yet to blog about my favorite WNS paper, because it only just came out this week in Nature! I might be a bit biased in my evaluation, but it was certainly worth coming out of my blogging torpor to write about. Give it a read!

Let me tell you about a lovely dream that I share with many other disease ecologists: a new wildlife pathogen emerges; funding to study it becomes immediately available; we rush in and quickly figure out how the pathogen is transmitted by observing how hosts contact other hosts and/or pathogens in the environment; we thus quickly figure out how to interrupt pathogen transmission, our control efforts save an imperiled host species, and the crowd goes wild. Most of that scenario is still just wishful thinking, but today I’ll focus specifically on the difficulties associated with observing and quantifying the contacts that matter for pathogen transmission. There are two scenarios that can turn my lovely dream into a nightmare: the contacts I can observe are not important for transmission and/or the contacts that I cannot observe are important for transmission. Here are some examples: 

(1) The mycoplasma pathogen that causes house finch conjunctivitis seems like it should be transmitted from one bird eyeball to the next when birds physically contact each other. Direct contacts between birds aren’t necessarily easy to observe, but they can be quantified with proximity loggers and similar technology. But those obvious, quantifiable bird–bird contacts don’t really explain mycoplasma transmission dynamics. Instead, transmission seems to occur only when birds visit the same bird feeders subsequently – an infected bird visits, deposits some pathogen, and leaves, and then a susceptible bird visits later and gets exposed. These infected and susceptible birds are “connected” across time in a way that would be completely missed if we didn’t record videos of bird feeders or do feeder RFID experiments.

(2) Mountain brushtail possums spend their days in tree hollow dens and often share their dens with other individuals, especially their pair-bonded mates. Obvious contacts! But contact networks based on den-sharing contacts did a poor job of predicting E. coli strain sharing among possums. Spatial overlap in home ranges (and thus exposure to the same E. coli contaminated environments) wasn’t a great predictor of E. coli strain sharing either. Instead, brief (~4 min), nocturnal, cryptic contacts best explained E. coli transmission.

(3) And finally, we have the new white-nose syndrome example. It’s hard to imagine a more adorable and obvious contact than two bats snuggling for days at time while they hibernate. On average, each cave-hibernating bat in the Midwest is snuggled up with ~2% of the other bats in the cave during visual surveys. But if you cover individual bats in ultraviolet-fluorescent powder and leave them for a few months, you’ll come back to find that during their occasional bouts of arousal, they have actually contacted ~15% of the other bats and much of the cave environment, leaving little puffs of powder in their wakes. And it turns out that those cryptic contacts – the ones that were illuminated by powder trails but not by counting snuggling bats – do a much better job of predicting fungus transmission within and between bat species. For instance, northern long-eared bats were usually seen roosting alone, but the powder revealed a wealth of cryptic connections to individuals of the same and other species. Those cryptic connections likely explain why most northern long-eared bats are infected by the white-nose syndrome fungus by the end of the hibernation season. In contrast, tri-colored bats are rarely seen cuddling and were rarely contaminated by powder from other bats, confirming that they’re the loners of the cave world and explaining why so few tri-colored bats are infected by the end of the hibernation season. Really cool stuff!

These examples illustrate an important point that is easy to forget: if you have gone into the field and quantified a contact network for a host species, you have not necessarily also quantified a transmission network for that host species. To construct transmission networks, you need to know all contact types, and you need to actually quantify transmission.

References:

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.

Blyton, M.D.J., S.C. Banks, R. Peakall, D.B. Lindenmayer, and D.M. Gordon. 2014. Not all types of host contacts are equal when it comes to E. coli transmission. Ecology Letters 17: 970–978

Hoyt, J. R., K. E. Langwig, J. P. White, H. M. Kaarakka, J. A. Redell, A. Kurta, J. E. DePue, et al. In press. Cryptic Connections Illuminate Pathogen Transmission within Community Networks. Nature.