Parasites and host body condition

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.