Sunday, 9 November 2008

A Conundrum of Parasites

I was asked to do a talk at the BCT Scottish Bat Conference this year about bat parasites. What follows is a simplified version of my presentation...

When Anne Youngman first asked me to do this presentation I put the phone down and found myself looking at the slides, jars and vials, containing hundreds of specimens of bat parasites, which as you can see take pride of place on my desk. I found myself wondering what the collective noun for a group of parasites might be. You get a herd of cattle, a parliament of owls, a murder of crows and even a boogle of weasels: what about parasites?

My first thought, given the reaction of most people to parasites was a yeeuch of parasites. Then I reflected that that doesn't match my own view: I find these strange creatures quite fascinating. Then I considered an omnibus of parasites, given the number of times I have searched in vain for specimens of a particular species, only to have several come along at once. I finally settled on a conundrum of parasites: there are many gaps in our knowledge and unasnwered questions about the parasites hosted by bats, so conundrum seems an appropriate noun.

What I would like to do today is introduce you to just a few of these conundrums or unaswered questions and hopefully show you how we, as active bat-workers, can make a contribution to answering these condundrums.

First though, for the benefit of those who haven't recently looked at page 54 of "The Bat Worker's Manual", which gives an excellent summary, here's a brief overview of British bat parasites, to put what follows into context.

The basic definition of a parasite is an animal (or plant), which lives on another animal and gains nourishment from the host, without benefitting it or killing it. It is also useful to understand the difference between ectoparasites, which live outside the host's body (e.g. fleas and ticks) and endoparasites, which live within the host's body (e.g. tapeworms or helminths). In this talk I will be concentrating on ectoparasites, and specifically those which are large enough to be found by us when handling live bats.

We should also consider host specificity: some parasites are generalists and may parasitise almost any warm-blooded animal. For example the ticks or hravest mites that pester me are as likely to pester my dog or a passing fox or deer. On the other hand, some parasites are highly host specific and will only parasitise a single species or perhaps a genus or small group of hosts which share a roost. Many bat parasites are highly host specific.

Let's briefly consider parasites taxonomy. British bat ectoparasites fall easily into five convenient groups. The arachnids are closely related to spiders and this is reflected in the fact that adults have 8 legs. These comprise the ticks and mites. Insect parasites of bats comprise fleas, bat bugs and bat flies.

Clockwise from top left - Nycteribia kolenatii (bat fly); Ischnopsyllus octactenus (bat flea); Argas vespertilionis (bat tick); Spinturnix myoti (bat mite). Centre: Cimex lectularius (human bed bug).
These pictures show a Blyborough Tick or Argas vespertilionis, one of just two species of tick wheich exclusively parasitise bats in Britain.
The mites are represented by Spinturnix myoti, one of over 50 mite species recorded on bats in the UK. As well as the largest group they are also the most diverse, occupying many different niches around the body. This species lives exclusively on the wing and tail membranes. This is a female, indicated by the rounded abdomen. This species is viviperous and she is gravid: carrying a larva, to which she will soon give birth as a protonymph. Or that would have happened had she not been pickled in alcohol!
As you can see, bat fleas look superficially like the fleas you may find on your cat or dog: dorsally flattened and with huge legs. Eight flea species have been recorded on bat in Britain.

There are two species of bat fly believed to be present in the UK, usually found on Daubentons and Bechsteins Bats. A third species is believed to be extinct. These animals are highly adapted to life on a bat. Although they are flies, their wings are reduced to simple buds.
Finally, I have shown here a picture of a human bed bug to illustrate the very close similiarities between bed bugs and bat bugs.

A fascinating aspect of this subject for me is the lessons that bat parasites can teach us about their hosts. For example, when sampling mites on Natterer's and Daubenton's Bats in autumn I have often noticed a significantly higher parasite load on females and juveniles than on adult males. This presumably reflects the fact that the females and juveniles have been confined together within the maternity roost for a number of weeks, giving the mites the opportunity to reproduce and spread from host to host. The males on the other hand, will have been in smaller groups and able to move between roost sites much more frequently, reducing the opportunity for the parasites to spread.
With the development of Mitochondrial DNA analysis, there will be many more opportunities to use parasites to learn about bats. A good example is a piece of work recently completed in Switzerland, which studied MtDNA in Greater Mouse-eared Bats, a species of mite which parasitises them and another bat species which also hosts the same parasite. Using their data, the researchers were able to demonstrate that the Greater Mouse-eared, whose distribution is restricted to mainland Europe, was previously present in Corsica.

My first conundrum relates to the Spinturnix family of mites: the Spinturncidae. These are the largest mites found on bats and often the most obvious to the naked eye. They are between 0,5 and 1.5mm long and are only found on the win and tail membranes of the bat, making them easy to see. This slide shows a Daubenton's Bat and you can just make out something within the red circle.

When we zoom in we can clearly see a mite on the wing membrane. This is Spinturnix myoti, a species which parasitises Daubenton's, Natterers and Whiskered Bats.

This brief segment of video shows it's close relative Spinturnix acuminatus. I recently removed this specimen from the wing of a Noctule and here we can see it walking across a microscope slide. You can make out the slightly pointed abdomen, in contrast to the rounded abdomen of the gravid female we saw earlier, indicating that this is a male.

In 2003 Anne Baker of the Natural History Museum and Jenny Craven of Leeds University published a paper which brought together a piece of work funded by the british Ecological Society. They set out to gather all the known records of bat mites in Britain and to examine all available specimens. Their paper set out a checklist of species. This slide summarises their results for the Spinturnix family: eight species, each with the main hosts. However, there are two problems.
Spinturnix Species A has yet to be formally named as a species and may turn out to be a variant of Spinturnix acuminatus. A few female specimens were found on Barbastelles and, until more specimens are founf, the status of these mites will remain uncertain.
Closer to home is the question of Spinturnix mystacinus and Spinturnix myoti. S. myoti is found on Daubenton's, Natterer's and Whiskered Bats. S. mystacinus is found only on Whiskered Bats, the difference between the two being very small. It may be the case that it is in fact a synonym of S. myoti. As you migh expect, a problem with resolving this taxonomic issue is the fact that Whiskered Bats are far from common. More specimens of Spinturnix mites from Whiskered Bats could help in clarifying the status of this species.

Conundrum two concerns the geographic distribution of ectoparasite species. To illustrate this I have chosen to use the Blyborough Tick Argas vespertilionis. This slide shows dorsal and ventral views of an adult. The ruler alongside shows millimetre divisions. I have selected this species because it is easily identified: it is almost entirely round and usually looks like a little 5p coin, either lumbering about the roost as an adult or as a larva, attached to a host, lying vertically within the fur.
The other reason for choosing this species is that it is supported by a professional recording scheme: the Tick Recording Scheme, run by the Health Protection Agency. If any bat parasite species is likely to be well recorded, it is this one.

The main chart here shows the existing distribution records in Scotland: just four records, some of them quite old. Does this indicate that this species is scarce? Or that it is declining, or limited in range to the west?
Probably not: if you look at the inset map, I have added records based on specimens I have found or which have been sent to me over the past two years. As you can see, this has trebled the number of records in Scotland for this species. Bearing in mind that this is probably the best recorded bat parasite species (possibly excluding the fleas, which have a very dedicated national recorder), you can see the problem with distribution data!

Conundrum 3 relates to the so-called Chigger Mites or Trombiculidae. This picture shows the larav of a member of this family. You can make out the mouth-parts to the left, sourrounded by the legs: only six of them as this is a larva. The remainder of it looks pretty much like a little orange jelly-baby.

This slide shows them attached to a host: in this case a Soprano Pipistrelle, with four larvae attached to her ear. They remain attached whilst taking a blood-feed, which provides what they need to metamorphose. After a few days they leave the host and as nymphs and adults they predate on smaller arthropods within the bat roost.
I have seen these larve on Soprano and Common Pipistrelles, Natterer's Bats and Daubenton's Bats. (at this point I asked for a show of hands and over half the audience had also seen Trombiculidae larvae on bats). From that we can see that this is far from an unusual feature.
When Baker and Craven completed their study of British bat mite records in 2003 they had found only four records of Tromiculidae, one of which is questionable. Why should this be? As with the Blyborough Tick, may be partly about a lack of recording effort, but there is another problem with Trombiculidae: identification. There is in fact a published key to thes family. So surely it's just a matter of working through the key until you arrive at the species? The problem is that the key runs to five volumes and the volume which refers to the species found on British bats is 1,100 pages long! So identification of these mites is a real labour of love.

The final conundrum concerns bat bugs. This amazing picture was sent to me recently by Paul Hope and shows a Noctule with two bat bugs attached to it's forearm. My question is: are they Cimex pipistrelli or Cimex dissimilis? There is a long-standing uncertainty about whether both these species are present in the UK or not, fuelled by the fact that the differences are tiny and the taxonomy is the subject of some uncertainty. A DNA study in the Czech Republic aims to resolve these issues and specimens of bat bugs, especially from Pipistrelles, are sought to assist in this.

One of the joys of working with parasites is the occasional opportunity to gross people out. I notice I wasn't scheduled last before lunch, probably for very good reasons...
This slide shows the business end of Cimex pipistrelli. It's a ventral view of the head and I've labelled the forelegs and antenna, to help you get your bearnings. You can just make out the stylet, the organ the bug uses to feed, lying flat against the underside of the head, within it's protective sheath.

This slide shows how the bug uses it's stylet to go about feeding. You'll notice I have coloured the host a fetching pink, to reflect the fact that human bed bugs feed in exactly the same way!
First, the bug pushes it's stylet through the skin of the host...

This is where it gets interesting. The stylet is both flexible and prehensile and it commences probing around the flesh...

...until it finds a capillary and commences feeding. The probing and cutting through the flesh creates a contusion and slight swelling which is occasionally visible on the wing of bat. You may also find it on your own body if your choice of last-minute bargain holiday doesn't wuite work out as you had hoped!

I hope you have found this talk interesting and that one or two of you may still feel like eating your lunch. Hopefully I have also shown what an opportunity there is for us, as active bat workers to make a very real difference to the sum of human knowledge in this area. The four conundrums I have described barely scratch the surface: the simple fact is that any and all parasite records are useful.

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