"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

October 23, 2016

Alaria spp.

Today we are featuring a guest post by Dr Emily Uhrig, a postdoctoral research fellow currently at Linköping University, Sweden. She has written a post on a study that she and her colleagues conducted on a parasite that congregate in the tail of garter snakes, and the role that these reptiles play in the life cycle of this parasite.

Parasites are found in a tremendous range of hosts spanning the animal kingdom and beyond. However, the consequences of parasites for their hosts have not been thoroughly studied in many cases and this is particularly true for parasites infecting snakes. Even in very common snakes, such as the garter snake which is widespread throughout North America and has been studied extensively with regard to many aspects of their biology, their parasites have received little attention.

Histological cross-section of an infected snake's tail
(m = mesocercariae, v = vertebra)
During my PhD research, I aimed to shed light on snake parasites by focusing on the red-sided garter snake of Manitoba, Canada, and I was especially interested in a trematode of the genus Alaria. Interestingly, Alaria infections in snakes have been noted in the literature for years, but mostly in ecological surveys of parasite communities, and their possible effects on the snakes’ evolutionary fitness were unclear.

Alaria spp. have complex life cycles consisting of a snail host in which Alaria eggs multiplies into asexual stages called sporocysts, which then produce multiple clonal larvae called cercariae. These cercariae emerge from the snail and infect frogs. Within the frog, Alaria develop into mesocercariae, a non-reproductive ‘resting’ stage. A mammalian carnivore, usually a canid (e.g., coyote) or mustelid (e.g., mink), serves as the final host in which the parasite reaches sexual maturity. So where does the snake fit in?

It turns out, the garter snake is a paratenic host, also known as a transport or reservoir host, which ends up accumulating Alaria mesocercariae through eating frogs. Paratenic hosts are not physiologically necessary for the parasite’s development as a part of its life cycle, but they help bridge ecological gaps between hosts. In this instance, the snake, which has quite a penchant for frogs, helps Alaria move from a (mostly) aquatic intermediate host to its terrestrial final host. Interestingly, Alaria spp. can infect many species paratenically - including humans; however, since relatively few humans fall prey to carnivores, Alaria that end up in humans are usually at a dead end.
Tail morphologies observed in red-sided garter snakes. Arrows mark the position of the cloaca.
Photos modified from Figure 1 of the paper.
Once inside the snake, the life of Alaria gets even more interesting. In the field, we commonly observe snakes to have ‘puffy’ tails where the end of the tail is obviously swollen and often discoloured. These puffy tails are fragile and can rupture with the gentlest handling or even by the snake’s own movement along the ground. The ruptured tail oozes a pink-coloured fluid which, on close inspection with the naked eye, clearly contains moving organisms, and microscopic examination reveals multitudes of writhing Alaria mesocercariae. Thus, the parasites apparently make a rather impressive migration through the tissues from the snake’s gut to its tail.

Left: Ruptured tail with ‘ooze’ containing Alaria; Right: Alaria mesocercaria from Figure 2 of the paper.

It is not uncommon for a snake’s tail to harbor several thousand mesocercariae, and the record holder in our studies had over 6000 mesocercariae in its tail. Alaria infections seem to be ubiquitous in our study populations as all snakes examined have been infected to some degree. Parasite mesocercariae are nearly impossible to visually identify to species level because different species are very similar in morphology. Thus, we used genetic analyses to determine that the snakes in our study population are often co-infected with at least three different Alaria species (primarily A. mustelae and A. marcianae, but also another as yet unidentified species).

Having identified the infection, the next obvious question to ask was, what are these parasites doing inside the snake’s tail? To answer this, we collected tails from recently dead snakes and prepared them for histology. Examining those samples, revealed that, in severe infections, the tail essentially becomes a bag of parasites and the tail musculature is destroyed (similar to what another parasite – Curtuteria australis – does to the foot of a New Zealand clam), likely through compressive effects of so many parasites in a relatively small space. The mesocercariae tend to be surrounded by pockets of mucous, the accumulation of which leads to the swollen puffy tails. The source of the mucous (host or parasite) is not entirely clear, but we believe it is the host’s body attempting to ‘wall-off’ the infection. Interestingly, some highly infected snakes do not have puffy tails, which suggests there may be variation in host tolerance of the infection.

As parasites destroy the tail musculature, the connection of the tail to the rest of the body is weakened and the likelihood of tail loss is increased. Loss of the tail is probably beneficial to the parasite because it could help facilitate transfer to the definitive host. In an attempt to catch a fleeing snake, a predator may come away with only the tail, especially if the tail is fragile, so aggregating there could prove a useful strategy for Alaria transmission. As we often observe wild snakes that are missing portions of their tails (stub tails), it may be common for predators to end up snacking on only a tail.

Unlike lizards, snakes cannot regrow their tails so tail loss is permanent, and also costly. Previous work found that males with stub tails have compromised reproductive ability. During the garter snake’s mating season, as many as 100 males compete for a single female. In these “mating balls”, males use their tails to wrestle with one another for access to the female. Males with stub tails are less successful competitors and much less likely to obtain a mating.

For females, tail loss also has reproductive implications because males appear to rely on female tail length to align properly with her cloaca during mating. When attempting to mate with a stub-tailed female, males can misjudge the location of her cloaca, reducing the changes of a successful copulation. Thus, through mechanical impairment, Alaria infections can have a direct effect on the fitness of both male and female snakes.

The association of Alaria and garter snakes was first mentioned in the literature nearly a century ago, but has received little attention until very recently. Thus, one need not visit exotic locations to learn new things about host-parasite associations as there is still much to learn about the consequences of parasites even in common species.

Uhrig, E. J., Spagnoli, S. T., Tkach, V. V., Kent, M. L., & Mason, R. T. (2015). Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy. Parasitology Research 114: 4451-4461.

This post was written by Dr Emily Uhrig.

October 6, 2016

Peltogaster sp.

Most people are familiar with how barnacles look like - sedentary creatures which filter the surrounding water for food while being stuck attached to rocks or other hard surfaces. Parasitic barnacles on the other hand looks nothing like those creatures. In fact, they don't look anything like what most people would expect an animal to look like. The most well-know example of a parasitic barnacle is Sacculina carcini, but that infamous species is only one of an entire order of such body-snatching parasites that infect crustaceans like crabs and crayfish.

Left: Peltogaster externa attached to their hermit crab host.  
Right: The externa (orange) and interna (green) of Peltogaster in its hermit crab host
Photos from Fig. 1 and Fig. 2 of the paper
These parasitic barnacles belong to a group call Rhizocephala and the body of the adult parasite can broadly be divided into two parts: The "externa" which is the bulbous reproductive organ that sticks out of the host's abdomen, and the "interna" which is found inside their host's body. The interna is a network of root-like tendrils which wrap themselves around the host's organs (hence the name "Rhizocephala" which roughly translates into "root-head").

Most depiction of rhizocephalans have those parasitic roots running throughout the entire body of the host - this is based on an illustration of S. carncini drawn by the famous artist and biologist Ernst Haeckel. Haeckel's original drawing has been copied by many others since it was first published in the book Kunstformen der Natur, and has been treated as the definitive depiction of the rhizocephalan interna. But the thing is, Haeckel has never actual seen a Sacculina in person - he simply based his illustration upon descriptions of the parasite in a monography published in 1884. So while Haeckel's original drawing is iconic and has been replicated countless time in many books, that depiction of these parasitic barnacle is not entirely accurate. Much like tropes in other areas of scientific illustration (such as depictions of extinct animals), Haeckel's depiction of Sacculina has been faithfully and unquestioningly used and copied ever since.

It is understandable that not much is known about the true three-dimensional structure of the rhizocephalan interna - because of its complex and delicate nature, it would really difficult to tease apart all those roots which are tightly intertwined with host tissue to get an accurate picture of the parasite's extensive root network. But now there is technology available which can resolve this question. In the study featured in this post, a group of researchers used X-ray microtomography to obtain a 3D image of these parasites' root network inside their hosts. They performed this procedure on five species of rhizocephalan barnacles collected from the coast of Norway and the United States; four of the species were hermit crab parasites belonging to the genus Peltogaster, and one - Briarosaccus tennellus - was from the hairy crab.

From the microCT scans, they found that the barnacle's "roots" are not spread evenly throughout the body, but were wrapped around certain organs, with most concentrated near the hepatopancreas  - an organ found in crustaceans which is also known as the digestive gland, which would be prime place to suck up nutrients. And in contrast to Haeckel oft-cited and copied drawing, none of the roots actually penetrate into the muscles. While the roots of the four Peltogaster species were mostly wrapped around the hepatopancreas, the roots of Briarosaccus also extended to the host's brain and central nervous system, which may explain how some of these parasites can manipulate the behaviour of their crustacean host.

Parasite can often manipulate their host's behaviour and physiology to an amazing degree. While many of those interactions are very complex, with the use of techniques such as micro CT, we can begin to unravel the intricacies of how these body-snatchers interact with and manipulate their hosts.

Noever, C., Keiler, J., & Glenner, H. (2016). First 3D reconstruction of the rhizocephalan root system using MicroCT. Journal of Sea Research 113:51-57

September 22, 2016

Plectocarpon lichenum

Lichens can be found all over the world, even in the most barren and inhospitable environments (even near active volcanoes). They grow on exposed surface like moss, but they are very different to those plants. Lichens are the outcome of a highly successful conglomerate resulting from the fusion of a pair of very different lineages of fungi combined with a photosynthetic alga. Together they form a beneficial tripartite that has allowed lichen to colonise environments all over the globe

Photo of parasitised lichen from Fig 2. of this paper
However, lichen are also involved in other forms of symbiosis which are more deleterious - to the lichen anyway. There are parasitic fungi call lichenicolous fungi that have evolved to parasitised lichens. There are about 1500 known species of such fungi and they vary in their specificity and their harmfulness, and some of them form galls on their host. In addition to such parasites, lichen also has to contend with a range of animals that feed on them, including (but not limited to) reindeerscaterpillars, and snails.

Since lichens are constantly being attacked from multiple fronts, some species have evolved various forms of chemical defences that make themselves less appetising to animals that try to eat them. But no counter-measures ever survive intact in evolution's battlefield, and lichen-infecting fungi like Plectocarpon lichenum can mess with their host's attempt at avoiding being eaten.

The scientists in this study looked at how these parasitic fungi affect their lichen host, specifically how tasty they might be to other animals. Plectocarpon lichenum infects a species of lichen call Lobaria pulmonaria. Generally, snails prefer eating those parasitised lichens over unparasitised lichens, but they avoid eating the parasitic galls themselves (see the photo above where the snail has neatly grazed the lichen around the parasitic galls).

So on top of already drawing nutrient away from its host, this parasitic fungus also make the lichen more delicious to the lichen's predators - a double whammy. Now this isn't like other cases featured on this blog where the parasite alters the host to make it more edible because it would help get the parasite transmitted. It doesn't benefit P. lichenum to have the snail munching on its host, but this is simply a side effect (a tasty one for the snail) of the infection. But how is how is P. lichenum causing this?

The scientists measured the level of carbon and nitrogen in both parasitised and unparasitised lichen, and found those with the parasitic galls had lower concentration of carbon. In addition to altering the nutritional content of L. pulmonaria, parasitised lichen also had lower level of defensive chemicals. So is this reduction in defensive chemicals the reason why the snails preferred parasitised lichen? While it seems to make intuitive sense, that turned out not to be the case. When they remove the influence of those defensive compounds in both parasitised and unparasitised lichen by rinsing them with acetone, the snails still preferred the parasitised lichen.

So lichen-infecting fungi makes their lichen host more tasty to snails - but that's not the full story. When they investigated a related host-parasite pairing - in this case Lobaria scrobiculata infected by Plectocarpon scrobiculatae, they found that the presence of L. scrobiculata did not make any difference to their palatability to snails

Despite being in the same genus, these two parasitic fungi affected their lichen host differently. In any case, the effects that P. lichenum have on its lichen host was what the scientists had predicted, but not for the reasons they had thought. This shows that ecological interactions are often messy and complicated, and the dynamics found in one particular relationship or species may not be applicable to another - even if they are closely related.

Asplund, J., Gauslaa, Y., & Merinero, S. (2016). The role of fungal parasites in tri‐trophic interactions involving lichens and lichen‐feeding snails. New Phytologist 211: 1352–1357

September 8, 2016

Tylodelphys sp.

There are many examples in nature where parasites are able to alter their host's behaviour in some way. More recently, some scientists have been investigating just how the parasite are altering or controlling host behaviour. Most of them had looked at the chemicals secreted by the parasites to lull the host into compliance, but the study we're featuring today looked at something different - how the behaviour of the parasite itself can affect the behaviour of the host.

Left: Histology section of an infected bully's eye from Fig. 1. of the paper (r = retina, l = lens, m = metacercariae [flukes])
Right: Tylodelphys in the eye of a common bully from this video

The star of today's post is Tylodelphys - a parasitic fluke which infects a small freshwater fish in New Zealand call the common bully. In order for this parasite to complete its life cycle, Tylodelphys must enter the gut of a fish-eating bird, which would naturally involve the unfortunate fish being eaten by the said bird. While it is in the common bully, Tylodelphys dwells in its host's eyes in the vitreous liquid between the lens and the retina (see video here).

Unlike other species of flukes which turn into dormant cysts at a similar stage of development, Tylodelphys stays active and free to roam around inside the fish's eye - which provides it with plenty of opportunity to get up to all kinds of parasitic hi-jinx. When Tylodelphys larvae are crawling around inside a fish's eye and happen to get in between the retina and the lens, this can partially blind the fish and prevent it from being able to notice incoming predators such as birds.

To examine what Tylodelphys gets up to during the day, researchers at the Otago Parasitology Lab collected some common bullies and gave them eye examinations using an opthalmoscope (yes, like the one used for your eye exam). Using the opthalmoscope, they captured a series of short videos of the infected fish's eyes at different time of day, and watched what eye flukes got up to. They also performed histology to examine if the flukes are damaging the fish's eyes.

The bullies they examined varied in how heavily infested their eyes were - this range from just having a single fluke in the eye, or it can be up to seventeen flukes, with the average being about seven. Living in a crowded eye is not good for the parasites either, as the researchers found that flukes from heavily infected fish are comparatively smaller. But despite being found in a vital and sensitive part of the host body, Tylodelphys was otherwise a relatively benign tenant - they didn't mess up any eye tissue.

Compare this with other species of eye flukes which can cause cataracts in the eye of their fish host, Tylodelphys seems rather well behaved. However, that does not mean Tylodelphys isn't bad news for the bully - just that its modus operandi is more subtle. Instead of impairing the fish's sight by damaging the eye, as mentioned the above, when the flukes position themselves in front of the retina, they act like internal blinkers. Surprisingly, fish that are more heavily infected didn't have their retina more covered up by the flukes than less heavily infected fish, which means it's not simply the sheer number of flukes that blinds the fish - it's something else the flukes are doing.

Tylodelphys  has a daily routine and shifts its position in the eye throughout the day. During day time, the flukes sit between the lens and the retina, blocking the host's line of sight. But at night, they settle down to the bottom of the eye, allowing the fish to see properly again. But if Tylodelphys is trying to get its host eaten by a predator, why doesn't it just stay in front of the retina all the time? That is probably because not all predators are the same for Tylodelphys.

During the day, the main predators of bullies are fish-eating birds (which are Tylodelphys' final host), whereas at night, the main predators are longfin eels (which are not suitable as host), so it'll be good for to the fluke if their host fish can still see and avoid the incoming predators at night. So the flukes keep this fish's eyes covered during the day, but move aside to not get in the way at night, and this seems to follow a circadian rhythm.

While this helps the fluke reach its final bird host, the reason why this behaviour manifests probably has nothing to do with trying to change the host's behaviour. As mentioned above, unlike other flukes that become a dormant cyst at this stage of development, Tylodelphys keeps growing so it needs to feed - and the only thing around to eat in the eye of a fish is the fluid in the eye's vitreous body. The partial blinding of the fish host during daytime might simply be a side-effect of the parasite's feeding routine.

So while the fluke moves around in the fish's eye to get its daily dose of eye jelly, this also produce a useful side-effect by making the host more vulnerable to fish-eating birds. Such "useful side-effects" could be how many parasite host manipulation tactics have evolved. Indeed, that is often how evolution often work; co-opting preexisting features and behaviours into new roles. To understand how a parasite affect the behaviour of its host, sometimes perhaps it is best to start with studying the behaviour of the parasite itself.

Stumbo, A.D., and R. Poulin. 2016. Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143: 1261-1267

August 26, 2016

Trypanosoma tungara

This is the fourth and final posts in a series of posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2016. This particular post was written by Sierra Weston and it is about how male Tungara frog end up receiving a parasitic present while trying to call out to female frogs.(see also the previous post about picky bat flies, monkey-infesting botflies, and the caring maternal side of a parasitoid wasp).

Like many species of frogs, during breeding season the males of the túngara frog produce a mating call to attract female frogs. But instead of just serenading his own species, the male frog may inadvertently be announcing his location to nearby frog-biting midges.

TFW you're trying to serenade the ladies and end up with a face full of 
blood-sucking midges. Photo from Fig. 1 of this paper
All adult frogs are at the mercy of a range of opportunistic and specialised insects, some of which are potential vectors for all kinds of blood parasite. There is a species of frog-biting midge (Corethrella spp.) which preys predominantly on the túngara frog (Engystomops pustulosus) - a species of small frog found in the region between the south of Mexico to northern South America. The female midge takes advantage of the male frog’s mating call during their breeding season as a host detection system. The midge follows the sound, finds the frog and voila, it gets a blood meal. A male can attract up to 511 midges in half an hour. Unfortunately, again for the poor frog, midges are the perfect vector for a wide variety of diseases and parasites including trypanosomes.

Trypanosomes are single-celled protozoan parasites that infects hosts from all vertebrate classes; birds, mammals, reptiles, fish and amphibians. Some of these protozoans can cause diseases, including sleeping sickness (Trypanosoma brucei gambiense), in humans, as well as making their hosts more susceptible to sickness. Although frog trypanosomes are a less studied group, there are some parasite-vector-host relationships that have been documented.

The study featured in this post investigated trypanosome infection in túngara frogs. The aim of the study was both to determine that trypanosomes affected the túngara frog and identify the species of parasite if present, and whether there is a difference in trypanosome prevalence between male and female frogs. Since it is the males that produce the mating call, it was predicted that any midge transmitted trypanosomes would only occur in male frogs.

The researchers confirmed the presence of trypanosomes in the blood of the frogs, but also observed that the parasites possessed a some unique characteristics that set them apart from previously described species. However, frog trypanosomes are also known to be able to significantly change their shape when infecting different hosts. This presents the possibility that the trypanosomes infecting the túngara frogs could be a previously identified species with a slightly altered form which make them more suited to life as a parasite in the túngara frog.

Through further analysis and DNA sequencing, researchers were able to confirmed the discovery of a new species of trypanosome: Trypanosoma tungara. In terms of prevalence in male and female hosts, results showed a much greater percentage of males infected with trypanosomes showing that the mating call results in the male frog being the ‘easiest’ and most predominant target for the frog-biting, trypanosome vectoring midges. There were also female frogs infected with trypanosomes, which was surprising because female frogs do not vocalise. A potential transmission path is presumed to be the close proximity of the frogs when they are in amplexus, (the mating ‘embrace’) which allows the midge to move directly from the male to the female frog.

X.E. Bernal, C. M. Pinto (2015) Sexual differences in prevalence of a new species of trypanosome infecting túngara frogs. Internations Journal for Parasitology: Parasites and Wildlife 5: 40-47

This post was written by Sierra Weston.

That wraps it up for ZOOL329 class of 2016 - I would like to thank all the students for their posts! Next month, it's back to writing my usual posts about newly published parasite-related papers which you might not have noticed, and/or papers that were not as widely covered by the press - so stay tuned for more!

August 19, 2016

Sclerodermus harmandi

This is the third post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2016. This particular post was written by Jarrod Mesken the more maternal side of a parasitoid wasp (see also the previous post about picky bat flies and monkey-infesting botflies).

When most people think of parasite behaviour, horrific tales of behavioural and physiological manipulation are what come to mind. This is not without cause; many parasites are definitely scary to think about. However, many pursuers of the parasitic lifestyle also display behaviour that would be thought of as normal, perhaps even charming in an anthropomorphic kind of way. An example of this is seen in the parasitoid wasp Sclerodermus harmandi, in the form of maternal care.

Photo of multiple female Sclerodermus harmandi engaging in brood care from Figure 1 of this paper

This stories begins when the female wasp finds a suitable host for her eggs. She injects the host with paralysing venom, and cleans an area of the body to lay eggs on. Once laid, she routinely inspects the eggs with her antennae and mouthparts. If an egg is found to have detached from the host, she would gently reattach it. Maternal behaviour continues when the eggs hatch, when the larvae must be fed. To do so, the mother wasp bites a hole in the host, which is still alive at this point and injected with paralysing venom periodically to prevent it from moving. The hole fills with haemolymph, the insect equivalent of blood, which is consumed by the larvae.

During this stage the mother S. harmandi also moves the larvae around to prevent them from overlapping each other as they grow. If a larva dies, the mother moves the body far from the other larvae to prevent their habitat becoming unsanitary. Even during the cocoon stage the mother continues to rub the offspring, despite them being encased. Eventually, the males of the clutch hatch out as adults. These few males (there is considerable female bias in the ratio of this species) chew holes in the female wasps’ cocoons to assist them in emerging, after which they mate with them. While it has negative affects in many taxa, this kind of inbreeding is less likely to have negative effects in hymenopteran insects, where haploid males act as a purge of deleterious alleles.

So why does S. harmandi provide such comprehensive maternal care? Because it increases the likelihood of offspring surviving. Experiments in which the wasp mothers were removed at varying stages of offspring development showed that not only were offspring that received maternal care more likely to survive to adulthood, but that this was proportional to how much maternal care they received. Experiments also showed that when a mother was taken away and replaced with another female who has previously laid eggs, the ‘stepmother’ will exhibit the same behaviour as the mother would, with the same rise in offspring survival.

Why the stepmother expend her own energy to raise another wasp’s offspring is just as interesting; it is because of the high levels of inbreeding in the population. Since most of the reproduction in this species is done through inbreeding, there isn’t much genetic variation going around. This means that there is a good chance of two wasps being related, so the stepmother may increase the chance of her genes being passed on by raising another wasp’s offspring. Female S. harmandi that haven’t laid eggs yet do not exhibit this behaviour, preferring to leave the offspring alone; this would indicate that the maternal behaviour is initiated by laying eggs.

So for a parasitoid wasp, it turns out that the females of S. harmandi make for very responsible parents or stepparents. That is, if you consider letting your children live on the body of something you paralysed, feeding off its blood until they grow up, and then mate with each other to be “responsible”.

Hu, Z., Zhao, X., Li, Y., Liu, X., & Zhang, Q. (2012). Maternal care in the parasitoid Sclerodermus harmandi (Hymenoptera: Bethylidae). PloS One 7: e51246.

This post was written by Jarrod Mesken

August 12, 2016

Alouattamyia baeri

This is the second post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2016. This particular post was written by Gabrielle Keaton and it is about a nasty botfly that lives in the neck of howler monkeys (you can read the previous post about picky bat flies that live on bats here).

Photo of botfly pores on howler monkey neck from Plate 1 of this paper
You know how itchy a mosquito bite can be - you scratch it then a lump forms. Imagine that lump forming but not going away. Instead, it grows and grows inside of you until finally a black grub plops out of a hole in your neck onto the ground. Well that’s what it’s like for the howler monkeys of Panama!

This nasty parasite in this case is the larvae of Alouattamyia baeri, a botfly that lives on free-ranging howler monkeys (Alouatta palliate). In a study conducted over seven years from 1987 to 1993, researcher Dr Katherine Milton investigated a variety of factors relating to this parasite's life cycle including its infection prevalence and intensity. She found that 60% of the howler monkeys on Barro Colorado Island (BCI) were infected by this botfly.

Alouattamyia baeri are large (18 to 20mm in length) black flies. The adult fly sounds and look like neotropical bees. When flies that were collected from the howler populations on BCI were reared in captivity, it was found that female flies produced an average 1400 eggs each, laid in discrete rows. These eggs required the appropriate stimuli (carbon dioxide and heat) to hatch into parasitic larvae that then invade their host through the nose and mouth where it migrates to the neck and opens a up larval pore. The larva reside in the howler’s neck for approximately 6 weeks, passing through 3 instars (developmental stages). After this, the larva drops out of the monkey's neck warble and burrows into the soil where it finishes the last developmental stage underground.  The study found that the entire life cycle takes approximately 13 weeks.

Dr Milton discovered that most of larval growth (86%) occurs during the 3rd instar when its food consumption increase by about 20%. This means the larva was trying to extract the most resources at the last possible moment of its stay, so if it ends up killing the host, it wouldn't matter to them because they are out of there.

Infestations were the highest during the wetter seasons and these periods also strongly correlated with peaks in the monkey’s mortality. Monkeys carrying the botfly larvae lack subcutaneous fat reserves. As if having a 2.4 centimetre long and 1.5 centimetre wide maggot in your neck wasn’t bad enough, even after the botfly has made its exit, the hole they made in their host remains open for several days. That’s pretty like much waving a neon ‘vacancy’ sign in front of the primary screw worm fly (Cochliomyia hominivorax) - an even nastier parasite that lays its eggs in open flesh wounds. When the screwfly larvae hatch, they feast on anything and everything surrounding that wound. Some monkey cadavers were even found with hands eaten down to the bone from these nasty little maggot and at least half of the C. hominivorax infestations found on howler monkeys were the result of prior A. baeri infections

Now, I’m sure you might have a bit of a panic next time you feel a little raised bump hanging around your neck, but remember - even if it is a botfly, at least you know it will be gone in 6 weeks' time.

Milton, K. (1996), Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. Journal of Zoology 239: 39–63.

This post was written by Gabrielle Keaton

August 5, 2016

Trichobius sp.

Those who have been reading this blog for a while will know that August is student guest post month! All this month this blog will be featuring posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class. One of the assessment I set for the students is for them to summarise a paper that they have read, and write it in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2016. To kick things off, here's a post by Melissa Chenery about some picky bat flies.
Photo of Trichobius johnsonae from Figure 2 of this paper

The public often view bats as repulsive, disease-carrying animals and are subsequently disliked. “Argh! They’re repulsive!” is just one of the many lines I have heard from people walking by while I observed a local colony. But do you know what is even more horrifying than a bat? A bat fly! These ectoparasites belong to two families of flies know as Streblidae and Nycteribiidae. But these hematophagous (blood-feeding) parasites don’t always fly like the name suggests - most species actually have no wings at all, and some look more like spiders than flies.

Disgusting, right? But not to worry, these external parasites have evolved to feed exclusively on bats. The bat flies are quite specific towards their hosts and tend to stay on a particular bat host. They are even picky about where they live on the host, whether on the bat’s fur or hiding within folded wing membranes. Occasionally they can be found in the fur and these individuals possessed comb-like structures (called ctenidia) for attaching to fur. It is assumed that long-legged species move quickly to avoid being scratched by the bat during grooming, whereas the short-legged species hide within the membrane folds to avoid getting licked. Bats use grooming as a behavioural defence against bat flies and other external parasites, and bats with a high number of flies groom more often than those with only a few. For the parasites, action can result in their removal and often their death.

In a study which took place in Belize, Central America, a team of researchers demonstrated just how host-specific the bat flies can be. They examined over thirty two species of bat flies, and in the twenty species for which they were able to collect more than five individuals, they found that eighteen of those species showed strong site preferences. The majority of the bat flies were constrained to a single host-species, and amazingly, bat flies with functional wings (which would allow them to be more mobile) weren't any more or less picky than those without. The study also found that only two species (Trichobius yunkeri and Trichobius dugesioides) weren’t too fussy in respect to host-site preference.

For bat flies that were the dominant species of their respective hosts, six out of those seven species were fur-specific, suggesting that in most cases, bat flies are highly host site-specific. They also discovered an interesting correlation between leg length and host-site preference. Bat flies with longer legs are able to push up over the surface of the fur, and are more likely to be found dwelling in fur. Conversely, short-legged individuals moved much more slowly and were mostly membrane-dwelling.

The team also conducted a study where three bats were restrained and three left unrestrained, with six bat flies placed on each. All unrestrained bats had only one bat fly remaining after five days, whereas all bat flies remained on the restrained bats. This suggests that the elimination of the flies is due to grooming behaviour. This may also be the cause of host-site specificity in bat flies, although further studies are needed Despite their nightmarish appearance, bat flies can still be very fussy eaters, and they have adaptations which allows them to specialise on particular bat species and host-sites.

Hofstede, H., Fenton, M., & Whitaker. J. (2004). Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on neotropical bats (Chiroptera). Canadian Journal of Zoology 82: 616-626.

This post was written by Melissa Chenery

July 29, 2016

Gordionus kimberleyae

We have featured hairworms (Nematomorpha) quite a few times before on this blog, but for those who are new to them, they are parasitic body snatchers of insects and other terrestrial arthropods. The hairworm larvae are parasitic and must develop inside an arthropod host, but the adult worm is free-living and has to enter a water body in order to reproduce. To achieve that end, once they reach maturity, they make their host seek out a body of water and jump in, at which point the adult worm make their exit. This can look quite dramatic / horrifying to onlookers as the length of a fully grown hairworm can be several times longer than the host itself.

Specimens of Gordionus kimberlyae emerging from beetles, from Figure 2 of this paper
Hairworms are found all over the world, and the study we are featuring today shows that they can thrive even at the Arctic Circle, in the most northern parts of Canada. Despite the harsh conditions there, Arctic Canada is home to over 2000 species of terrestrial arthropods, including many species of beetles - some of which are host to parasitic hairworms.

In this study, a team of researchers sampled insects from twelve different locations in northern parts of Canada, and at five of those locations, they found seven species of beetles which are host to hairworms. All the hairworms they found belonged to a single species - a newly discovered one that has never been described before. They named it Gordionus kimberleyae, and these parasites happened to be most common in beetles on Banks Island in the Canadian Arctic Archipelago.

At Banks Island, 13.4% of the beetles that the research team collected were found with G. kimberleyae emerging from them. Most of the hairworms were found in beetles that were hanging around near water, and it's possible that those infected beetles weren't there by accident - as mentioned above, hairworms are known to modify their host's behaviour so that they would seek out water when the parasite is ready to exit their host. Most beetles were only infected with a single worm, which is bad enough considering how big they are and what they do to the host, but there were a few beetles that had two or even three inside them.

So how do these parasite manage to survive in the frigid cold of Arctic Canada? While adult hairworms don't do particular well in cold conditions, they are very short lived and die shortly after they reproduce anyway during the warmer months. However, the larvae have adaptations for surviving in freezing conditions.

In addition to the seven species found in this study, it's not clear how many other ground beetles that G. kimberleyae infects. The ground beetles which these hairworms infect are carnivorous insects, which means they probably acquire their hairworms from eating flying insects that have aquatic larval stage (such as mosquitoes) which can become host to these parasites' larvae. The beetles occupy an important part of the food web as the link between tiny invertebrates and larger insect-eating animals. But the hairworms may also be keeping their population in check.

Additionally, by causing their host to jump in the water, they are transferring where nutrients are flowing in the environment. While these beetles would usually be eaten by land-dwelling animals, by dunking their host in water, the hairworms may also be feeding a range of aquatic animals that depend on their hairworm's "donation" of dying insects into their realm. Despite their gruesome methods, parasites also play important roles in many ecosystems.

Ernst, C. M., Hanelt, B., & Buddle, C. M. (2016). Parasitism of ground beetles (Coleoptera: Carabidae) by a new species of hairworm (Nematomorpha: Gordiida) in Arctic Canada. Journal of Parasitology 102: 327-335

July 10, 2016

Cuscata campestris

One of the key characteristic of plants is their ability to produce food using sunlight via the process of photosynthesis. But there are many plants that do not photosynthesise - holoparasitic plants obtain all the nutrient they need from their host. One of the most well-known group of holoparasites are the dodders. There plants have no roots, their leaves have been reduced to tiny scales, and are composed entirely of elongated tendril-like vines. Because of their appearance and what they do to the host, the dodder has also acquired many common names including "Angel Hair", "Witch's Hair" and "Devil's Hair". When the dodder latches on to an appropriate host, it extends structure call haustoria which penetrate into the host plant's tissue to suck out its nutrients. This has led to the dodder also being called "vampire plants".
Dodder seedling in the process of coiling around its host (image from Fig. 1. of this paper)
There are 200 known Cuscuta species and of those, a small handful of them (10-15 species) are considered as serious agricultural weeds. These parasitic plants wrap their vines around their hosts and literally suck the life out of them. Infestation of this plant have been known to cause massive losses in alfalfa, tomatoes, carrots, and cranberry crops, and these "vampire plants" are very difficult to get rid off; since dodder vines often completely smother their hosts, it requires a lot of manual and mechanical labour to remove them. Additionally, dodders can also produce large numbers of resilient seeds that can linger in the soil for a long time, waiting for the next year to erupt in another outbreak.

For dodders, as with most other organism, the first moments of its life are the most critical - the newly germinated dodder seedling must secure a grip on a host plant within two to three weeks of germinating, otherwise the seedling would use up its energy reserves and expire. From the moment they germinate, these parasitic plants have various ways of finding their host. Dodder vines are able to "sniff out" host plants through the chemical they give off (essentially plant BO), but they can also use other senses to find their host. A newly germinated dodder seedling can also detect the specific wavelength of light which are reflected off the surface of plants, and use it to reach a host.

The scientists in this study investigated whether exposing dodder seedling to different spectrum of light can disrupt their ability to find their hosts. They conducted their experiments on the seedlings of two dodder species - Cuscuta campestris (which parasitises tomatoes) and Cuscata gronovii (which parasitises jewelweeds), and exposed them to three light source with different spectrums - the spectrum similar to unfiltered sunlight, mostly red light, and mostly far red light. Far red is a wavelength of light which is barely visible to our eyes, but it is the wavelength which is most reflected by the surface of plants. It is also the wavelength which dodders use to home in on their host.

From the experiment, the scientists found that almost all the dodder seedlings that were exposed to unfiltered light and mostly far red light were able to attach to a host after a week or two, in fact those bathed in far red light grew faster than the other groups. However, most of those that were bathed in red light lost their ways. Only 15% of the C. campestris and 27.2% of the C. gronovii seedling that were exposed to high levels of red light had managed to wrap themselves around a host.

So will it possible to control dodder infestation simply by bathing crops in red light? No, not quite since some dodder still managed to wrap themselves around a host plant and the red light treatment is only effective during the earliest stage of the dodder's life. But at least the findings of this experiments have shown that perhaps light manipulation can be combined with other control methods to control dodder infestation.  Additionally, we have gained an insight about how these parasitic plants sense and find their way through the world.

For this particular vampire, its weakness is not against sunlight, but rather, red light.

Johnson, B. I., De Moraes, C. M., & Mescher, M. C. (2016). Manipulation of light spectral quality disrupts host location and attachment by parasitic plants in the genus Cuscuta. Journal of Applied Ecology 53: 794-803.

P.S. I recently drew some dodder-inspired art, yes, it is more Parasite Monster Girls - meet Cassandra the Dodder...