Passeromyia longicornis

This is the third and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2018. This particular post was written by Lachlan Thurtell and it is about a fly that parasitise the chicks of some birds in Tasmania (you can also read a previous post about how parasitoid larvae are affected by what their caterpillar host eats here, and a post about why cuckoo eggs have thicker shells here).

Top left: Pardalote hatchling with a single maggot
Passeromyia longicornis maggot (Top Right), pupa (Bottom left),
and adult (Bottom right). Photos from Fig. 1. of the paper.

Have you ever had a nightmare where you have some strange creature crawling under your skin? Only for that creature to burst from underneath your skin, wriggling around and you can’t do anything to prevent it, or even escape after it emerges? This nightmare is very real for some native Australian wildlife.

Surviving the extreme conditions of Tasmania, competing for territory with your own species and others, avoiding predation, and facing habitat loss caused by human activities are all part of a pardalote's  daily life. However along with these trials this endangered Australian bird also faces parasitism from Passeromyia longicornis, a native Australian parasite that feeds upon weak and defenseless pardalote young.

P. longicornis is a Dipteran (an order of insects comprised of flies and mosquitos) belonging to the same family as the houseflies - the Muscidae. Houseflies are often seen as vectors of disease, carrying pathogens and eggs of other parasites. Passeromyia longicornis itself is a parasite which targets avian hosts. As an adult these flies are not thought to be parasitic but rather free living flies that feast on the decaying flesh of fruit. The larvae, however, are subcutaneous parasites that burrow their way underneath the skin of newly hatched pardalote chicks, possibly hours after the chick’s birth. Location is not very important for the larvae as they bore through the skin in a variety of different places, including the head.

Once the larvae have burrowed into the body of its vulnerable host, they begin to feed on the blood of the helpless hatchlings, a form of parasitism known as hematophagous parasitism. These vampiric creatures are known to suck the blood from their hosts for up to a week! Whilst the larvae are only known to feed upon blood, the effects on their hosts can result in death. In this study the researcher found that a whopping 85% of forty-spotted pardalote (Pardalotus quadragintus) nestlings which are parasitised by the larvae end up dying. Striated pardalotes (Pardalotus striatus) seemed to be more resistant to parasitism with only 65% of nestlings experiencing mortality. The larvae begin to pupate 3-6 days after emerging from their bed ‘n’ breakfast hosts and form cocoons where they develop over the next 17 days, however the duration of the pupal stage is shorter in warmer weather. The adults emerge from the cocoon, transitioning from a parasitic to a free living lifestyle.

Parasitism by P. longicornis is quite prevalent in both species of pardalotes. The larvae of P.longicornis were found in 87% of forty-spotted pardalotes, and 88% of striated pardalotes. Other birds were found to be parasitised by P. longicornis, such as the New Holland honeyeater, house sparrow and European Goldfinch, but showed much lower levels of parasitism than pardalotes, indicating that pardalotes are important hosts for these little blood suckers.

The pardalotes themselves may be to blame for the prevalence of P. longicornis as, unlike other birds, they pack their nests full of bark strips and grass. The nesting material is used in the pupal stage of P. longicornis as it provides a toasty environment to transition from a vampire living beneath the skin into a beautiful (if that’s your thing) fly.

Reference:
Edworthy, A. B. (2016). Avian hosts, prevalence and larval life history of the ectoparasitic fly Passeromyia longicornis (Diptera: Muscidae) in south-eastern Tasmania. Australian journal of Zoology 64: 100-106.

This post was written by Lachlan Thurtell

Cuculus canorus

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 2018. This particular post was written by Simone Dutt and it was titled "Keeping eggs warm: brood parasites and their early-hatching thick-shelled eggs" about a rather different type of parasites to the ones usually featured on this blog - the cuckoo (you can also read a previous post about how parasitoid larvae are affected by what their caterpillar host eats here).

Some birds manage to evade the burdensome task of caring for their own young by laying their eggs in the nests of other birds for them to raise. Cowbirds, honeyguides and the more well-known cuckoos are families of birds in which some members have adopted this parasitic lifestyle. Known as brood parasites, they force unsuspecting host birds to care for the parasitic chicks, often at the expense of their own young.

Photo of newly-hatched Cuculus canorus chick by Per Harald Olsen

Previous studies have found that parasitic chicks tend to hatch earlier than the host’s chicks and that brood parasites also tend to lay eggs with shells that are structurally stronger and thicker than those of both their non-parasitic relatives and their hosts. Hatching early gives a parasitic chick a head-start to enacting their instinctual plans for total nest domination by out-competing their nestmates for food and space, and in some cases, evicting rival eggs from the nest altogether. It is obvious how such extreme sibling rivalry would suit a parasitic lifestyle, however the evolutionary advantages of producing thicker eggshells are not as clear.

Several suggestions have been made to explain this adaptation: to provide extra calcium for chicks that require stronger bodies with which to evict their nestmates; to provide protection from microorganisms; or to prevent damage incurred during laying, incubation or being punctured and evicted by a host. While these benefits certainly apply to some brood parasites, they don’t generally apply to all. For example, some parasitic chicks can play nicely and refrain from evicting their step-siblings, and many of the dangers faced by parasitic eggs also affect non-parasitic eggs, thus these explanations are not wholly adequate.

A recent study published in The Science of Nature offers evidence to support a more general explanation for the evolution of early-hatching eggs and thicker eggshells in brood parasites. Based on the well-established knowledge that elevated incubation temperatures improve the development rate of bird (and other egg-borne) embryos, the researchers hypothesised that the brood parasites’ thicker eggshells may have evolved as a kind of insulation to maintain high egg temperatures and improve resistance to temperature disturbances, increasing the embryo development rate and enabling the parasite chicks to hatch earlier and carry out their nest takeover plans unchallenged.

Comparing host and parasite eggs collected from the nests of Oriental reed warblers (Acrocephalus orientalis) parasitised by common cuckoos (Cuculus canorus), they found that the cuckoo eggshells were 17% thicker than the warbler eggshells and that, as expected, the cuckoo chicks all hatched before the warbler chicks. By incubating the eggs in a laboratory and measuring the temperature of the eggshells under different conditions, the researchers found that the cuckoo eggs were significantly warmer than the warbler eggs during normal incubation.

When the incubation temperature was disturbed by exposing the eggs to different-length bouts of cooling, they found that the temperature of the cuckoo eggs remained significantly more stable than the warbler eggs throughout the temperature disturbances. The researchers also found that the warbler eggs exposed to longer periods of cooling required a significantly longer total incubation time before they hatched, whereas the total incubation time for the cuckoo eggs was not significantly affected by the length of cooling bouts.

The researchers suggest that these findings provide a general explanation for the evolutionary drivers of the fast-hatching, thick-shelled eggs of brood parasites and noted that the parasitic eggs also tend to be more spherical than those of their hosts, potentially contributing to their heat-retaining qualities; a possible direction for future study. Evolutionarily speaking, being able to maintain an optimally high temperature and withstand longer periods of cooling is a useful trait for ensuring parasitic chicks maintain their ability to hatch early in the nests of a number of different host species, who may leave their eggs unattended for varying periods of time during incubation.

Reference:
Yang, C., Huang, Q., Wang, L., Du, W.-G., Liang, W., & Møller, A. P. (2018). Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs. The Science of Nature, 105:10

This post was written by Simone Dutt

Copidosoma floridanum

It's time for some student guest posts! 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 2018. To kick things off here's a tale of how what a caterpillar eats can affect the growing parasitoid brood within it, written by Deanna O’Leary.

Meet a cabbage looper caterpillar’s worst nightmare – Copidosoma floridanum. This parasitoid wasp cannot produce offspring without its caterpillar host, and the caterpillar, once parasitized is a terminal ticking time bomb. It kind of puts a new twist on the Harry Potter quote “neither can live while the other survives”, however the wasps have revamped the plot slightly. They do in fact need and allow the caterpillar to survive and grow in order for the wasps themselves to survive to adulthood. But once the caterpillar is ready to pupate – all bets are off for our herbivorous friend. This gruesome parasitoid life-cycle tale goes something like this…

Parasitized caterpillar filled with Copidosoma larvae.
Photo by Silvia Mecenaro from here

A female C. floridanum seeks out a moth egg from a Plusiinae moth. She then inserts her ovipositor (aka egg depositor) into the moth egg and lays 1-2 eggs of her own. Now here’s where things start to get insidious. These wasps are polyembryonic – meaning one egg can divide to produce more than one identical embryo. However, unlike the identical twins of humans, they produce an average of 1500 and up to 3000 clonal offspring! This larval legion need time and space to grow and the body cavity of the newly emerged caterpillar provides the perfect safe and nourishing abode.

You would think that having thousands of larvae living inside you – sucking off your energy supply - would mean you won't have long to live, but the wasps have another card up their tibia. They are gregarious koinobionts, meaning they regulate their host’s growth and immunity, allowing the caterpillar to continue to live, and most importantly eat, providing nutrients for all inside. This can result in caterpillars growing up to 50% larger than an unparasitized counterpart by their final stage. Once the caterpillar reaches this final stage - its fifth instar - it is completely eaten from the inside leaving a hollow casing known as a ‘mummy’. The wasps then emerge as adults from this tomb.

Caterpillars can have devastating  effects on plants and the cabbage looper, as its name suggests, is quite partial to a munch on cruciferous plants (think cabbage, broccoli, kale etc.). Cruciferous plants produce defensive chemicals called glucosinilates, designed to deter the feeding of a herbivorous insect generally by reducing the ‘well-being’ of that animal. Herbivores, in turn, have evolved mechanisms to aid in overcoming this obstacle, however as always, it is an evolutionary arms race between plant and insect. But what does this have to do with our parasitoid?

In general, parasitoids of pest herbivores are considered beneficial biological control agents, reducing the number of pests found on a plant population. However, there's been little research into how these parasitoids affect the insect host-plant interaction at a chemical level. Like the “dream within a dream” in Inception, is there an effect on the plants from the parasitoids through the caterpillar? The feature study of this post set out to answer this.

A group of researchers tested the expression of glucosinilates from four cabbage populations under three different conditions – (1) fed on by unparasitized caterpillars, (2) fed on by parasitized caterpillars, and (3) untouched (control) plants. They focused on two types of glucosinilates – indole and aliphatic. They not only wanted to measure the differences in plant chemical expression, but also the effect of these on both caterpillar and wasp growth, reproductive success, and survival. They found that plants fed on by parasitized caterpillars produced 1.5 times more indole glucosinilates than those fed on by unparasitized caterpillars, and 5 times more than the untouched plants! Because parasitized caterpillars needed to eat more to survive – the plants they fed on produced more defensive compounds in response.

An unexpected result of the study was that the effects of different glucosinilates have on the host and the parasitoids. Because of their close developmental ties, things that negatively affect the host can also affect the parasites inside them - but it depends on the specific compound. When feeding on plants producing higher levels of aliphatic glucosinilates, unparasitized caterpillars suffered reduced on growth and fertility, while parasitized caterpillars had decreased survival rates. In contrast high levels of indole glucosinilates resulted in negative brood size and developmental impacts on the parasitoid, with no effect on the caterpillars.

The researchers suggested that the reason for this could lie in the way the different compounds are broken down by the caterpillar during digestion. So, C. floridanum may have far reaching effects that not only impact their hosts, but also extend to other levels of the food web, and even possibly affecting the evolution of insect-plant interactions! Maybe these parasitoids are not such a hideous nightmare considering their beneficial traits – from a human perspective at least. But they’ll never be anything but a terror for the cabbage looper!

References
Ode, P. J., Harvey, J. A., Reichelt, M., Gershenzon, J., & Gols, R. (2016). Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal, multitrophic interactions. Oikos, 125(10), 1398-1407.

This post was written by Deanna O'Leary