Written by Joe Ballenger

This is a naturally occurring transparent caterpillar! However, you can clearly see the the tracheal system connected to the spiraces.
Photo: Jim Cordoba, Enio Cano

In the first part of our post, Wait, Insects Breathe? But How?, we talked about how insects breathe. Although they use oxygen, like humans, they don’t use lungs. Instead, they use a system of hollow tubes that carries oxygen throughout the body.

Also unlike humans, bugs don’t use a nose or mouth to breathe. Instead, they have openings along the sides of their body that let air in. These openings can be modified in all sorts of interesting ways to help them get air when they’re living in challenging places.

Getting air is easy for about 90% of insects. For most insects, it’s as easy as breathing in and out is for us. A big chunk of insects are able to use gills to breathe, like fish. Some need to run up to the surface of the water to grab a quick breath, like dolphins and whales. Bugs which need to surface use their water repellent outer shell to breach the surface to get airs. For these guys, breathing is different but still pretty easy.

Then, there’s that other 10% of insects which live as parasites on other bugs as a major part of their lifecycle. This video shows a lot of different ways this can work…from living amongst other bugs, to living inside other bugs:

So if you’re living inside someone else, how do you get oxygen?

That big white thing on the bug’s booty is another bug. Specifically, it’s a caterpillar which feeds on planthoppers. Eventually, it turns into a moth. Picture courtesy of Edward Trammel, via Bugguide.net.

Most of these guys live a life like the critters in the Aliens movies, happily munching on their host until nothing remains. A parasite which eats up it’s host like a predator is termed a ‘parasitoid’ because that host ends up not competing with anything else for resources after it dies. Ecologically speaking, it’s a bit different from parasitism.

A good chunk of these guys, like the caterpillar to the left, live on the outside of their host and can use the standard tracheal system to get air. Living as a parasitoid on the outside of a host is a lot harder than it looks, though. The host can always molt, leaving you without a meal unless you keep it from growing. In a lot of cases, the host can also tear you right off their skin with a small amount of damage. Plus, there are always other parasites which are looking to put their babies inside you.

So a lot of parasites prefer to live inside their hosts. It’s a lot safer, but now you’re separated from your air supply by a really thick wall of insect tissue. It’s a steep challenge, but it can be overcome in a lot of ways.

Oxygen can come to you in the blood!

Although the blood in insects, called haemolymph, doesn’t transport oxygen, there is still a lot of dissolved oxygen in there. Most insects have proteins which transport oxygen, although it’s unclear how important these are. The dorsal vessel and heart also pump oxygenated, and nutrient rich blood up to the head of the insect so its brain keeps working. Regardless, a lot of parasitoids are able to persist only on the oxygen dissolved in the haemolymph. In fact many parasitoid wasps can drive out their competitors by suffocating them, which means that this is the only way these species can obtain oxygen.

If you closely watch the video below, the wasps which have parasitized the caterpillar don’t have any apparent connections to the outside. They’re floating in the body of the caterpillar, and almost certainly getting their oxygen from the caterpillar’s blood:

This isn’t completely unlike using gills to breathe, because they’re able to get all their oxygen through the fluid they’re submerged in. There are other ways to do this, like…

Hijacking the host to get air.

This is where I think this question gets really cool. Parasitoids are the masters of manipulation, and will bend their host’s physiology to their needs. Wasps are biochemists and genetic engineers, using venom or modified viruses to change their environment in a variety of ways. They are, in my opinion, the most specialized, elegant, and beautiful insects in existence.

If wasps are the sophisticated neurosurgeons of the insect world, then flies are overzealous early explorers hacking their way through the forest which is why I think they’re more interesting. If a wasp is a scalpel which makes precise cuts, flies are a machete which does the same job by brute force. Flies don’t have elegant venom or virus delivery systems like wasps do, but they’re still able to manipulate the physiology of their hosts in some rather impressive ways.

The two flies discussed below show how different animals are able to come up with different solutions to the same problem. Let’s meet the guests of this show:

Compsilura concinnata hacks into its host’s tracheal system.

Compsilura concinnata is one of my favorite animals. It’s a fly which can parasitize over 200 species of insects, which is the broadest host range of any parasitic insect as far as I know. Like any other insect, it needs air to survive and this insect gets it’s oxygen by patching into the host’s tracheal system. While not particularly elegant, taking advantage of a pre-existing system gets the job done.

Image of Compsilura concinnata, showing larval attachment to host tracheal system. Image from Ichiki & Shima, 2003, and superimposed over Eric Carle’s The Very Hungry Caterpillar.

Compsilura starts it’s life as a larva, when the female uses a can opener-like apparatus on her abdomen to inject a larva directly into the caterpillar. After injection, it makes it’s way into the stomach of the insect. After burrowing into the stomach, the larva pulls trachea from the surrounding tissue into the stomach and attaches itself to the inside of the stomach using the trachea.

It sits here in the larva, and most likely feeds on the stomach contents of the insects until the caterpillar begins to pupate. After this, it detaches itself from the trachea and eats as much of the caterpillar as it can before emerging.

Exorista larvarum tricks it’s host’s immune system into building a snorkel.

Exorista larvarum, unlike C. concinnata, tricks it’s host into building a snorkel by manipulating a system designed to kill the fly’s larva.

Capsule surrounding a glass rod, taken from a Soybean Looper as a part of Joe’s thesis project.

Insect immune systems are much different than human immune systems in terms of how they handle invaders. Both insects and humans have cells which seek and destroy invaders, but insects circulate cells in the haemolymph which attach to the outside of invaders. These cells, known as haemocytes, form a capsule around the foreign object. After capsule formation, the insect produces a scab around the invader in a process called ‘melanization’. During the formation of this scab, some really toxic byproducts are formed and these byproducts kill the invaders.

…well, usually. We’re dealing with parasitoids here

For whatever reason, the larvae of the fly Exorista larvarum are able to withstand this onslaught with no ill effects. The females lay eggs on the outside of the caterpillars they parasitize, the larvae burrow into the host, and eventually allow the host to cover them in a scab.

After they burrow into the host, something interesting happens. The larvae don’t go into the body cavity right away. They attach to the hole they bit into the caterpillar, and hang out in the fatty tissue just inside the caterpillar. The inside of this fatty tissue is shielded from the bloodstream. After the fly grows up a bit, it begins to protrude into the bloodstream. Rather than preventing the caterpillar’s immune system from encapsulating them, they allow the process to happen and don’t appear to make any attempt to knock out the immune system.

Picture of Exorista larvarum captured by Valigurová et. al 2014 superimposed over Eric Carle’s The Very Hungry Caterpillar. The respiratory funnel can be seen as a black line over the legs.

While the caterpillar attempts to encapsulate the fly larva, it apparently scrapes right through the scab and keeps on feeding. The exposure of the maggot to the caterpillar blood again encourages the catterpillar to attempt to encapsulate the larva, only for the larva to chew through it’s scabby prison again. Eventually, a snorkel-like projection called a ‘respiratory funnel’ is formed.

The process was described in detail in 2014, by Valigurová and colleagues who took some really good pictures of what this process looks like in cross-section. The picture, superimposed onto an Eric Carle image, shows what the process looks like.

The process of repeated jailbreaks results in a larva which sits in a capsule, embedded in the caterpillar’s body wall. The respiratory funnel, created by the melanization process, allows the fly larva to breathe air from outside while it’s still inside the host. When the fly is ready to emerge and pupate, it simply burrows out the larva…a process which kills the caterpillar.

The Bottom Line

Insects have a respiratory system which resembles a series of tubes called trachea connected to the outside of the insect through openings called spiracles. Most don’t need special adaptations in order to obtain oxygen, because their spiracles are able to contact air directly. Insects which live under water have spiracles concentrated into specialized breathing structures, whether they’re gills or respiratory filaments. Some insects can even take air with them, to use either as a gill or like a SCUBA tank.

Parasitic insects employ a variety of tactics to get oxygen, and many of these tactics involve hijacking host physiology. The two examples discussed in the article are compared and contrasted in the picture below.

Citations:

A big THANK YOU to my co-blogger, Nancy Miorelli, for helping me make my lifelong wish to use a parody of Eric Carle’s work to explain parasitoid biology a reality!

Image credit:

Carle, Eric. The Very Hungry Caterpillar. New York: Philomel, 1987

Ichiki R. (2003). Immature Life of Compsilura concinnata (Meigen) (Diptera: Tachinidae), Annals of the Entomological Society of America, 96 (2) 161-167. DOI: http://dx.doi.org/10.1603/0013-8746(2003)096[0161:iloccm]2.0.co;2

Valigurová A., P. Koník, M.L. Dindo, M. Gelnar & J. Vaňhara (2013). Penetration and encapsulation of the larval endoparasitoid Exorista larvarum (Diptera: Tachinidae) in the factitious host Galleria mellonella (Lepidoptera: Pyralidae), Bulletin of Entomological Research, 104 (02) 203-212. DOI: http://dx.doi.org/10.1017/s0007485313000655