Gimme Air!
Breathing under water
By middle school, most people know that blood carries oxygen from the lungs to the tissues and carbon dioxide the other way. What they probably don’t know is that the mammalian circulatory system, including ours of course, is a messy work-around of the fact that the metabolizing tissues and organs are far from the site of gas exchange in the lungs, that is, they have no direct access to the atmosphere. To overcome this, we have a circulatory system with colored, oxygen-binding proteins packaged into a swirling hurricane of cells, and a sticky, pH regulated fluid, as well as an intricate system of arteries and veins and a pump to move all this goop around. When it comes to gas exchange, insects avoid all this messy work-around by putting every cell into a personal, direct relationship with the atmosphere. They do this through a tracheal system of branching and rebranching tubes that open to the atmosphere through pairs of openings (spiracles) on their body segments, and end in microscopic blind tubes within a micron or two of every body cell.
It is the direct cell-to-atmosphere relationship that has made insects unrepentant air-breathers, but in spite of this, there are thousands of aquatic insect species that spend their immature, adult, or both stages in water. For reasons involving way too much physics, a water-filled tracheal system cannot do its job of gas exchange, so insects have evolved an amazing array of work-arounds that allow them to retain their air-filled tracheae and still exchange vital gases under water. Some are as simple as carrying a bubble of air from the surface, while some are elegant exploitations of the physics of gases, water, and surfaces.
My favorite such work-around belongs to the aquatic nymphs of dragonflies. After rains, dragonflies bombard the temporary ponds on the Florida coastal plains with thousands of eggs that soon hatch into their aquatic nymphs. The bodies of these voracious little predators are so transparent that all the world can see (with magnification) their various parts at work—- muscles, guts, nerves, heart, brain, the whole works (see image at the top). Much of this is material for later essays, but for this one, I want to focus on how an unrepentant air-breather has evolved an efficient gill through a marriage of two different organ systems.
I will describe the current gill’s structure and how it works, and then trace how this novelty evolved from a union of the tracheal system with part of the digestive system. A fortuitous predecessor to this gill is a hindgut (rectum) that functioned (and still does) as an escape organ. By forcefully ejecting water from the hindgut, the nymph jet-propels itself out of harm’s way . This ability to draw in and eject water made the hindgut “pre-adapted” for evolving into a gill, with the anus becoming a multi-purpose valve functioning in escape, digestion, and breathing.
In the image at the top of this essay, the transparency of this little aquatic jewel allows you to see some of the main features of its work-around gill. The large pigmented tubes are tracheae and are filled with air. Note that in the abdomen these are highly branched with the finer, tree-like branches ending in what look like stacks of transparent cocktail plates, which are the folded walls of the hindgut (more details below). Between these plates, the tracheae end blind at a microscopic level, with espalier-like branched units of them wedged between the multiple folds of the wall (examples in the red ellipses in the image below). Each dorsal and ventral tracheal trunk has two branches, each associated with one row of cocktail plates, for a total of eight rows for the whole gill.
Given this intimate union between part of the hindgut and the tracheal system, gases are exchanged by diffusion across the gill surface. In the video below, you see how the nymph pumps water in and out of the gill chamber to freshen the water as it accumulates carbon dioxide and is depleted of oxygen. The greatly amplified surface area created by the eight rows of dense folds matches the extreme proliferation of tracheal branches, and assures an adequate rate of gas exchange (similar principles explain why your lungs have an inner surface area of between 50 and 75 square meters, about a quarter to half the area of a modest house). Cellular metabolism alters the air in the tracheal system, and gases diffuse into and out of the water in the gill chamber according to their relative concentrations. The pumping action freshens the water repeatedly, and voila, you have an efficient gill!
The freshened air is then distributed to anterior body tissues by a pair of large, dorsal, dark-pigmented trunk tracheae extending all the way to the head, eyes, brain, and appendages, and by a less pigmented ventral trunk tracheae to the gut and ventral tissues.
OK, you say. They evolved a nice gill. But wait! There’s more! Both the hindgut (rectum) and the tracheal system are part of the integument, and have cuticular linings secreted by the same tissue that secretes the more obvious exoskeleton. Everybody knows that insects grow by molting, shedding the old exoskeleton for a larger new one. What few people know is that during every molt, the linings of this tracheal system down to the last branching points are shed by pulling the old lining out of the new and larger lining. Likewise, the lining of the hindgut is also shed (as by the way, are a number of other integumentary structures not covered in this essay).
All of these structures can be seen in the shed nymphal cuticle below—- in addition to the obvious external body surface (looks like a nymph, doesn’t it?), the molt contains the linings of the tracheal system (faint in this image), the foregut, and the hindgut/rectum (visible inside the hind end). The next nymphal stage still has all of these structures, only larger. The wing buds and the gigantic labial grasping jaw are also conspicuous (but that’s another story).
In order to make the gill more visible, I dissected away the dorsal abdominal cuticle and stained the preparation with chlorazol black, which, in spite of its name, stains cuticle blue. The rows of accordion-like folds of the gill chamber are obvious (and are shown in greater detail in the next image), as are the “stringy” bundles of tracheal linings still attached to the spiracles of their origin.
If you have ever watched an insect molt, you will understand how remarkable it is for this creature to extract a complex system of old tubes and linings from a still more complex system of new tubes and linings. But even in this context, our dragonfly nymph is special because its gill complex is formed from the association of two disparate and separate integumentary systems, yet when it is time to molt, each of these is shed independently of the other without upsetting the integrity of the remaining gill arrangement. This shows clearly in the image of the entire molt above.
I have several times pointed out that evolution always starts with something that already exists, and this amazing gill is another example. What did it start with, and how did this association come about? The process is summarized in the schematic below. Of course it started with some version of the ancestral insect tracheal system, a system that opens to the atmosphere through eight pairs of spiracles, one pair on each of eight segments (see left image below). In the ancestral system, a longitudinal tube joins all the spiracles on each side of the body, while in each segment, there are dorsal, ventral and visceral tracheal branches that serve the corresponding regions of each segment.
Of particular interest to the future gill are the rather minor-looking visceral branches serving the gut epidermis in two posterior abdominal segments. The steps that lead to the evolution of the gill are (1) in order to become aquatic the spiracles become closed to prevent water from entering the tracheal system; (2) the visceral branches serving the hindgut became highly divided into espaliered tracheal “brushes”; (3) in parallel, the walls of the hindgut became highly folded, with the tracheal “espaliers” nestled within the folds; (4) some of the dorsal and ventral visceral branches unite to form the large, dorsal and ventral body-length trunk tracheae that are so conspicuous in the images and videos above. These “new” trunks replaced the lateral, body-length ones of most insects; (5) the escape jet-propulsion mechanism was captured to ventilate the gill rhythmically.
Breathing through a modification of the lower end of the digestive tract may seem counter-rational, but then where is it written that evolution and biology are rational? Anyway, that’s what happened over evolutionary time. The chance juxtaposition of a hindgut adapted for jet-propelled escape next to healthy visceral tracheae brought them together in a happy, functional, successful marriage that has lasted more than 325 million years. They must have done something right.
As a last remarkable observation, when the final nymphal stage molts into the a winged adult dragonfly showing off its marvelous aerial acrobatics, the tracheal patterns and the hindgut revert to the “ordinary” insect state, i.e. just a plain tube served by a few ho-hum visceral tracheae. Nothing special there.
On the other hand, the aquatic nymphs in all their transparency are little precious jewels that allow us, without dissection, to see all their parts at work. What a gift for those of us who appreciate and enjoy insects as the amazing creatures that they are!
What I love about Substack is the subject matter experts writing essays like this. EO Wilson would be proud of you Walter! 👏
Initially you stated humans have a messy, work around of a respiratory system. While what you have described in dragon fly nymphs is elegant in its way, it seems just as complicated and "messy" an adaptation as ours. Fascinating! I am always enlightened by your essays.