Inflation is probably what puffer fish are most known for (it’s what their common name comes from). Although this seemingly drastic process seems like it is too radicle to have evolved by chance in nature, Peter Wainwright has done extensive studies of puffer fish and has determined that inflation is only a few key mutations away from behaviors seen elsewhere in closely related fish families [16]. It turns out inflation has evolved in two steps, starting from fish who would seem to cough (expel water out of their throats/mouths) because they ate many slimy worms and other creatures. This slime would coat their mouth cavities and cover their gills. In order to dispel the slime that would otherwise inhibit normal function, the fish would close their gill slits and use muscles on the side of their “faces” to force water out, dispelling everything in their mouth cavity (including the slime). The next step in inflation was from a “water blowing” behavior. Fish strengthened their muscles used to cough and contracted them for longer in order to more forcibly expel water, and constricted their mouths in order to get a smaller, more powerful stream. The would use this targeted water jet to overturn sea urchins and other invertebrates in order to expose their weak, edible underside, circumventing their usual defenses[16].
Diagram of inflation behavior phylogenetic tree. Courtesy of 16.
Inflation uses these same muscles to force water into their stomachs, as opposed to out of their bodies. Fishes’ heads are usually firmly attached to their shoulders, over puffer’s head are hinged, which allows them to dramatically increase the size of their mouth cavities. Full blown inflation begins when the puffer takes about thirty-five gulps of water over the course of 14 seconds. Then, a key valve usually keeping the esophagus closed flips up blocking the mouth[15]. The fish then uses the muscles described above to force water towards the front of the mouth, directing it down the esophagus, filling the stomach with water. A puffer may inflate for many reasons: if it feels threatened (increasing size makes it seem larger and more intimidating), if it may become eaten (a large water-filled fish is much harder to swallow), if it hasn’t inflated in a long time, or for no apparent reason. A puffer can generally maximally inflate to two to three times its normal size. It can remain inflated until it no longer feels threatened, with no consequences other than loss of mobility. It’s also important to note that a puffers stomach and skin are remarkably stretchy, for obvious reasons. Also, puffers do not have ribs, which if present, would inhibit the inflation process[15].
Here’s an example of a puffer inflating/deflating (with hilarious British commentary). Note the visible valve that covers the puffer’s mouth at times. This puffer also doesn’t fully inflate.
http://www.youtube.com/watch?v=NWKbKRu9KJM&feature=related
Diagram of a fully inflating puffer. Source: http://www.allisterlee.com/2007/09/puffy-debate.html