A Huff to the Pufferfish’s Puff

This is a guest post by PhD student and science writer JakeBuehler. Heblogs over atSh*t You Didnt Know About Biology, which is full of hisunrepentantly celebratory insights into life on Earths under-appreciated, under-acknowledged, and utterlyamazing stories.

Nature is a rough place. If you live your life skirting along the more vulnerable, fragile, tasty threads of the food web, the world is just a whirlwind of claws and fangs flung about by cruel scaffolds of bone and muscle. But just as predators have evolved an assemblage of tools useful in catching, killing, and dismembering prey, their quarries have evolved a staggering number of defenses aimed at keeping themselves from being shoveled down another animals maw. There are many ways to protect yourself. You can be face-meltingly fast, like a pronghorn or a gazelle. You can live in huge herds, and rely on communal vigilance and statistics to keep you safe. You can also be as unappealing a meal as possible, and the variation in approaches to this evolutionary strategy that results in nature is astounding. Porcupines and their grapple-deterrent spines. Turtles and their notably unbiteable shells. Skunks and their odoriferous chemical weaponry. And, if you want to get gross with it, theres always going horned lizard-style and turning your own eyes into a blood Super Soaker, or, like the young of the Eurasian roller, vomiting all over yourself like you took ten shots of tequila as the preamble to a ride on the Tilt-a-Whirl.

These anti-predator adaptations abound in our oceans as well, employed by everything from urchins to hagfish, and perhaps no other sea critter provides a more iconic predation avoidance mechanism than the pufferfish (a member of a diverse group of armored/toxic/weird fish called Tetraodontiformes, which I can gush at length about, but I might be a little biased, considering they are the subject of my research). When confronted with a predator, these fish famously gulp down large quantities of water into their elastic stomachs, bloating their svelte, oval bodies into living balloons. In many species, the turgidity also raises small prickles embedded in their hide, and this, combined with their newfound voluminousness (which can leave them several times larger than their normal, deflated selves), makes them somewhat of a chore to choke down a big fishs gob. The predatory beastie realizes a lunch made of pokey exercise ball isnt going to be feasible (and an attempt might actually be fatal, as in this sea turtle), so it swims off. The pufferfish stops being all about that bass and slims down, surviving another day and (most importantly) potentially going on to breed.

Its an effective defense, but to work, the pufferfish needs to stay puffed long enough to convince the predator that better options should be sought elsewhere. The question of the energetic sustainability of the, er, inflational fortitude of these fish is made more complicated by observations in the scientific literature that suggested that when inflated, pufferfish held their breath; it appeared as though water wasnt actually passing over the gills. To make up for this inevitable loss of oxygen uptake, it was also thought that the fish were increasing absorption through their skin in their rotund form. If indeed pufferfish were holding their breath during inflation, one would think that their defense only lasts as long as they can stand going without oxygen. No one had ever actually directly tested whether or not pufferfish stopped respiring when puffed, and thats precisely what a team of Australian scientists, made up of Georgia Evelyn McGee at James Cook University and Timothy Darren Clark at the Australian Institute of Marine Science, set out to do. Their findings, published this week in the journal Biology Letters, illustrate that not only do pufferfish breathe while inflated, oxygen uptake is boosted fourfold during the act, returning to normal levels following deflation. The researchers also showed that the oxygen is being drawn in through the gills, not the skin.

The puffer of choice for this study was Canthigaster valentini, the black-saddled sharpnose puffer. Sharpnose puffers are a group of diminutive, reef-inhabiting puffers, and the black-saddled variety is common throughout much of the Indo-Pacific. The Canthigaster clan have a fan in me, as they include a unique, endemic form found only in my home of Hawaii (Canthigaster jactator), and often have interesting ecological stories; for example, the very species in this study, the toxic, black-saddled puffer, is closely mimicked by a species of non-toxic filefish for protection from predators. The fish are also commonly referred to as tobies, which is a name I far more instinctively associate with that kid in The Cider House Rules than with any fish.

Mr. Maguire is ready for his closeup. Photo from Wikipedia

Black-saddled pufferfish were collected by SCUBA from the Cairns and Lizard Island areas of the Great Barrier Reef, and then once housed and settled in tanks in the lab, they were ready for the inflation experiment. The fish were set up in customized respirometer tanks, hooked up with the capacity to measure the rate of oxygen consumption by the puffer before inflation, during inflation, and post-inflation. To persuade the little pufferfish to make like a basketball and get spherical, the scientists introduced a suction tube into the respirometer. This was then used to gently tug and suck onto the fish, imitating harassment from a predator. The pufferfish were not amused by this, and responded in the standard, unhappy pufferfish way.

Exhibit A: One very upset black-saddled toby. Photo from McGee and Clark (2014), taken by Phil Mercurio

Oxygen consumption rates collected throughout this process of puffing, deflating, and recovery showed a pronounced spike in respiration, up to four times the pre-inflation level, right as the pufferfish began to bloat (Figure 1, below). This was followed by a decline back down to near pre-inflation consumption rates throughout the duration of inflation, and subsequent further decline and slow return to normal oxygen use. So, the conventional idea that pufferfish hold their breaths during expansion couldnt be more wrong; they actually manage to breathe very well when they puff, well enough to send their oxygen consumption off the charts. This breathing continues throughout their globose tantrums, and does so solely through their gills, confirmed by the research team by 1) checking for an oxygen level dip when water was expelled (which would indicate oxygen absorption inside the stomach), and 2) using a custom-built respirometer against the skin of the fish to measure if anything was getting absorbed through the skin during inflation. No noticeable dip in oxygen levels was found upon deflation, and respiration through the skin was negligible, accounting for some 0.001% of total fish respiration.

Figure 1. Oxygen consumption rates (M_O2) of black-saddled pufferfish (C. valentini) prior to inflation, during inflation and throughout the post-deflation recovery period. The orange box highlights the period of inflation activity, with the inset showing a higher resolution trace of the mean M_O2 during the inflation period. N = 8 for all points except at 6 min during inflation (N = 6) and at 9 min during inflation (N = 4). Values are means s.e. Figure from McGee andClark (2014) DOI: 10.1098/rsbl.2014.0823

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A Huff to the Pufferfish's Puff