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Hold Me, Squeeze Me, Bite My Head

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Last year, Katie Goldin was walking in her Los Angeles neighborhood when she saw, in the middle of the sidewalk, two lizards interlocked. The male, flecked like a pebble and about a foot long, had his jaws fully around the slightly smaller female’s head. “He was tenderly clasping her neck in his mouth,” said Ms. Goldin, host of a podcast called “Creature Feature.” “She seemed like she was in a trance.”

Even in a world absolutely full of bizarre reproductive strategies, southern alligator lizards are up there. The pair Ms. Goldin spotted were engaged in what’s known as “mate-holding,” a part of the copulatory process in which a male grips a female’s head in his mouth for hours or even days at a time.

It’s not clear why the lizards do this. But recently, two research projects have looked into the animals’ ecology and anatomy to better understand where, when and how this strange behavior happens. By approaching the same subject from these very different vantage points, scientists can inform each other’s research, and get a clearer picture of what’s really going on.

After Ms. Goldin saw the happy couple, she sent pictures to the Natural History Museum of Los Angeles County. Since 2015, the museum has put out a yearly call for photos and videos of alligator lizards getting it on, which it collects through emails, social media and the platform iNaturalist.

The species is the most widespread reptile in Los Angeles. But because the city is a “jigsaw puzzle of private property,” it’s difficult to do traditional wildlife surveys, said Greg Pauly, the museum’s herpetology curator. There are only a handful of published accounts of the lizard’s mating behavior in the scientific literature.

He saw a perfect opportunity for a community science initiative. Unlike more subtle natural processes, this is the kind of attention-grabber an ordinary civilian might stop to gawk at. “It’s a biological spectacle,” Dr. Pauly said. (It helps that the lizards will gladly do it in the road, as well as in apartment courtyards and backyards.)

Over the past five years, the museum has collected nearly 500 observations of mating southern alligator lizards, and another 88 of their similarly freaky cousins, the northern alligator lizard. This year, he said, city dwellers seem especially happy to play the part of lizard paparazzi during pandemic lockdown: “We saw a big uptick in submissions” from urban areas, he said.

The data set has yielded some surprises. About 7 percent of observed couplings are actually threesomes, with two males biting one female — or, in some cases, a male biting another male who is biting a female, in a kind of reptilian love sandwich. Cross-referencing the observations with weather data suggests that mating season lasts about a week and corresponds with temperature, and that mating activity increases in wet years.

The jury is still out on why the lizards mate in this manner, exposing themselves to predators, cars, the elements and prurient citizen scientists. The male might be guarding his partner, trying to make sure another doesn’t come along to take his place — although this theory is complicated by all the group sex. Or the female might be assessing the male’s strength. More long-term observations will help tease out “what in the world is going on,” Dr. Pauly said.

Sometimes, observers are able to revisit pairs to see how long they stay coupled up. (The record is 48 hours, 43 minutes, set by two sweethearts in a backyard in Lemon Grove.) “We now know from some of these observations that they will mate multiple times” during a hold, Dr. Pauly said, which may reveal one possible reason for such prolonged attachments.

A. Kristopher Lappin, a biologist at California State Polytechnic University, Pomona, is also befuddled by the mating behavior of the alligator lizard. But to him, a different mystery sticks out. In his own observations — as well as those he has perused on iNaturalist — he has noticed that “the male is holding with some degree of force,” he said. “You can see the female’s head is sort of squashed.”

Ordinary vertebrate muscles can’t exert significant force over such a long period. Imagine squeezing a stress ball all day without ever releasing, he said: “It’s not possible.”

For a paper published last week in Proceedings of the Royal Society B, Dr. Lappin and colleagues took a closer look at the southern alligator lizard jaw. The reptile’s strange mating behavior, they found, is underpinned by a special kind of muscle fiber, one rarely seen in the animal kingdom.

Most skeletal muscles are made up of twitch fibers, which contract quickly. Some of these fibers are fast and powerful, while others are slower and more resistant to fatigue. Your calf, for example, has two muscles: the gastrocnemius, full of fast twitch fibers, lets you bound up a flight of stairs, while the soleus, mostly slow twitch fibers, keeps you standing.

But other muscle cells, called tonic fibers, contract more gradually and take far longer to tire out. These have been found in human vocal cords, in fish, in the legs and necks of some turtles and in the arms of male frogs, who also hold their mates for a long time.

To test whether something similar was happening with this species, the researchers performed a fatigue test, repeatedly stimulating the jaw muscles of several lizards and measuring the bite force produced. Previous research on twitch-heavy muscles shows that they generally tense and then fatigue soon after. Measured on a graph, the force they create looks like a series of mountain peaks.

Instead, the lizard jaw muscles tensed, fatigued slightly and then tensed again even harder. On a graph, they formed a line like a staircase, which eventually plateaued into a constant bite force. The performance surprised even the researchers. “We thought there was something wrong with the equipment,” Dr. Lappin said.

Molecular analysis confirmed the presence of tonic fibers. But some of the results remain confusing. The sustained bite is also pretty forceful, which is rare with tonic muscles. And male and female lizards both had these fibers, even though it’s unclear when the females might use them.

These two forms of inquiry — a wide-ranging ecological survey, and an experimental anatomical study — are very different. But together, they help us slowly close in on a fuller understanding of a common animal with a strange behavior.

The Natural History Museum’s citizen science database helped his team see many examples of mate-holding, and to learn much more about how long it can last, said Dr. Lappin.

And knowing how the muscles work will influence Dr. Pauly’s thinking about how the lizards pull off these feats of strength, he said. He wondered whether sex differences between the lizards might become more pronounced during mating season. Such changes are observed during frog reproduction time, when males of some species suddenly develop “Popeye arms,” he said.

The lizards have their own concerns. Having made their contribution to science, Ms. Goldin’s pair eventually scurried off — “doing a clumsy sort of three-legged race, as they weren’t willing to let each other go,” she said. “Hopefully they found some privacy.”



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