The Lizard and the Rotting Meat Lily

Lizards are attracted to the smells, sounds associated with the dead horse arum.

Posted Oct 05, 2020

Ana Pérez-Cembranos, used with permission.
Male Balearic lizard basking on a dead horse arum spathe.
Source: Ana Pérez-Cembranos, used with permission.

On the Balearic Islands of Spain, in the Mediterranean Sea, a complex relationship has evolved between a lizard and a lily.

The lily is the dead horse arum (Helicodiceros muscivorus), a plant that relies on trickery for pollination. It looks and smells like rotting meat, attracting female blowflies looking for a meal and a place to lay their eggs. But the deception doesn’t end there: The dead horse arum is also capable of producing its own heat, which volatilizes its putrid odor and intensifies the imitation of a decaying carcass.

Flies, loaded with pollen from other dead horse arums, arrive at the plant and enter the floral chamber across a dark tubule that likely simulates a natural orifice in a dead animal. There, the flies become trapped and, in their attempts to escape, transfer pollen to receptive female flowers. Each individual arum blooms for no more than two days and, in some cases, only for a few hours.

Enter the Balearic lizard (Podarcis lilfordi). These reptiles hunt insects and other invertebrates but also feed on plant matter, carrion, and even food left by tourists.

Miquel Angel Ballester, via Flickr. Distributed under a CC BY-NC-ND 2.0 license.
Balearic lizard.
Source: Miquel Angel Ballester, via Flickr. Distributed under a CC BY-NC-ND 2.0 license.

“They explore almost every new potentially edible element,” says Ana Pérez-Cembranos of the University of Salamanca, who studies the complex mutualism between these lizards and flowers.

Pérez-Cembranos and her colleagues previously showed that Balearic lizards are attracted to chemical cues from carcasses, as well as chemicals from the dead horse arum. Once drawn in by the stink, lizards take advantage of the abundance of flies for an easy meal. They also seem to enjoy basking on the warm spathes (flower clusters) of the dead horse arum.

But this relationship isn’t one-way. The lizards have also learned to eat the fleshy berries of the arum and studies have found that seeds that have passed through a lizard’s gut are twice as likely to germinate. During the fruiting season, the lizard is a major seed disperser of the dead horse arum.

Both lizard and plant appear to benefit from this relationship. At Pérez-Cembranos’s research site, Aire islet off the coast of Menorca, Balearic lizards scurry everywhere and the dead horse arum has gone from being relatively rare to extremely high density in only the last 30-40 years.

The Sound of Food

While working on Aire islet, the researchers noticed something peculiar. When trapped in the floral chamber, blowflies produce an audible buzzing sound, amplified by their plant prison. Not only could the researchers hear it, but it also appeared that the lizards hear it, too.

“Sometimes, we observed that, when the buzzing of a trapped fly was heard, some nearby lizard turned its head and immediately went towards that plant to enter the tubule and capture the fly,” Pérez-Cembranos says. “Those observations made us wonder if lizards are able to detect trapped flies just by the sound they make.”

Ana Pérez-Cembranos, used with permission.
A Balearic lizard in the floral tubule, searching for flies.
Source: Ana Pérez-Cembranos, used with permission.

Pérez-Cembranos and her colleagues set up an experiment in the field to investigate. They placed an opaque cup containing trapped flies and an identical empty cup 80 cm apart on a wooden board. Then they left it on the ground in a place where wild lizards forage and observed their reactions.

Lizards reacted immediately to the first sounds of trapped flies, turning their heads toward the noisy cup and approaching it from one to three meters away. They approached and explored the cup with flies significantly more than the empty cup. In addition, their behaviors at the two cups were strikingly different. Lizards tongue-flicked at the cup with trapped flies, often trying to find a way to get inside it. Although some lizards approached the empty cup, they never explored or tongue-flicked that cup.

Interestingly, most of the lizards that participated in the experiment were male. Pérez-Cembranos says there could be several reasons for the sex difference. It could just be that there were more males than females in the experimental area. However, male lizards access dead horse arum spathes more frequently than females, even defending the resources, so it’s also possible that males respond more quickly to the sound of trapped flies. In addition, Pérez-Cembranos says that males appear to be bolder than females. In other field experiments she’s conducted, she obtained more participation from males than females.

Pérez-Cembranos anticipates that further investigation on Aire islet, with its high density of both Balearic lizards and dead horse arums, should reveal more of the secrets of this complex mutualism.

“The lizards are so curious that performing experiments there is always rewarding,” she says. 

References

Pérez-Cembranos A and Pérez-Mellado V. (2020). It sounds like food: Phonotaxis of a diurnal lizard. Behavioural Processes 179:104217. Doi: 10.1016/j.beproc.2020.104217.

Pérez‐Cembranos A, Pérez‐Mellado V, and Cooper WE. (2018). Balearic lizards use chemical cues from a complex deceptive mimicry to capture attracted pollinators. Ethology 124: 260– 268. Doi: 10.1111/eth.12728.