Lizards respond to the chemical call to arms of plants

Blog written by Jay Keche Goldberg. Read the full paper here.

Compared to our fast paced animal lives plants often appear inanimate, but they live dynamic lives and respond to their environment in curiously creative ways.  One of their more intriguing responses is the production of herbivore induced volatiles. These small airborne molecules are referred to as a plant’s “cry for help” since they are produced when a plant is under attack and often attract the enemies of the attacker to rescue the plant from being eaten. This phenomenon – known as indirect defense – was discovered in the 1980s and has since been an ongoing source of fascination and scientific inquiry.

Indirect plant defenses – unlike direct defenses like noxious chemicals or physical deterrents such as thorns – recruit a third party to protect the plant, rather than directly impacting the plant’s enemy. Perhaps the most well studied forms of indirect defenses are the domatia and extrafloral nectaries that Acacia trees use to house and feed the ants that protect them, but the body of literature regarding the production and perception of herbivore induced volatiles is rapidly catching up.

Since their initial discovery, herbivore induced volatiles have been shown to be produced by a diverse array of plant species – with some compounds in particular being nearly ubiquitous among plants. Unsurprisingly, they have also been shown to be responsible for attracting a wide range of predators, parasitoids, and even pathogens to the location of herbivores.  The vast majority of these animals are invertebrates – parasitoid wasps, predatory bugs, and even pathogenic nematodes – and only recently have researchers begun to examine the role that vertebrates might play in mediating this phenomenon.

Ornithologists have thus far led the charge in studying the relationship between predatory vertebrates and the plants that host their herbivorous prey. For decades researchers assumed that birds barely used their sense of smell, opting to locate prey using their acute vision instead; however, recent findings are challenging this view. Great tits (Parus major) will use herbivore induced plant volatiles to identify herbivore-infested trees, although other bird species will ignore these same prey-associated cues. Birds have been the focus of research on plant-vertebrate interactions, even though lizards and snakes have long been known to use olfaction when foraging for prey.

Anyone who has watched a lizard or snake has surely observed their tendency to tongue-flick the object around them. This uncanny behavior allows these animals to smell the world around them using a specialized organ known as the vomeronasal organ. By observing the rate at which reptiles perform tongue-flicks herpetologists have been able to study the role of different chemical cues in mediating the lives of lizards and snakes. Researchers have been able to identify the pheromones that reptiles use to find and assess the quality of potential mates, determine the prey-derived chemicals that are used while foraging, and how different species and clades differ in their reliance on chemical versus visual cues while performing these tasks.

Herpetologists have identified two distinct foraging strategies that are used by predatory lizards: active and ambush. Active foragers are constantly on the move, tongue-flicking the environment frequently as they go, while they search for prey. Ambush foragers on the other hand, sit in a location and wait for their prey to move close to them. They tongue-flick infrequently, especially when compared to active foraging species. This has led researchers to consider them primarily visually-oriented and largely ignore food-associated chemical cues, although this paradigm begins to break down when omnivorous and herbivorous lizards are studied as they are known to use chemical cues to locate plant-based foods – even when they are a member of an otherwise ambush foraging clade. Despite having known that some lizards will respond to plant-derived chemicals for years, no one had examined the response of predatory lizards to herbivore-associated plant volatiles until now.

Lizard photo
Photos of study species. (a) Striped Plateau Lizard (photo credit: Genevieve Pintel) (b) Chihuahuan Spotted Whiptail (photo credit: wikimedia commons)

During the summer of 2016 my colleagues and I decided to tackle this gap in the literature and examine the responses of lizards to isolated herbivore associated volatiles. Given the exploratory nature of our study, we selected two well-studied chemicals that are already known not be associated with herbivores and attractive to invertebrate predators: trans-2-hexenal and hexanoic acid. Trans-2-hexenal is member of the green leaf volatile class of compounds – these small lightweight compounds are nearly ubiquitously produced by damaged plants with some being produced by mechanical damage and others being exclusively associated with herbivores. Hexanoic acid is a common component of herbivore body odor and is often derived from compounds present in the herbivore’s diet. These two compounds allowed us to compare the response of lizards to herbivore-associated chemical cues that are derived from the prey itself and the prey’s host plant.  We presented these compounds to two species of lizards – one that forages actively and another that waits in ambush – on cotton swabs, as is standard in studies of lizard olfaction.

We found that our active forager responded to insect body odor, an unsurprising finding given that previous studies have found that close relatives of our study species will not only tongue-flick at prey chemicals, but even try to eat scented cotton swabs. We expected our ambush foraging species to not respond to either chemical given that it is considered a visually-oriented predator but were surprised to find that it responded to our selected herbivore-induced plant volatile – indicating that it may contribute to indirect plant defenses. We hope that future studies may expand upon ours and determine if lizards are attracted to these compounds or even analyze the response of whole families of lizards to better understand how these responses change over evolutionary time.

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