Author: Bryan Falk

Broken Caribbean termite nest.  These termites may infect anoles with a thorny-headed worm parasite, Oncicola venezualensis.

Among the many anole parasites are the acanthocephalans, or thorny-headed worms, which in anoles are typically found as encysted larvae in the body cavity, muscle, or under the skin. One of these acanthocephalans – Oncicola venezualensis – is relatively common in anoles on the Puerto Rican Bank, and is the main character in one of my favorite anole-parasite stories. The story has three parts: 1) how the parasite gets into anoles, 2) how it continues its life cycle beyond anoles, and 3) the mystery of when it all began.

In addition to anoles, O. venezualensis larvae occur in the Caribbean termites Nasutitermes acajutlae on the Puerto Rican Bank, which is a partially submerged landmass comprised of Puerto Rico and all the Spanish, U.S., and British Virgin Islands except St. Croix. These termites construct protective nests and foraging tubes in which they live (see photo), and each individual termite belongs to a morphologically distinct caste. Most are in either the soldier or worker caste, and soldiers are larger than workers, aggressive, and armed with big mandibles. These two castes also have slight color differences – worker termites have yellow heads, whereas soldier termites have dark yellow heads.

Anoles eat termites, and O. venezualensis manipulates both the behavior and appearance of its termite hosts in order to increase the likelihood that the parasitized individuals will be preyed on by anoles (Fuller et al. 2003). Infected termites behave carelessly when compared to their uninfected peers. When a foraging tube is broken, for example, the parasitized workers arrive quickly and then linger, a behavior that makes them more susceptible to predation by anoles. Infected termites also look different, as the head color of infected workers changes to a pale yellow. This increases the difference in appearance between the parasitized workers and the aggressive soldiers, and anoles presumably try to avoid eating soldiers (remember that anoles are smart decision-makers!). The color-changing strategy is effective – in feeding trials with Anolis cristatellus where the lizards were presented with petri dishes containing both parasitized and parasite-free workers, the lizards consistently preferred the light-colored parasitized termites.

After the anole ingests a termite infected with O. venezualensis, the parasite encysts (i.e., forms a cytacanth) somewhere outside of the host’s gastrointestinal tract. In anoles it remains in its larval form, unable to complete its life cycle, and waits for the lizard to be ingested by its definitive host where it will mature into an adult and undergo sexual reproduction. The identity of O. venezualensis‘s definitive host remained elusive for some time. Two primary suspects were mongooses and the pearly-eyed thrashers, since both eat anoles and are common on the Puerto Rican Bank. But, O. venezualensis remains in its larval form in both of these hosts (Nickol et al. 2006). The mystery was solved a couple of years ago – it’s cats! Fuller and Nickol (2011) necropsied a feral cat on St. John and found 87 adult worms. The life cycle for O. venezualensis is now understood to be termite → lizard or bird → cat, then begins again when termites ingest parasite eggs in cat feces. The mongooses aren’t eaten by cats, and so are dead-end hosts for the parasites.

For me, learning that the cat is the definitive host was a head-scratcher. We know that cats eat anoles, and feral cats are abundant on the Virgin Islands, particularly St. Thomas. But, it’s hard to imagine how a parasite with a complex life cycle of at least three hosts (termites, anoles/birds, cats) became invasive across so many islands. It’s also possible that a different, native anole-eater also serves as the definitive host. Bats are the only extant native mammal species on the Virgin Islands, and we know that some bat species eat anoles. Perhaps bats are the original definitive hosts? In any case, the populations of O. venezualensis have likely increased in recent times due to the introduction of cats on those islands, and whether that’s had any effect on the anole populations is unknown.