Gonatodes antillensis, Curaçao

Reptiles as transport hosts for mammal parasites

Last year, our intern April Lamb had the opportunity to go to Curaçao to aid Dan Warren and Teresa Iglesias with their fieldwork. While there, April was also sampling the gecko species Gonatodes antillensis for some ongoing natural history studies we have been working on. During the course of sampling, April found geckos with curious lumps beneath the surface of their skin.

She emailed me some photos asking what these were. I had never seen anything like this and asked Greg Watkins-Colwell at the Yale Peabody Museum and Greg Lewbart at the NC State University Veterinary college. Both suggested parasites as a possibilty.

April brought back some of the infected geckos from the field and we brought them to the lab of parasitologist Dr. James Flowers. He quickly identified the subcutaneous cysts as cystacanths of Oncicola likely Oncicola venezuelensis. Here is what is odd. Oncicola starts its life in termites and finishes its life in mammals such as cats. What was it doing in small ground dwelling gecko?

A. Image of individual G. antillensis with visible subcutaneous cystacnaths highlighted. Taken from our upcoming paper (link coming soon!)

What April had stumbled upon turned out to be the first observation of Gonatodes antillensis acting as a transport host for a species of Oncicola, a type of spiny-head worm (Acanthocephala) Although numerous parasites start their lives in invertebrates and must somehow get to various birds or mammals, transport hosts are woefully understudied. This is particularly true for squamate reptiles. James and I scoured the literature and found that for the Carribean, almost all records of squamates acting as hosts came from the observations in Anolis lizards.

B. Dorsal view of G. antillensis with C. slide of Oncicola cystacanth extracted from a cyst. Taken from our upcoming paper (link coming soon!)

This seemed strange to me, so James and I decided to do a thorough literature review to see if scientists had often reported squamates as transport hosts for mammalian and avian spiny-head worms in other parts of the world. We also asked collection managers in other collections to survey Gonatodes antillensis specimens for us to see if infected individuals had been hiding in plain site on collection shelves. The answer to both questions was yes.

We found over 200 records from 35 countries spanning 184 species. Over half were from snakes and the majority of records in general actually came from only a small handful of parasitologists. We further found another Oncicola in a specimen of Gonatodes antillensis collected in 1984 from Bonaire.

The results of our literature and specimen survey suggest squamates to represent an under-appreciated component of the ecology and life-cycle of spiny-head worms. These species span the squamate Tree of Life, so it is very likely that this mode of transmission may be a pervasive squamate-wide phenomenon.

In the case of Gonatodes antillensis, lets consider the life cycle of Oncicola venezuelensis. This parasite utilizes Nasutitermes termites as intermediate hosts. Parasitized termites have been found to be more vulnerable to lizard predation, and laboratory studies have demonstrated that ingestion of infected termites by lizards will result in transmission. Nasutitermes are considered native to Curaçao and species of Gonatodes for which diets are known have all been documented to eat termites. This suggests that the feeding ecology of G. antillensis may predispose this species as a transmission vector for Oncicola.

It gets worse here. Nasutitermes do very well in disturbed habitats. So do cats. The site April found these infested geckos was highly degraded to say the least and also full of cats. In other words, a perfect storm for parasite transmission.
Locations in Curaçao where we found evidence for Oncicola cystacanths in Gonatodes antillensis . A. Frequency of cystacanths per site. B. Location of sites on the island. Blue color indicates absence of cystacanths while yellow color indicates presence of cystacanths.

This ability of spiny-head worm species to infect non-definitive hosts while remaining transmittable offers a solution to the ecological problem of transitioning between different trophic levels at different life stages. We propose the following hypothesis: parasitic lineages evolve to co-opt pathways of energy flow across community food webs to reach their target definitive hosts.

If this hypothesis is true, it shouldn’t be surprising that squamates are broadly used as transport hosts, as these often represent direct links between lower trophic level consumers (e.g., arthropods) and higher level vertebrate predators. Given that we found documented instances of squamate paratenic parasitism that span the globe, we think that investigating the ecology and evolution of transport parasitism in squamates represents a potentially rich area of research of high importance to both wildlife medicine.

Our manuscript is currently accepted and I’ll post a link to it here once it is out. In the meantime, keep an eye out for lumpy lizards and snakes!

Dialogue & Discussion