Armillifer armillatus

In this post, we're going to focus on a paper about a peculiar group of parasites - the Pentastomida, also known as tongue worms. Despite their worm-like appearance, tongue worms are actually a group of heavily modified crustaceans. Pentastomids have been around since the Cambrian period, and the fossil record indicates that they were once external parasites of other crustaceans. But over geological time, they have evolved drastically and ended up living in the respiratory tract of land-living vertebrate animals - mostly reptiles.

Armillifer armillatus nymphs in the viscera of the leopard. Photo on the bottom right is a close-up of the nymph's head region, showing its mouthpart and hook-shaped clawed legs.
Photos from Fig. 1 of the paper

This paper is about a male leopard at Kruger National Park, South Africa, which became heavily infected with tongue worm parasites, specifically Armillifer armillatus. Now, a big carnivore like a leopard would usually serve as a final host for the adult stage of many worm-like parasites, and usually parasites are less harmful to their final host compared to the intermediate host which simply serves as a vehicle for the larval stages to reach their final host.

But there was one BIG problem for the leopard in this case - A. armillatus uses snakes instead of mammal as their final host. And to this parasite, even a big hypercarnivore like a leopard is just another mammal - which for A. armillatus means a temporary, disposable host for the parasite larvae to get to a reptilian host. And that leopard was infected with A LOT of baby tongue worms. Researchers found hundreds of A. armillatus larvae throughout the leopard's body cavity, encysted or crawling through the liver, spleen, intestine, and lungs. So how did this leopard ended up serving as an unwitting mobile pentastomid hotel?

Usually intermediate host for larval pentastomid are small and medium-sized mammals that pick up a few infective eggs at a time, and through this process, gradually accumulate hundreds or even thousands of larvae. But this unfortunate big cat got hit with hundreds to thousands of little baby tongue worms pretty much all at once - it doesn't matter to those parasites that they are inside a big cat and not a shrew or a opossum - it smells and feels like a mammal, so it will serve as an intermediate host.

In this case, the leopard might have eaten snakes which were infected with female tongue worms that were full of fertilised eggs. After the eggs were liberated from the adult tongue worm's body, they hatched and enter into the next stage of development - the nymphs. These larval parasites registered the surrounding tissue as that of an intermediate host, and their response was to find a cosy spot in the viscera to grow and prepare themselves for entering the gullet of a snake.

On top of that, the leopard was already in a bad state which had nothing to do with being infected with hundreds of tongue worms - that big cat was dehydrated, anaemic, blind in the right eye, with chronic wrist injuries, and covered in infected bite wounds. That leopard had 99 problem and the tongue worms were just one of them. The moral of the story here is if you are going to be eating snakes, then you better watch out for tongue worms.

Reference:
Junker, K., & de Klerk-Lorist, L. M. (2020). Severe infection caused by nymphs of Armillifer armillatus (Pentastomida, Porocephalidae) in a leopard, Panthera pardus, in the Kruger National Park, South Africa. Parasitology International 76: 102029.