Kerstin Junker, ARC-Onderstepoort Veterinary Institute

Do you remember James Thurber’s fable “The Peacelike Mongoose” about the little guy who got into serious trouble because he did not want to fight snakes? Well, the spotted guy in our story got into trouble, too, even though he had no such qualms; or was it because he didn’t?

Wondering what this is leading up to? Well, to the story of a leopard severely infected with Armillifer armillatus (Pentastomida, Porocephalidae). The full story can be read in Junker & de Klerk-Lorist (2020), but here is what we think might have happened in a (coco-) nutshell.

In April 2019, a leopard male had to be lethally removed from the area of the Lower Sabie tourist camp in the Kruger National Park. The section ranger had noticed the leopard’s severely debilitated condition, and the risk of allowing it to remain in the vicinity of the camp was judged too high. Hence, late on Sunday evening, a phone call reached Dr Lin-Mari de Klerk-Lorist, State Veterinarian at Skukuza, if she would want to conduct a necropsy on this leopard’s carcass. Being acutely aware of the importance of expanding our knowledge on wildlife diseases, Lin-Mari grasped the opportunity to conduct a full pathological investigation.

Not surprisingly so, the necropsy confirmed that the leopard was blind in one eye, emaciated, dehydrated and anaemic, had several infected bite wounds, a permanent and chronic foot injury, an abscess and suspected osteomyelitis. In addition, and quite unexpectedly so, necropsy revealed the presence of hundreds of parasites, either moving or encysted, that had invaded the intestine, liver, spleen, mesentery, peritoneal fold, mediastinum and lungs. The typical cork screw-like appearance of these parasites suggested they might be nymphs of the genus Armillifer. Seeking confirmation, Lin-Mari sent samples to the National Collection of Animal Helminths, ARC-Onderstepoort Veterinary Institute.

 

Fig. 1. Nymphs of Armillifer armillata on and in the viscera of the leopard. ©Lin-Mari de Klerk-Lorist
Fig. 2. Close-up of a nymph (centre). Upper right: cephalothorax with hooks and oral cadre. Lower left: cyst opened to show nymph. ©NCAH, ARC-OVI

Mounting some of the specimens in Hoyer’s medium allowed us to study them in detail under a compound light microscope. The morphometrics of the anterior and posterior pairs of hooks as well as the oral cadre situated in the cephalothorax and the number of annuli on the pseudosegmented abdomen allowed us to confirm the initial suspicion and to assign the specimens to Armillifer armillatus.

What makes the presence of A. armillatus in a large African carnivore so special that one would choose to report it here? Well, typically, Armillifer species are parasites of large snakes. In other words, their life cycle involves snakes as final hosts (in which the parasite reaches sexual maturity) and mammals that form part of the snakes’ prey spectrum as intermediate hosts (in which the parasite develops to the stage infective to the final host) (Riley, 1986). Snakes become infected by eating infected prey; intermediate hosts become infected when accidentally ingesting eggs containing primary larvae and shed in the snake’s faeces or sputum.

To the best of our knowledge, our findings represent the first record of nymphs of A. armillatus in a leopard in South Africa. That said, let me hasten to add that a number of large African carnivores are actually the natural final hosts for a number of pentastomids, for example Linguatula multiannulata in spotted hyaenas; Linguatula serrata in wild dogs, jackals and lions; and Neolinguatula nuttalli in lions and leopards; with numerous antelope species recorded as intermediate hosts (Christoffersen & de Assis, 2013). Even the infection of a large African carnivore with nympsh of A. armillatus is not unheard of, and leopards, lions and cheethas have previously been found to harbour Armillifer spp. in Central and East Africa (Heymons & Vitzthum, 1935; Fain, 1961; Graber et al., 1973).

Fig. 3. Leopard (Panthera pardus) ©Kerstin Junker

Consequently, what really astounded us was the extraordinarily high intensity of infection we saw. We began looking for possible scenarios to explain our finding, thinking it unlikely that such a heavy infection could have originated from mere accidental exposure to pentastome eggs in a snake’s secretions. While pentastome females are known to be prolific egg producers, they shed eggs on a continuous basis (Riley, 1986). Therefore, in order to have acquired such a heavy dose of infective stages, it appeared much more likely that our leopard had ingested one or several gravid females of A. armillatus, either on single or repeated occasions.

This scenario is supported by reports of leopards occasionally preying on pythons (Skinner & Chimimba, 2005), as well as by numerous reports of nymphs of Armillifer spp. in mustelids, viverrids and other small carnivores that hunt snakes (that is if we exclude “The Peacelike Mongoose” – and maybe that one was not peacelike at all, but simply knew its host-parasite lists). Did this leopard develop a taste for pythons and subsequently become an expert at hunting snakes, thus increasing its risk of exposure? Untypical food preferences have been recorded for leopards (Skinner & Chimimba, 2005). Or did the persisting injuries and loss of sight in one eye prevent it from successfully hunting larger, faster prey, forcing it to target slower prey? It is impossible to say and will remain an intriguing question.

Fig. 4. Southern African python (Python natalensis) ©Kerstin Junker

Similarly, we cannot judge if this extraordinarily heavy infection with A. armillatus would have ultimately resulted in the leopard’s death. However, together with the remaining anomalies established during necropsy, the severe pentastomosis undoubtedly contributed to its anaemia and overall poor body condition.

What has become abundantly clear from this case, though, is how much we still have to learn about host-parasite relationships in wildlife and the important role routine post-mortem investigations can play in increasing our knowledge base.

And the moral of it all?

“Moral: Ashes to ashes, and clay to clay,
if the enemy doesn’t get you your own folks may
the parasites may

(based on “The Peacelike Mongoose”, James Thurber, Further Fables for Our Time, 1956)

References
Christoffersen ML, De Assis JE, A systematic monograph of the recent Pentastomida, with a compilation of their hosts, Zool. Meded. 87 (2013) 1–206.
Fain A, Pentastomides de l’Afrique Centrale, Ann. Mus. Roy. Afr. Centr. Sér. 8, 92 (1961) 1–115.
Graber M, Troncy P, Thal J, Présence de larves d’Armillifer armillatus Wyman, 1847 chez divers mammifères domestiques et sauvages d’Afrique centrale, Bull. Soc. Path. Exot. 66 (1973) 183–191.
Heymons R, Vitzthum HG, Beiträge zur Systematik der Pentastomiden, Parasitol. Res. 8 (1935) 1–103.
Junker K, de Klerk-Lorist L-M, Severe infection caused by nymphs of Armillifer armillatus (Pentastomida, Porocephalidae) in a leopard, Panthera pardus, in the Kruger National Park, South Africa, Parasitol. Int. 76 (2020) 102029.
Riley J, The biology of pentastomids, Adv. Parasitol. 25 (1986) 45–128.
Sachs R, Rack G, Woodford MH, Observations on pentastomid infestation of East African game animals’, Bull. Epizoot. Dis. Afr. 21 (1973) 401–409.
Skinner JD, Chimimba CT, The mammals of the southern African subregion, 3rd edition, Cambridge University Press, Cape Town (2005).

Facts about Pentastomida

  • The phylum contains 8 Palaeozoic fossil species, and c. 144 Recent species and subspecies.
  • Pentastomes date back to more than 500 Million years ago.
  • Adult pentastomes are obligatory parasites of the respiratory tracts of especially reptiles, but also of amphibians, birds and mammals.
  • Adult and larval stages of pentastomes are haematophagous.
  • Pentastomes can cause zoonotic diseases, for example Halzoun syndrome caused by Linguatula serrata, a parasite of the nasal passages of carnivores.
  • Worldwide, the genus Armillifer is the most common in human infections.
  • Human infection with Armillifer is acquired by ingesting undercooked snake meat or contaminated water.