The invasive pentastome Raillietiella orientalis in a banded water snake from the pet trade

Abstract

Raillietiella orientalis is established in Florida and rapidly spreading both geographically and in known host species. A banded water snake (Nerodia fasciata), purchased in Michigan at a regional reptile show, expectorated a pentastome whose morphology and DNA sequence indicated that it was R. orientalis. This event indicates that, through the pet trade, R. orientalis has been spread 1,500 km from its previously known distribution limit. Fecal sample analyses indicated that the snake was shedding large numbers of embryonated eggs for at least several months. The diversity of reptile species that are both known hosts of R. orientalis in Florida and are commonly sold in the pet trade indicates that this invasive pentastome may become a widespread health concern for pet owners and veterinarians.

Several invasive pentastome species, including Raillietiella frenata^8,15 and R. orientalis,^9,11 are strong conservation concerns in both Australia and the southern United States. In Florida, R. orientalis uses many wild squamates as definitive hosts, including species that are commonly part of the pet trade, including Burmese pythons (Python bivittatus), corn snakes (Pantherophis guttatus), ¹² tegus (Salvator merianae), ⁶ and tokay geckos (Gekko gecko). ⁵ Here we report R. orientalis infecting a pet snake.

Pentastomes have a variety of impacts on snake health, including tissue damage caused by migrating nymphs or larvae, damage to the lung tissue by feeding adults, and secondary pneumonia and septicemia associated with this damage. ¹⁴ In Florida, infection by adult R. orientalis has been associated with morbidity and mortality in pygmy rattlesnakes (Sistrurus miliarius), ⁴ a banded water snake (Nerodia fasciata), ¹⁶ and an Eastern indigo snake (Drymarchon couperi). ¹ The life cycle of R. orientalis appears to involve 2 intermediate hosts, with larvae initially developing in coprophagous insects such as roaches, then residing in insectivorous anurans and lizards, until these second intermediate hosts are consumed by a definitive host. ¹³ This parasite appears to have negligible health impacts on the lizards and anurans that serve as intermediate hosts. ¹³ Although R. orientalis was initially restricted to south Florida, ¹¹ it has now spread north rapidly, occupying much of peninsular Florida.^12,16

A concerned owner posted on a social media site in January 2022 that their pet banded water snake had expectorated a parasite while producing an audible retching sound. The snake’s owner had previous experience in raising Nerodia and noticed that this snake had failed to grow and gain weight in the 5 mo that they had the snake, despite regular, routine feeding and no display of abnormal activity. The photo of the parasite posted by the owner showed a pentastome that resembled R. orientalis. This snake was acquired at a reptile exposition in Grand Rapids, MI, USA, in August 2021 and was labeled “Florida banded watersnake.” A photo of the snake adjacent to a ruler indicated that the snake was 47.5 cm in snout-to-vent length. We contacted the snake’s owner and requested that they freeze the parasite. We sent them several microcentrifuge tubes filled with 70% ethanol and requested that both the frozen parasite and several fecal samples from the snake be placed in the alcohol and shipped to us for evaluation.

Upon receiving the parasite, we examined it using a dissecting microscope (20×) and found that it was the anterior portion of a Raillietiella pentastome with characteristic head shape, anterior and posterior hooks, and buccal cadre. Nucleic acids were extracted from a sample of the parasite, and a portion of the small subunit ribosomal RNA gene was amplified and commercially sequenced bidirectionally, as done in prior research. ¹⁶ The determined sequence was 100% identical to the R. orientalis sequences in GenBank. We also microscopically examined wet mounts of a 0.0104-g fraction of a small fecal sample on a series of slides and counted 1,756 embryonated pentastome eggs (Fig. 1). A second fecal sample collected in late May, 4 mo after the single pentastome was expectorated, was also examined. It also contained a high density of Raillietiella eggs, indicating a patent infection.

Figure 1.

An embryonated Raillietiella orientalis egg in a wet mounted fecal sample from a banded watersnake (Nerodia fasciata).

To our knowledge, R. orientalis has not been reported previously in a captive animal acquired via the pet trade. In the future, we expect more instances of this parasite in captive reptiles given that R. orientalis is very prevalent among wild snakes in southern Florida, exceeding 50% in several common snake species, ¹² and there is often no clear demarcation between animals in the pet trade and wild reptiles and amphibians. In some cases, reptiles sold as “captive-bred” are actually wild-caught animals, as may have been true for our case. Furthermore, young snakes are often fed live wild-caught “feeder” lizards, typically Cuban brown anoles (Anolis sagrei), a species known to serve as an intermediate host for R. orientalis. ¹³ The United States exported >28,000 A. sagrei annually from 2000 to 2010, ⁷ and most of these lizards were probably wild caught in areas of Florida where R. orientalis now occurs, given the geographic ranges of these species.

The presence of R. orientalis in Michigan represents a jump of 1,500 km from its previously known northern distribution limit in North America of Alachua County, Florida. ¹⁶ Human-aided transport of pet snakes represents a rapid path to great increases in geographic range for this parasite. Florida is a global hub for the reptile pet trade, ³ and exports of R. orientalis–infected snakes and feeder lizards could result in further national and international dispersal of this invasive species. R. orientalis in pets could establish new wild populations through the escape or intentional release of snakes, through invertebrate consumption of pentastome eggs in discarded snake feces, or by using pentastome-infected lizards or frogs as feeders for snakes in short-term captivity.

The zoonotic potential of R. orientalis is unknown, but several other pentastomes that use snakes as definitive hosts can produce visceral pentastomosis in humans ¹⁰ and domestic animals. ² Veterinarians and pet owners who work with wild-caught snakes or large lizards from the southeastern United States, or snakes fed live lizards and frogs from that region, should be aware of the growing prevalence of R. orientalis and the threat it poses to pet and wildlife health.