Parasite-Swapping Between Two Introduced Species: The Cane Toad Strikes Again
Aliens are among us, and they don't have to come in the form of little green humanoids to cause problems. Non-native species create major headaches, whether they are introduced intentionally or arrive at far-flung places as stowaways. These "alien" invasive plants and animals can (and often do) wreak havoc on native species, because local organisms often lack the adaptations to deal with a novel predator and/or competitor to which they've never before been exposed. Entire ecosystems have been disrupted as new arrivals simply overwhelm native communities, and this often has profound economic as well as ecological consequences.
Examples are legion. European rabbits swarmed Australia, zebra mussels clot North America’s Great Lakes, and gray squirrels are driving declines in red squirrels in Europe. Among our photosynthetic friends, kudzu has blanketed the southeastern United States, Sri Lankan hydrilla chokes waterways across the globe, and New World prickly pear cacti are progressively invading landscapes in Africa and Australia.
One aspect of invasion ecology is often overlooked, however: many “attempted” invasions fail (Miller & Ruiz 2009). If an introduced or stowaway species doesn’t have just the right adaptations to flourish in a novel environment, or if too few individuals are transferred to produce a sustained population, the would-be invader can quickly die out. Even successful invasions sometimes require multiple introductions in order for an invasive species to establish a strong footing in a new place (or to take root, in the case of plants).
So, the success of an invasive species depends upon its being able to survive and thrive in a novel environment. But there is a potential twist in this story . . . parasites and pathogens can also be shuffled around the globe, arriving uninvited in novel environments and naïve hosts with no inherent defenses. This was tragically demonstrated by the decimation of native American populations after Europeans introduced smallpox and other diseases several hundred years ago.
The pattern continues. Chytrid fungus is devastating New World amphibian populations, the southeastern United States lost nearly all of its American chestnut trees to a Chinese chestnut blight in the early 20th century, and the possibility of an introduced pathogen or parasite wiping out major food crops (a very real risk, given our penchant for monocultures and mass-production) strikes fear into the heart of agriculturalists and foodies everywhere.
Parasite introductions are interesting for another reason: most parasites hitch rides within the body of a host—their ideal habitat happens to be portable. If its host flourishes, a parasite is relatively protected and can prosper in tandem. If the parasite can successfully transfer to native species, its rate of spread may even outpace the expansion of its original host. It is a biological version of the Trojan horse story.
So, in a nutshell, if an introduced plant or animal carries a parasite that is capable of transferring to alternate hosts in its new environment, a double-whammy invasion can occur. This carries potentially devastating consequences for native species, as they must then battle both new competitors for external resources and a novel invasion of their own bodies by a new parasite. [I am focusing on parasites in this instance, but a very similar dynamic can apply to pathogens such as viruses].
Now, a case study. The Asian house gecko (Hemidactylus frenatus) was introduced to northern Australia through the port of Darwin in the mid-20th century, most likely by hitching rides on incoming cargo ships. Although it has established itself in Darwin, this gecko remains restricted to urban environments, and has not spread significantly through the countryside.
The Asian house gecko did not arrive in Australia alone. It plays host to the pentastomid parasite Raillietiella frenata, which infects lizards and amphibians across the globe. Infected animals shed pentastomid embryos in their feces, which are then consumed by coprophagous insects, such as cockroaches. These insects serve as intermediate hosts. Inside the insect’s body, the pentastomid embryos mature into infective nymphs.
It turns out that geckos find cockroaches very tasty. (We won’t dwell on the fact that the gecko’s favorite food is an animal that commonly chows down on gecko feces. To each their own). When a gecko consumes an infected insect, the nymphs burrow into the gecko’s lungs and feed on its blood. This can cause fatal pneumonia, hemorrhaging, or just plain suffocation. The Asian house gecko clearly would have been better off leaving R. frenata behind in Asia, but alas, that was not the case.
Native Australian species were lucky at first: as we noted, the Asian house gecko is limited to developed environments. The only known intermediate hosts of R. frenata are urban cockroaches. Where there are humans, roaches are abundant, providing a strong incentive for both gecko and pentastomid to stick around urban areas. The geckos also apparently find it easy to hunt insects under urban lights (Hoskin 2011). Fortunately for the native wildlife, only a few patches of Australia are truly developed, and the invasive pair has not been able to span across rural areas.
Nothing can ever be that simple, of course. Here, yet another invasive species comes into the picture (a common theme in Australia’s beleaguered environmental history). The cane toad (which achieved most of its infamy under the name Bufo marinus, but has recently been renamed Rhinella marina) has been introduced all over the globe, and generally wreaks environmental havoc wherever it goes. In the first half of the 20th century, the cane toad was often introduced to new regions in hopes that it would control crop-eating insects that threatened crops. As it turns out, the toad turned out to be more harmful than helpful. It is toxic to predators, has a voracious appetite to support its hefty bulk (in the words of its USGS Non-native Aquatic species account, it is "enormous"), and disperses across the landscape rapidly. In other words, not many things can eat it yet it eats prodigiously and spreads far and fast: the cane toad is a perfect candidate to become an invasive species.
The observant reader may have noticed something worrying: remember, pentastomids infect both reptiles and amphibians. Toads are amphibians. And herein lies the potential catastrophe: if the aggressively invasive cane toad were to pick up a novel parasite from, say, an introduced gecko, and then ferry it around rural Australia, the potential ramifications for native species could be huge.
A team of researchers from Sydney decided to investigate this case, to determine whether the cane toad might facilitate an amped-up R. frenata invasion by presenting itself as an alternate host to the strictly urban gecko. Their results were published in a recent issue of the journal Oikos (Kelehear et al. 2013).
Kelehear and colleagues tackled three main objectives:
1 ) Conduct an experiment to test whether toads are good hosts for R. frenata: can the pentastomids breed inside toad bodies?
2) Determine whether R. frenata infection in cane toads is correlated to proximity to the city of Darwin, degree of urban development, and/or time since toad invasion.
3) Quantify whether urban development affects the the rates of pentastomid infection in cane toads.
A lab experiment was conducted to test whether cane toads are successful hosts for R. frenata. Wild toads were collected from an area known to be R. frenata-positive, and while in the lab their feces was collected to check for pentastomid embryos. After 20 days, the toads were euthanized so that their lungs could also be checked for the parasites.
This experiment showed that toads do indeed pass pentastomid embryos in their feces, meaning that they’re capable of distributing the parasite as they go about their nomadic lives. No embryos were found in the toads’ dissected lungs, but the presence of “fully embryonated” eggs in their feces shows that the cane toad is an effective vector for the parasite.
With the cane toad’s status as a vector confirmed, it was time to look at host-parasite dynamics in the wild. Kelehear and colleagues spent six years collecting toads (by hand!) from 22 sites across Australia’s Northern Territory. Darwin was a hub for the sampling sites, but collection efforts radiated out up to 708 km to the south of the city. Many of the sites were visited for at least a dozen sampling sessions over a period of years.
The toads were euthanized, and their internal pentastomids were harvested and counted to calculate both prevalence (the proportion of individuals in the population infected with R. frenata) and intensity (the number of R. frenata individuals within an individual toad). Remember, this is an aggressive, overpopulated invasive species, so the animal sacrifices can actually be seen to serve a greater good in this case.
To relate infection metrics to urban development, the team used aerial images to count the number of buildings with in a 650 m radius of each collection site. Finally, the team documented potential temporal changes in host-parasite metrics by repeatedly sampling two focal sites for nearly three years.
The results are both fascinating and ominous. The prevalence of pentastomid infection in cane toads was negatively correlated with distance from Darwin—the farther from the city, the lower the infection rate in a population. Likewise, prevalence was positively correlated to the number of buildings at a collection site. So it seems that, as expected, pentastomid infections radiate from urban centers—namely, the city of Darwin.
When it came to infection intensity—the number of individual pentastomids found in each cane toad—there was no relationship between either distance from Darwin, the number of buildings at a site, or the prevalence of infection in the population. This may indicate that cane toads have a carrying capacity for the pentastomids above which they either cap their personal collections of parasites or simply die. Neither prevalence nor intensity changed over three years at the long-term collection sites.
To sum up the results, Kelehear and colleagues found several items of acute concern:
1) Cane toads are effective vectors of a novel parasite.
2) Darwin is a critical hub for the radiation of the parasite
3) Although prevalence decreases with distance from Darwin, toads are indeed carrying viable R. frenata populations out into rural areas.
It is mildly promising that prevalence was stable over time, meaning that there may be some biological checkpoint to R. frenata infection rate in cane toads—perhaps in rural areas there aren’t quite enough roaches or other intermediate hosts to allow many pentastomids to complete their life cycles. Still, at some point the parasite could adapt to a new intermediate host, or for some other shift in dynamics could occur. The potential for a a broader establishment of R. frenata looms over northern Australia like a second shoe waiting to drop.
R. frenata has already been found in both a native frog (Kelehear et al. 2011) and a native lizard (Barton 2007), showing that establishment in local species may be more a question of “when” than “if.” In addition, cane toads have very wide ranges, and have spread over a prodigious swath of Australia. If they manage to ferry the parasite between urban centers, they will create new hubs of infection that will radiate into local countrysides, and “safe” areas will contract. Efforts to curb cane toad populations are already in effect due to their other negative impacts on native communities, but the situation will clearly need to be intensely monitored. This case is a prime example of how mixing new species in new environments can create dramatic shifts in community dynamics, with potentially dire results.
Barton, D. P. 2007. Pentastomid parasites of the introduced Asian house gecko, Hemidactylus frenatus (Gekkoniade), in Australia. Comparative Parasitology 74, 254-259.
Hoskin, C. J. 2011. The invasion and potential impact of the Asian house gecko (Hemidactylus frenatus) in Australia. Australian Ecology 36, 240-251.
Kelehear, C. et al. 2011. Using combined morphological, allometric, and molecular approaches to identify species of the genus Raillietiella (Pentastomida). PLoS ONE 6:e24936.
Kelehear, C., Brown, G. P. & Shine, R. 2013. Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion Oikos 122, 1317-1324 DOI: 10.1111/j.1600-0706.2013.00292.x
Miller, A. W. & Ruiz, G. 2009. Differentiating successful and failed invaders: species pools and the importance of defining vector, source and recipient regions. In: Rilov G, Crooks JA, editors. Biological Invasions in Marine Ecosystems. Berlin: Springer. pp. 153–170.