Banner image: A group of hyenas are taking a nap together. (Image: Zach Laubach)
While the 1994 animated classic The Lion King contains fairly precise antagonistic relationships between lions and spotted hyenas, Disney left out a critical player in the cycle of life: the parasite Toxoplasma gondii (T. gondii). This parasite is best known for its presence in domestic cats and its tendency to infect rodents and humans and to change behavior. This parasite has also been linked to bold behavior in wild hyena pups and the risk of death from interactions with lions, new CU Boulder research finds.
The results, published this week in Nature Communications, corroborate previous research showing that the parasite can cause profound behavioral changes in its hosts and potentially the 2 billion people worldwide estimated to be infected with it. Although T. gondii has been well studied in laboratory settings with humans and wild-caught rodents, this is one of the first studies to examine how the parasite affects game host behavior when interacting with wild cats.
Above: A spotted hyena cub in the Masai Mara National Reserve in Kenya. Below: A young, subadult, and adult hyena in the Masai Mara National Reserve in Kenya. (Image: Zach Laubach.)
The research uses a rich dataset from more than three decades of continuous fieldwork in the Masai Mara National Reserve in Kenya. It shows that hyena pups infected with T. gondii, but not subadult or adult animals, behave more courageously in the presence of lions and that infected pups are at greater risk of being killed by lions.
“This project is one of a handful of continuous long-term studies in a long-lived mammal,” said Zach Laubach, co-lead author of the study and a postdoctoral fellow in ecology and evolutionary biology. “Our results suggest that infection in early life leads to bolder behavior and is especially costly for young hyenas.”
Several strains of T. gondii are found around the world and infect warm-blooded animals – including people with domestic cats – at various stages of life through contaminated soil, drinking water, or eating meat from other infected animals. It can also be passed on from mother to baby.
The researchers found that infections are widespread in the hyena populations they studied, but more common in older animals, meaning they are most likely to become infected from eating contaminated meat or water.
In infected cubs – hyenas up to a year old – they found infected animals more courageous and approached lions from a closer distance than uninfected cubs, and this infection among cubs also corresponds to a higher likelihood of being killed by lions. In this study, lions were responsible for all hyena cub deaths in infected animals, but only 17% of uninfected cubs died before the age of one year from lion attacks.
This is a vulnerable time in the life cycle of spotted hyenas who, while seasoned hunters, take a long time to develop and rely on the support and protection of their mothers, Laubach said.
“Hyena mothers invest a lot of time and resources in their offspring. They breastfeed until they are around a year old and only become independent when they are two or more years old, ”says Laubach. “But after they are one year old, regardless of the infection status, we found no difference in close proximity to lions.”
Some scientists suggest that this parasite manipulates the behavior of its hosts (hyena or human) in order to return to cats where it can reproduce sexually. But the data from this study does not provide enough evidence to separate the theory supporting an adaptive mechanism for the parasite from other plausible alternative theories. However, it shows that T. gondii has a direct and detrimental impact on the fitness of hyenas.
Above: A teenage male lion and a spotted hyena in the Masai Mara National Reserve in Kenya. (Source: Wikimedia Commons) Below: A lion and two hyenas south of the border with Kenya’s Masai Mara National Reserve in the Ngorongoro Crater, Tanzania. (Photo credit: Megan Coughlin / Flickr)
Measure the cost of trust
The Masai Mara National Reserve is a biological hotspot in southwestern Kenya, between Lake Victoria and the bustling city of Nairobi. For more than 30 years, the Mara Hyena Project, co-authored by Kay Holekamp, has been collecting data on the health and behavior of spotted hyenas in one of the best places in the world to study a wide variety of large carnivorous mammals.
“It really is a unique system, especially for studying large predators in a natural setting, which is a rare opportunity,” said Laubach. “I can’t think of any other place in the world where you can see the same number and variety of species of large mammalian carnivores, it’s pretty spectacular.”
Laubach notes that there is a lot of misunderstanding about hyenas. They are quite gregarious and live in large groups, some with more than 120 individuals. They are also impressive in size and strength, up to 170 pounds when fully grown (twice the size of a large dog), and they have one of the strongest jaws in the animal kingdom.
“They can eat bones, their bite can crack a giraffe’s thigh bone,” says Laubach.
Still, hyenas and lions compete for territory and food, and these interactions with lions are the number one natural cause of hyena injury and mortality.
Since previous research has shown that T. gondii can affect animal behavior in laboratory settings, the researchers wanted to know: How does T. gondii affect the behavior of wild hyenas around lions, and what are the consequences?
Laubach and co-first author Eben Gering analyzed archived data collections from numerous research associates and doctoral students. They collected blood samples and documented the interactions between the hyenas and with lions. From the safety of their vehicle, researchers Benson (Malit) Pioon and Holekamp from the Mara Hyena Project 166 gave hyenas tranquilizers to test their blood for the parasite. They found that 108 or 65% had previously been exposed.
Over the years, researchers have spent many hours in the field every morning and evening, recording the hyena behavior of individuals, which can be identified by their unique speckle patterns on their fur. The data showed that infection with the T. gondii parasite was related to boldness and a higher risk of lion mortality in hyena cubs, but not in older animals. The lack of effect in older animals could be because they have had time to learn while young animals have less than a year of experience to compete with the parasite’s influence.
“One limitation of this work is that it was an observational study. But restrictions are interesting because they show what you could do next, ”said Laubach. “We want to go back and work out how behavior changes in individuals by comparing how their behavior differs before and after infection.”
Other contributors to this paper include Eben Gering of Michigan State University and Nova Southeastern University; Patty Sue Weber, Gisela Soboll Hussey, and Thomas Getty from Michigan State University; Kenna Lehmann and Kay Holekamp from Michigan State University and the Mara Hyena Project; Tracy Montgomery of Michigan State University, the Mara Hyena Project, and the Max Planck Institute for Animal Behavior; Julie Turner of Michigan State University, the Mara Hyena Project, and Memorial University of Newfoundland; Wei Perng of the Colorado School of Public Health, Denver CU Anschutz Medical Campus; and Malit Pioon from the Mara Hyena Project.
