Ecology of amphibian pathogens

 
Ranavirus-infected tiger salamander larva

A tiger salamander larva showing signs of ranvirus infection.

Ranaviruses are emerging pathogens of cold-blooded vertebrates, including amphibians. Ranavirus epidemics decimate amphibians in natural populations and aquaculture and have recently been linked to amphibian declines in Europe. In much of the world it is unclear whether these viruses present a significant conservation risk or are a more-or-less "normal" part of the communities. What is alarmingly clear, though, is that the number of reports, their geographic and taxonomic distribution, and their movement around the world in trade are all growing.

We are thus actively and passively (see the sample submission page) looking for more instances of ranavirus in new hosts and locations. We are part of a larger effort to map the distribution of ranaviruses around the world, the Global Ranavirus Reporting System. In addition, we and our colleagues have recently sequenced several dozen ranavirus isolates. We are beginning to sketch out the phylogeography of one "species" of ranaviruses, the FV3-like viruses, to determine whether there are a few wide-spread ranaviruses or many local types and what can be learned from their evolutionary history (e.g., patterns of spread). Genetic tools may also help us map the spread and introduction of novel viruses into new locations or hosts and document the consequences.

Chronic infections. In a slightly different vein, we have documented a surprisingly high prevalence of low-level, chronic infections among adult wood frogs returning to ponds. We suspect that such chronic infections may be critical to the long-term persistence of ranaviruses within highly seasonal populations. We are working to explore both the causes and consequences of chronic infections in amphibians.

Environmental DNA and other non-lethal methods of surveillance. Lastly, we have been spending a great deal of time developing and evaluating methods for detecting ranavirus in different settings (the laboratory, zoos and aquariums, international trade, wild populations), with a focus on non-lethal methods. In particular we have been working to establish how (and how well) we can detect ranavirus DNA that has been shed into the environment (eDNA). This offers the promise of rapid, low cost, non-invasive, and sensitive detection of ranaviruses (and other pathogens) in aquatic environments. This work has been funded by the American Association of Zoo Veterinarians and the Association of Zoos and Aquariums./p>

Host behavior, susceptibility, & disease transmission

In collaboration with Erica Crespi in SBS at WSU, and others

 
VIE marked tadpoles

Infected wood frog tadpoles marked with fluorescent VIE tags.

Host behavior. Transmission---the way that pathogens and parasites get from one host to the next---is central in the evolution and ecology of infectious disease. It is crucial for predicting whether a disease will invade, persist, and spread or fade out; for designing control strategies; and for understanding the evolution of virulence. Crazy as it sounds, we know very little about how transmission works in real world systems. Our goal here is to develop a more mechanistic, empirically sound understanding of transmission by linking experiments and theory. Several years ago I had a hypothesis that the key to understanding transmission dynamics was to understand how hosts interact, and thus contact and transmit infections. We used mesocosm experiments and simple mathematical models to study the effects of host behaviors (e.g., anti-predator responses) on contact rates and disease transmission. After all, wouldn't you try to avoid that huge dytiscid larva?

A dytiscid diving beetle larva

A dytiscid beetle larva.

Susceptibility and transmission. What we learned, though, was surprising. At least in our mesocosms, transmission dynamics seem to be driven by variation in susceptibility more than differences in behavior. There are several levels of variation that we think may be important. First, even among siblings some individuals are more likely to get sick and die than others. Second, susceptibility changes a great deal throughout development; at least in wood frog tadpoles metamorphosis is a particularly vulnerable time, presumably because of changes in the immune system during this massive reorganization of tisses and structures. Third, in collaboration with Erica Crespi's lab, we have been finding very different outcomes of ranavirus infection among ponds and even regions. There are likely a number of environmental factors at work, but at least in the Northeast, roads (and perhaps road salt) seem to play an important role.

 

Stress, Immunology, & Susceptibility

In collaboration with Erica Crespi in SBS at WSU, and others

 

In a broad sense, stress-related hormones, like corticosterone in amphibians, mobilize resources and redistribute leukocytes, which make an animal more or less susceptible to infection. It turns out that being infected with ranavirus elicits a stress response, too, at least in tadpoles, which causes later stage tadpoles to develop and metamorphose more quickly. Later stage wood frog tadpoles, however, are more vulnerable to ranavirus infections. We are sorting out how stress, stress responses, body condition, and development influence disease susceptibility.

Recently we have also become interested in co-infection of multiple ranaviruses (or even ranaviruses co-infecting with different pathogens) within a single host. Co-infection can influence the outcome of infections, drive the evolution of virulence, and certainly increases rates of recombination. Given the newly apparent diversity of ranaviruses and the fact that ranaviruses (and other pathogens) are being moved regionally and globally, understanding the consequences of co-infection is becoming really important.

 

Ranavirus transmission in a community context

 

We have been also begun to consider ranavirus transmission in the context of the larger aquatic community. For instance, we found that ranavirus is rapidly degraded in pond water when exposed to microbes or zooplankton. This means that transmission through the water, which is rapid in the laboratory, probably plays a minor role in ranavirus epidemics in nature. It also suggests that ranavirus does not persist between epidemics in the water. We would like to extend this work to focus on other members of the aquatic community such as scavengers and decomposers, testing whether they increase or decrease the rate of transmission from infectious carcasses in ponds. We are also very interested in understanding how ranavirus spreads between members of a community, particularly among different orders of hosts.

 

Host communities & tick-borne diseases

In collaboration with Richard Ostfeld, Felicia Keesing, Kathleen LoGiudice, Mary Killilea, and others

 

This is ongoing work on the "dilution effect" of host diversity (really, community composition) on the risk of tick-borne diseases, including Lyme disease, Human granulocytic anaplasmosis, and babesiosis. We have been using a combination of large-scale manipulations of the host community in forest fragments, lab studies of host competence and tick biology, and statistical models to understand the net influence of the whole community of tick hosts on the prevalence of infection and density of infected ticks in the forests of the Northeast. This is a big and fascinating topic that I remain really interested in, but I would direct you to Dr. Ostfeld's website for more information.

Forest fragment

A forest fragment in Dutchess County, NY that was part of our mouse and squirrel addition/removal experiment.

Modeling tick biology

In collaboration with Justin Calabrese at the Smithsonian Conservation Biology Institute

 
Mouse with many larva

White-footed mouse with many larval black-legged ticks on it.

Justin has a way of finding interesting problems in and unique angles to what most would consider well-trod, basic ecology. In fact, he has produced really novel insights into, in our case, the biology of Ixodes scapulars and other iodid ticks. We have addressed the cause(s) of aggregation of ticks on hosts,the reason(s) that adult ticks tend to attach to larger hosts ("deer topping"), and the importance of the phenology of tick emergence and questing to disease risk.