Risk of zoonoses in the wildlife trade

The United States is one of the largest importers of wildlife, both in terms of quantity and diversity. While there are some benefits to the wildlife trade (e.g., providing specimens for conservation research and zoos), there are many potential negative ecological, economic, and human health implications of moving species to novel places. In recognition of this threat, the Lacey Act was passed in 1900. One of the earliest conservation laws, the Lacey Act banned interstate transport of illegally taken wildlife, as well as created the Injurious Wildlife List. Species listed as Injurious are illegal to import into the U.S. without permit from the US Fish & Wildlife Service. Evidence suggests listing species as Injurious, thereby prohibiting their import, has been incredibly successful in preventing nonnative species introductions.

The American Rescue Plan Act (ARPA), passed in 2021 in response to the COVID-19 pandemic, directed the US Fish and Wildlife Service (USFWS) to evaluate the potential zoonotic threat of species imported through the wildlife trade, and to utilize these findings to inform Injurious Wildlife listing. In 2023, I worked as an Injurious Wildlife Listing Biologist for USFWS, helping develop and write federal policy to achieve the aims outlined by ARPA. In this role, I collaborated with scientists at the Smithsonian Institution who had been contracted to conduct the research to inform the Injurious Wildlife evaluations. When funding for my position was lost due to the Fiscal Responsibility Act, I was fortunate to accept an offer to join the Smithsonian Institution team. As an Applied Research Ecologist with the Smithsonian National Zoo and Conservation Biology Institute, I now work on a team that is identifying the thousands of bird, mammal, and reptile species imported into the U.S. and the zoonotic pathogens associated with these wildlife hosts.

Rose-ringed Parakeets on Kauai, Hawaii

Rose-ringed parakeets (Psittacula krameri) are one of the most invasive bird species in the world, having established nonnative populations in over 35 countries. While these birds are beautiful, intelligent, and charismatic, they can devastate native species and ecosystems where they are introduced. Further, they cause significant agricultural damage by eating crops. Rose-ringed parakeets were introduced on the island of Kauai, Hawaii, in the 1960s. What began as only a few animals is now in excess of 10,500 birds.

From 2019-2022, I led a study in collaboration with the USDA National Wildlife Research Center to evaluate management options to reduce the rose-ringed parakeet population size on Kauai. This work was funded by the Hawaii State Legislature Senate Bill No. 772, which was passed in response to the impacts the parakeets have caused on the island. Our work included 1) evaluating the efficacy of a roost culling effort – using air rifles to cull parakeets in their large nightly congregations – conducted by a private wildlife control company; 2) efforts to habituate the rose-ringed parakeets to bird feeders to evaluate the potential use of contraceptives; 3) spatial modeling to predict locations on Kauai where the population may spread; 4) evaluating the genetic diversity of rose-ringed parakeets on Kauai, relatedness to a population on Oahu, and how this information could be used to guide future rose-ringed parakeet population management in Hawaii. My collaborators and I consolidated this information into a recommended management plan for rose-ringed parakeets on Kauai.

Ocelots in South Texas

Ocelots (Leopardus pardalis) are a medium-sized felid native throughout Central and South America. Once widespread throughout Texas, Louisiana, and Arkansas, the U.S. population of the federally endangered ocelot is now restricted to the Lower Rio Grande Valley (LRGV) of South Texas. It is estimated <80 individuals remain between two genetically isolated breeding populations. While the population decline is due to several factors, vehicle collisions have been found to be one of the leading contemporary causes of ocelot mortality in the LRGV. Wildlife crossing structures may provide a viable mitigation strategy but must be placed in locations that maximize likelihood of use by ocelots.

From 2018 – 2019, I led a team contracted by the Texas Department of Transportation to provide guidance on optimal locations to build wildlife crossing structures to protect ocelots in the LRGV. My team and I analyzed an ocelot telemetry dataset spanning 35 years coupled with transportation data to conduct several studies to address this goal. We evaluated landscape features at locations where ocelots frequently cross roads and where they have been struck by cars and found ocelots are likely to cross roads which bisect large woody patches (their preferred habitat). We also evaluated behavioral patterns in ocelot road-crossing patterns (no surprise, risk-prone males cross more often than females!). This information is now being used by TxDOT to inform future roadway mitigation strategies to protect ocelots.

Invasive Rhesus Macaques in Florida

Rhesus macaques are a medium-size monkey. Spanning west to Afghanistan and east to the Pacific coast of China, they have the largest native range – or area in which a species naturally occurs – of any primate other than humans; this means they have adapted the ability to thrive in a diversity of habitats, including the frigid foothills of the Himalayas and arid semi-deserts of India. This ability to survive just about anywhere means they are also adept at invading new habitats when they are introduced.  Approximately 10 rhesus macaques were introduced in what is today Silver Springs State Park, central Florida, in the 1930s and 1940s in an effort to increase tourism. This population has demonstrated considerable growth and reached ~400 individuals by the mid-1980s. From that time until 2012, the population was controlled through a trapping and removal program, but no population control has been implemented for the past decade. From 2012 – 2018, I led several studies of this population.

In other places rhesus macaques have been introduced, they have devastated local bird populations by predating eggs. To evaluate if rhesus macaques may be depredating bird nests in Silver Springs, my team and I placed artificial nests baited with quail eggs in the macaques’ habitat. Each nest had a camera trap facing it to document predation activity. At least twenty-one of these nests were consumed by the macaques, indicating that they may be impacting native breeding bird populations.

Understanding the occupied habitats and movement patterns of invasive species is important to evaluating their potential ecological impacts. To better understand where rhesus macaques are located in Silver Springs, we placed a VHF radio collar on a female macaque. Because female rhesus macaques remain with their natal groups for their entire lives, the movements of a female serve as a proxy for the entire group. Using the data from this collar, we described the winter home range and habitat selection of a rhesus macaque group in Silver Springs. Interestingly, we found that, within the home range, the macaques maintained shorter distances to the Silver River on weekends compared to weekdays. Because many park visitors feed the macaques from boats, this indicates the macaques are likely altering their movement patterns to take advantage of these easy food opportunities.

While the radio collar study provided inference on the spatial patterns of the rhesus macaques, we were still uncertain of the population size. Using a camera trap study, we estimated the number of macaques in Silver Springs State Park, as well as the proportion of adult males, adult females, and juveniles. Using this information, we developed population models to estimate how the population may increase or decrease under different management scenarios. We found that culling (trapping and permanently removing animals from the environment) could potentially eradicate the population, whereas sterilization could decrease the population to a substantially smaller size.

From 2011 – 2016, there were ≥38 observations of rhesus macaques in Florida  outside of Silver Springs State Park. It is unknown whether these individuals represented separate introductions or if they were emigrants from the Silver Springs population. To evaluate the genetic diversity of rhesus macaques in Florida, we presented cotton swabs soaked in sucrose (i.e., snow cone syrup) to the macaques; the macaques chewed the swabs until they lost flavor, then spit out the swabs. We then collected the swabs and extracted DNA from the residual macaque saliva. We used genetic sequencing to characterize the mitochondrial genetic composition of this population. We described five haplotypes within the population, supporting the notion all members of the current population came from small, isolated introductions. Further, we collected a sample from an adult male rhesus macaque captured >100km from the Silver Springs population and determined he had a haplotype identical to members of the population. This indicates males may be dispersing great distances from the source population.

Rhesus macaques are believed to be the natural host of the Herpes B Virus. Like humans who contract Herpes Simplex 1 or 2, macaques infected with Herpes B Virus show few symptoms and experience little to no impact on their life expectancy. Transmission of Herpes B Virus from rhesus macaques to humans is extremely rare, but can be fatal. To understand this potential threat to humans in Silver Springs, my team and I evaluated historic sampling records and determined the seroprevalence rate of Herpes B among the Silver Springs macaques. To understand whether the rhesus macaques in Silver Springs were actively shedding the virus (and therefore capable of spreading it others), we utilized the saliva sampling technique used in the genetics study. We found that, while rare, active shedding was present, indicating these animals are capable of transmitting the virus.

Invasive Monkeys in Florida  

Humans have introduced other primate species to new places for at least five centuries. In the U.S., people have introduced 10 species of primates ranging from lemurs to chimpanzees. Three species of primates  have been introduced into Florida: rhesus macaques (Macaca mulatta), vervet monkeys (Chlorocebus sabaeus), and squirrel monkeys (Saimiri sciureus). As a Ph.D. student, I led a team that described the history and status of these species. We noticed an interesting trend; despite having the most introduced populations, squirrel monkeys had had the least success in establishment in the state. Conversely, the vervet monkey population had remained remarkably stable, and introduced rhesus macaque populations in both the forests of central Florida and the mangrove islands of the Florida Keys had thrived.

Climate envelope models are a unique tool to understand the climatic variables that defines a species’ range. We developed climate envelope models to characterize the climatic conditions in which the three monkey species occur in their native range, and then compared these to the conditions in Florida. Our models indicated the climatic conditions within Florida and throughout much of the southeastern U.S. are similar to those of each species’ native range. Interestingly, this suggests climate is not the limiting factor of squirrel monkey survival or vervet monkey spread in Florida. It also suggests climate will not limit continued spread of rhesus macaques. This information can be used to prioritize use of limited research and management funds.

Capybaras in Florida

Native throughout South America, the capybara (Hydrochoerus hydrochaeris)  is the world’s largest rodent. This species has recently expanded its native range in Paraguay. Further, it has been regularly observed since 1992 throughout Florida, U.S.A, where at least one introduced population included ~60 individuals. Given the potential impacts capybaras could have on native species and demonstrated ability to establish in Florida, we sought to evaluate whether climate throughout  Florida and  the southeastern U.S. is conducive to capybara requirements. We developed a climate envelope model (methodology described above) and determined climatic conditions expanding Florida and much southeastern U.S. are unlikely to curtain capybara establishment. Our results suggest managers should make efforts to quickly control future capybara introductions.

When an animal enters an environment, it leaves bits of its DNA through hair, skin, or bodily fluids; this is referred to as environmental DNA (eDNA). Detecting eDNA in water or soil is a novel technique for detecting cryptic species. Essentially, it allows us to determine whether an animal has entered a habitat without actually observing the animal. Researchers are now refining this tool to understand how long eDNA persists in different environments and how to best use to detect different species.                             Given the potential for capybaras to establish populations in Florida, managers need a low-cost and efficient mechanism to detect potential future introductions. In this study, we sought to develop an eDNA assay for the detection of capybaras in novel environments. In summer 2017, we conducted a pilot study using water from a capybara exhibit from the Rolling Hills Zoo, preserved with Longmire’s solution; we were able to successfully extract capybara DNA from the water sample, even after leaving it untouched for 85 days after initial collection. To determine if this method would work under varying environmental conditions and water body sizes, we collected samples of capybara scat from the Jacksonville Zoo and placed it in water bodies in the lab and in the field. We found we were able to detect eDNA in all water bodies, but the duration of detection varied. Future research can expand these results in environments where capybara have been introduced to better understand how the assay works in natural habitats.