Over the last decade, my research has included both field and laboratory-based data collection, with the integration of technology to study both the behaviour, population stability and health of Amazonian wildlife. In the Peruvian Amazon, I manage a long-term mark-recapture program of saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins. Most recently, this work has expanded to include community-level disease screening of birds, bats and small mammals, with concomitant DNA barcoding and targeted population genomics screening. Rather than focus on exporting samples from host countries for analysis in foreign laboratories, not a possibility for some protected species, my team and I have focused on local capacity building by installing molecular genetics field laboratories in Peru, Mexico and India.
Biodiversity Monitoring through Field Genomics
The Why: As forests become increasingly fragmented wildlife populations become isolated from each other and conservationists are faced with evaluating the viability of populations of threatened species to implement species survival plans. Such research is often only successful, however, for species at high population densities or for those that we can easily track. Time and again, cryptic or rare species are routinely missed in even the most comprehensive surveys. For example, my previous work analysed mammal surveys over 40 years and revealed that the small and elusive Geoldi's monkey (Callimico geoldi) is present in areas that have little or no protection, and missing from many protected areas - if, that is, we can even locate it. Mostly, however, it is tough to survey on foot, and thus survey technology must adapt to be beneficial for such species, in a variety of habitats, regardless of the ease of tracking these animals in the wild. Obtaining biological samples from a broad group of animals is difficult, but once achieved, the obstacles to analysing them do not end there. When many surveyed species are either data deficient or threatened, laws protect the transport of these samples outside of host countries (and rightfully so). This has the unintentional difficulty of widening the gap between some countries in which tools and science are racing ahead, becoming increasingly more expensive and out of reach, and other countries in which the bulk of biodiversity resides today. So how can we improve biodiversity detection and monitoring to be low-cost, widely applicable, and available to all scientists?
The How: I believe that the answer today lies in the innovative use of decentralised field laboratories to address problems in situ that have been virtually impossible to study in the past. My research focuses on using molecular tools directly within an animal's habitat, in what is termed field genomics. Conservation genomics, when implemented outside of urban laboratories, can be all the more powerful by becoming efficient and accessible. Beginning in 2018, I have worked to establish four field laboratories, including the Amazon's first molecular genetics field laboratory, the Inkaterra Green Lab. In 2021, along with the In Situ Labs Initiative and the Gordon and Betty Moore Foundation (grants 1 and 2), we are expanding our efforts to establish a conservation technology hub with a focus on large-scale biodiversity and disease surveillance in southeastern Peru. Additional labs I have assisted in setting up are located in Mexico and India.
The What: My research today explores various avenues in which we can push the boundaries of what field laboratories are capable of. DNA barcoding: I'm exploring large-scale DNA barcoding of species in the Madre de Dios region of Peru, beginning with the sampling of over 500 animals in 2018, belonging to a minimum of 100 different species. Expanded datasets are due to be analysed in 2021-2022. Metabarcoding Diets: Field genomics can be used to assess dietary specialisations and overlap between species from noninvasive samples such as feces. For this, we use metabarcoding of eukaryotic DNA within each sample, comparing outputs to reference databases produced by DNA barcoding efforts in the region. This might sound more complicated to achieve, but ultimately it is far more detailed than any manual assessment of diet can be, particularly for small arboreal primates (see capture protocols below). Population Genomics: As a part of the Population Sustainability department of the San Diego Zoo, I am responsible for developing functional field genomics tools that we can deploy to our conservation programs globally. I serve as the coordinator of such efforts today for reticulated giraffe, Sumatran tigers, leopard in India and Kenya, sloth bears, and Andean bears. In addition, I'm developing similar programs for a broad swathe of neotropical mammals through the In Situ Labs Initiative.
The Sex-Health Paradox:
As early as the mid-1700s, the first life history tables assembled for human populations indicated that females experienced greater longevity than males. Despite many population-specific features, this general pattern seems to hold true across many different human communities. The paradox, however, lies in the fact that men tend to report better health parameters than females, despite on average not living as long as women do.
Testing the sex-health paradox involves measuring longevity, senescence and health indicators, and has been successfully attempted in numerous studies of human populations. Among the nonhuman primates, however, this paradox has only been investigated in the baboons of Amboseli. The Amboseli dataset is incredibly rich – spanning 40 years of near-continuous observation and detailed health monitoring. And at Amboseli, despite every expectation that baboons too would display this paradox, it was found not to be supported.
Why would this occur with long-lived, savannah primates such as baboons who so closely resemble our earliest ancestors? What can we expect among the callitrichids, with their significant departures from the baboon pattern? They are female dominant, cooperatively breeding, shorter-lived and rainforest-dwelling primates. At Los Amigos, we are building the robust dataset that is required to ultimately answer these questions. Every year, we add another piece of the life history puzzle while monitoring health indicators across seventy animals, two species, and fourteen primate groups.
To gain a better understanding of the physiology and health of wild primates, it is essential to be able to observe them up close. However, the capture-program at Los Amigos was initiated for reasons very far from these scientific aspirations. To put it quite simply, the Callitrichidae are notoriously homogenous in their appearance, making it virtually impossible to tell any adult from another in the group. Males and females look alike, and to make things more difficult, they routinely give birth to infants who grow quickly into morphologically identical adults. Thus, the study of the behaviour of these fascinating primates is often restricted to group-level approaches.
To circumvent such problems associated with studying diminutive arboreal primates, we implemented a mark-recapture protocol in 2009. We began with the saddleback tamarins (Saguinus fuscicollis, now known as Leontocebus weddelli or Saguinus weddelli), but soon incorporated emperor tamarins (Saguinus imperator) and titi monkeys (Callicebus brunneus) into the program. Today, our protocol for safely working with small arboreal primates has been published, and the detailed guide is available upon request for those with a scientific and noncommercial interest in working with these primates.
Although capture programs can and have been misused in the past for exploitative or even merely careless reasons, it is imperative not to keep protocols hidden from use. A good capture protocol can save lives and reduces unnecessary stress to animals. Thus, we are currently involved in soliciting and recording capture-and-release protocols used by primatologists and veterinarians on wild primate populations across the globe. For more information, or to participate in this program, please see here.