Primate field research during a pandemic: Lessons learned from the SARS-CoV-2 outbreak.

The COVID-19 pandemic abruptly halted most primate field research in early 2020. While international travel bans and regional travel restrictions made continuing primate field research impossible early on in the pandemic, ethical concerns of transmitting the virus from researchers to primates and surrounding human communities informed decisions regarding the timing of resuming research. Between June and September 2020, we surveyed field primatologists regarding the impacts of the pandemic on their research. We received 90 completed surveys from respondents residing in 21 countries, though most were from the United States and Canada. These data provide a valuable window into the perspectives and actions taken by researchers during the early stages of the pandemic as events were still unfolding. Only 2.4% of projects reported continuing research as usual, 33.7% continued with some decrease in productivity, 42.2% reported postponing research projects, and 21.7% reported canceling projects or postponing research indefinitely. Respondents most severely impacted by the pandemic were those establishing new field sites and graduate students whose projects were postponed or canceled due to pandemic-related shutdowns. Fears about increased poaching, the inability to pay local assistants, frozen research funds, declining habituation, disruptions to data collection, and delays in student projects were among the top concerns of respondents. Nearly all the projects able to continue research in any capacity during the early months of the pandemic were run by or employed primate habitat country primatologists. This finding is a major lesson learned from the pandemic; without habitat country scientists, primate research is not sustainable.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

Saltwater intrusion indirectly intensifies Phragmites australis invasion via alteration of soil microbes.

Although global change clearly influences species invasion, the exact mechanisms by which global change either intensifies or limits invasive spread remain elusive. Global change can affect invasion directly by altering abiotic conditions, as well as indirectly by altering the abundance and composition of interacting species. Here we examine the relative impacts of direct effects of saltwater intrusion and indirect effects via microbial interactions on the expansion of a model invasive plant species, Phragmites australis, in freshwater marshes of coastal Louisiana. Using a mesocosm experiment, we found that overall salinity strongly increases invasion, but the direction and magnitude of direct and indirect effects were context dependent. Indirect effects of salinity, via alterations in soil microbial composition, increased invasive performance when grown in monoculture and decreased native performance in native-only communities. However, when P. australis and natives were grown together, microbial indirect effects were not important; rather the salinity treatment increased P. australis invasion through reduction of native plant growth. Results suggest that salinity-induced alteration of soil microbes will increase susceptibility of native communities to invasion and promote P. australis monoculture expansion in later stages of invasion; whereas non-microbial effects of salinity are more important in early stages of invasion when P. australis is competing with native species. More broadly, these results underscore the importance of considering microbially-mediated indirect effects of global change in investigating the long-term outcomes of plant species interactions.

Female-committed infanticide followed by juvenile-enacted cannibalism in wild white-faced capuchins.

On 5 February 2021, we observed the first instance of female-committed infanticide followed by cannibalism in a long-studied (> 35 years) population of wild white-faced capuchins (Cebus imitator) in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. The events leading up to and including the infanticide and cannibalism were observed and documented ad libitum, with segments digitally recorded, and a post-mortem necropsy performed. Here we detail our observations and evaluate the events within the framework of leading adaptive explanations. The infanticide may have been proximately motivated by resource competition or group instability. The circumstances of the observed infanticide provided support for the resource competition, adoption avoidance, and social status hypotheses of infanticide, but not for the exploitation hypothesis, as neither the perpetrator nor her kin consumed the deceased infant. The subsequent cannibalism was performed by juveniles who observed the infanticide and may have been stimulated by social facilitation and their prior experience of meat consumption as omnivores. To our knowledge, cannibalism has been documented only once before in C. imitator, in an adjacent study group, with the two cases sharing key similarities in the context of occurrence and manner of consumption. These observations add to our growing knowledge of the evolutionary significance of infanticide and its importance as a reproductive strategy in nonhuman primates.

Cooperative rescue of a juvenile capuchin (Cebus imitator) from a Boa constrictor.

The threat of predation by snakes is considered to have played a significant role in the evolution of primate sensory systems and behavior. However, we know relatively little about individual and group responses given the rarity of observed predation events. Here we report an observed (filmed) predation attempt by an adult Boa constrictor (~ 2 m) on a juvenile white-faced capuchin (Cebus imitator) in the Sector Santa Rosa of the Área de Conservación Guanacaste, Costa Rica. The snake caught the juvenile monkey on the ground during a terrestrial play session. When the victim screamed, the alpha male, alpha female, and another adult female ran to the scene, physically attacked the snake (with bites and hits), and pulled the victim to safety. Most group members participated in the vocal mobbing of the snake both during and after the attack. Based on the outcomes of this predation attempt and published reports of other B. constrictor attacks on primates, the coordinated efforts of ≥ 2 group members is needed for a successful rescue. This observation adds to our growing knowledge of cooperative group behavior and its importance in predator defense.