NATURAL HISTORY NOTES NATURAL HISTORY NOTES The odd couple: interactions between a sloth and a brown jay 170 W African oxpeckers (Buphagus spp) perch on the backs of large mammals, such as zebras and rhinoceroses, and feed on ticks, botfly larvae, and other parasites (Dean and MacDonald 1981). Several South American bird species have been observed foraging for ectoparasites on the skin of capybaras (Hydrochoerus hydrochaeris) (Tomazzoni et al. 2005). Even close relatives of the brown jay, including magpies (Pica pica), have been seen perching on ungulates and pecking insects off the mammals’ bodies (Bent 1946). But this is the first known feeding association documented between a brown jay and any mammal. Brown jays feed opportunistically on a diverse assortment of prey including insects, spiders, small lizards, and frogs, as well as many wild fruits (Stiles and Skutch 1989). Now, you may be wondering why a brown jay would want anything to do with a mouthful of sloth fur. Three-toed sloths harbor a diverse and highly specific assemblage of algae, fungi, and coprophagous arthropods, including pyralid moths (Cryptoses spp) and scarabaeid beetles (Waage 1979), in their pelage. These arthropods depend on the sloth for phoresis, a special form of commensalism in which one organism attaches to another, primarily as a dispersal mechanism (Waage and Best 1985). However, phoresis can also facilitate reproduction, as in the case of the pyralid moths. Each week when a sloth descends from the canopy to the forest floor to defecate, gravid female moths leave their sloth host and oviposit in the fresh dung. After hatching, moth larvae feed on and pupate within the sloth dung, then emerge as adults and fly to the forest canopy to locate potential mates within the fur of a sloth (Waage 1979). These moths depend entirely on sloths to complete their life J Yu hen we speak of biodiversity loss, it is almost always in terms of the extinction of individual species. Forty years ago, however, Janzen (1974) wrote of “a much more insidious kind of extinction: the extinction of ecological interactions”. Ecological interactions are critical elements of biodiversity and the Earth’s ability to generate more biodiversity (Bøhn and Amundsen 2004). As conservation research is shifting toward a landscape perspective with an increasing emphasis on the structure and dynamics of species interactions, Janzen’s concerns are finally being addressed. In May 2014, I traveled to the cloud forests of Costa Rica to study the spatial ecology of three-toed sloths (Bradypus variegatus) for my thesis research. On one particular cloudy afternoon, I was searching for sloths on a 15-ha tree plantation near the town of San Isidro de Peñas Blancas. As I walked a transect, I spotted a sloth feeding on leaves in a Cecropia tree while a flock of brown jays (Psilorhinus morio, Corvidae) caused a commotion nearby. Although the raucous calls of the brown jays caught my attention, the sloth appeared to be unfazed. Three brown jays, perched on Cecropia branches, exhibited a keen interest in the sloth. What exactly the birds were so interested in was not initially apparent. As one brown jay audaciously inched closer (Figure 1), tilted its head, and drove its beak deep into the sloth’s fur, I began to better understand the bird’s behavior. While the sloth was busy feeding, the brown jay appeared to be searching for a meal of its own (Figure 2). Video recordings of this unusual interaction are available on YouTube (http://youtu.be/OwvvNKRFvIY). Feeding associations between birds and mammals are widespread, both taxonomically and geographically. Figure 1. A brown jay (Psilorhinus morio) approaches a brown-throated three-toed sloth (Bradypus variegatus) in San Isidro de Peñas Blancas, Costa Rica. www.frontiersinecology.org © The Ecological Society of America KD Neam © The Ecological Society of America 171 J Yu cycle. As a result of this phoretic relationship, the pelage of sloths contains a concentrated reservoir of moths and other insects that would certainly be appealing to a brown jay seeking a meal. Before making an attempt to tease apart the precise nature of the sloth–brown jay interaction, it is important to first discuss the types of ecological relationships that exist between sloths and their arthropods. Most research on sloth–arthropod relationships indicates that there is no apparent gain for the sloth host, and thus the interaction is a commensal one (Ratcliffe 1980; Waage and Best 1985), but recent work by Pauli et al. (2014) suggests that pyralid moths are “phoretic symbionts”, whereby sloths also benefit from the association through a series of linked mutualisms. Specifically, Pauli et al. postulated that the sloths’ precarious and energetically costly journey to defecate on the forest floor is not solely for the benefit of the moth; rather it is driven by a cryptic, yet critical, nutritional input. Whenever the adult moths die on their sloth hosts, fungi living within the cracks of the sloth’s hair decompose and mineralize their remains. This process increases the concentration of inorganic nutrients within the sloth’s ecosystem, thus fueling algal growth. Pauli et al. (2014) suggested that sloths consume these lipid-rich green algae (Trichophilus spp) in their fur to augment their nutritionally limited diet. In addition to nutrient supplementation, these fur-borne algal communities provide camouflage against aerial predators (Vizcaino et al. 2008). Under this scenario, it is a complex mutualism, rather than a commensalism, that drives the sloth–moth association. The implications of the sloth–brown jay association for the sloth depend on the nature of the relationship between arthropods and their sloth hosts. If it is commensal, then the observed consumption of arthropods by the brown jay may also be a form of commensalism, in which the brown jay benefits and the sloth is seemingly not affected. Alternatively, if the sloth–arthropod relationship is a form of mutualism from which the sloth also derives resource benefits, as suggested by Pauli et al. (2014), then the brown jay’s feeding behavior may represent parasitism. The removal of adult moths from the sloth’s fur could potentially cause indirect negative effects; decreased availability of organic nutrients would limit the release of inorganic nutrients by fungi, ultimately resulting in lower algal biomass and nutrient intake by the sloth. The loss of moths, and consequently algae, could also negatively affect the sloths by making them more visible to predators. Sloths also carry an assortment of hematophagous ectoparasites, including several genera of ticks, mites, biting flies, and triatomine bugs (Waage and Best 1985). If the brown jay was foraging for ectoparasites rather than moths, then they would be providing a beneficial service by removing these parasites. Sloths could further benefit from having brown jays in close proximity if the former are alerted to the presence of predators in the area by the birds. More research should be conducted to pinpoint the true ecological relationship between sloths and their Natural History Notes Figure 2. The brown jay feeds on pyralid moths and other arthropods hidden in the sloth’s fur. associated arthropods before any inferences can be made about the sloth–brown jay feeding association. The unforeseen events that transpired during my threemonth-long investigation show the advantage of spending an extended period of time in the field. Had I conducted a study using existing data on sloths rather than traveling to Costa Rica to collect data of my own, I would not have had the chance to witness this interaction. Field-based approaches to scientific research provide an opportunity for building a solid understanding of species distributions and activity patterns, as well as biotic interactions and their importance in maintaining ecosystem processes. Such new discoveries from the field offer important insights into the functioning of ecosystems and communities. Discoveries of new information about organisms often reset the research cycles of hypothesis testing and theory refinement that underlie progressive science (Greene 2005). Understanding how organisms interact through natural history and descriptive ecological research can help us make important scientific advancements and practice conservation more effectively. n Acknowledgements Financial support for this research was provided by the Department of Wildlife and Fisheries Sciences at Texas A&M University. This field work would not have been possible without the generosity of numerous landowners. I thank J Yu for permission to use her photographs, and T Lacher Jr for valuable comments and suggestions. n References Please see WebReferences Kelsey D Neam Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX (kelseyneam@tamu.edu) www.frontiersinecology.org