Arboreal herbivory is rare among mammals. The few species with this lifestyle possess unique adaptions to overcome size-related constraints on nutritional energetics. Sloths are folivores that spend most of their time resting or eating in the forest canopy. A three-toed sloth will, however, descend its tree weekly to defecate, which is risky, energetically costly and, until now, inexplicable. We hypothesized that this behaviour sustains an ecosystem in the fur of sloths, which confers cryptic nutritional benefits to sloths. We found that the more specialized three-toed sloths harboured more phoretic moths, greater concentrations of inorganic nitrogen and higher algal biomass than the generalist two-toed sloths. Moth density was positively related to inorganic nitrogen concentration and algal biomass in the fur. We discovered that sloths consumed algae from their fur, which was highly digestible and lipid-rich. By descending a tree to defecate, sloths transport moths to their oviposition sites in sloth dung, which facilitates moth colonization of sloth fur. Moths are portals for nutrients, increasing nitrogen levels in sloth fur, which fuels algal growth. Sloths consume these algae-gardens, presumably to augment their limited diet. These linked mutualisms between moths, sloths and algae appear to aid the sloth in overcoming a highly constrained lifestyle.
Our data suggest that a series of linked mutualisms occurs between sloths, moths and algae (figure 3). Specifically, sloths appear to promote pyralid moth infestation by descending to the base of the tree to defecate and assisting the life cycle of moths [16,19], even in the face of heightened predation risk and significant energetic costs [12]. Moths in the fur of sloths, in turn, act as a portal for nutrients, linking the ecosystem within sloth fur to the surrounding environment. Within the sloth’s ecosystem, fungi are common [14] and we postulate that moths are being mineralized by this abundant community of decomposers. Alternatively, moths could be directly transporting organic waste from the dung pile to the fur. Regardless of the mechanism, increasing moth biomass increased inorganic nitrogen levels, which appeared to augment the growth of algal communities on sloth fur. Sloths consume algae, presumably via autogrooming, for nutritional benefit. Our VFA and compositional data suggest that algae on the fur of sloths are especially rich in digestible carbohydrates and lipids. In short, we propose that sloths are grazing the ‘algae-gardens’ they have derived from a three-way mutualism
Postulated linked mutualisms (+) among sloths, moths and algae: (a) sloths descend their tree to defecate, and deliver gravid female sloth moths (+) to oviposition sites in their dung; (b) larval moths are copraphagous and as adults seek sloths in the canopy; (c) moths represent portals for nutrients, and via decomposition and mineralization by detritivores increase inorganic nitrogen levels in sloth fur, which fuels algal (+) growth, and (d) sloths (+) then consume these algae-gardens, presumably to augment their limited diet.
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In addition to providing nutrition, it is possible that algal cultivation enhances sloth survival via camouflage reducing mortality from aerial predators [13]. These two ultimate mechanisms of algal cultivation are not mutually exclusive, but we speculate that the camouflage provided by algae is secondary to nutritional supplementation. First, the advantage of increased concealment within the canopy would have to be very strong to offset the high predation rates encountered when descending the tree to defecate, yet the algae–sloth symbiosis appears unrelated to the distribution of the primary aerial predator of sloths, the harpy eagle (Harpia harpyja). Second, previously constructed energy budgets for three-toed sloths suggests that daily energy expenditure can actually exceed intake [3], which might be from computational error [10] or because a cryptic food item, like algae, has been missed. An unaccounted food source would help to explain why three-toed sloths are difficult to keep well nourished in sanitized captive facilities [33]. Finally, the mutualisms associated with the two-toed sloth, which is the more vagile and less restricted forager, were more equivocal. Two-toed sloths possessed significantly fewer moths, and less inorganic nitrogen and algae, even though they presumably face similar predation pressure in the forest canopy. Indeed, two- and three-toed sloths from the same geographical area harbour phylogenetically distinct groups of Trichophilus spp., suggesting a long coevolutionary relationship between sloths and their algal community [14].
Whatever advantage algae confer to sloths, this complex syndrome of mutualisms—among moths, sloths and algae—appears to have locked three-toed sloths into an evolutionary trade-off that requires it to face increased predation risk in order to preserve linked mutualisms. Supporting the life cycle of moths may explain why three-toed sloths possess a high fidelity to only a few modal trees, and a marked willingness to defecate in what is, for a sloth, the most dangerous part of the forest. These mutualisms could also contribute to the sloth’s success as an arboreal herbivore, one of the most constrained and rarest foraging strategies among vertebrates [1]. Our study is the first to suggest that unique ecological interactions, in addition to physiological and anatomical adaptations, may foster an arboreal and herbivorous lifestyle; future experiments that test the mechanistic linkages and putative benefits of the interactions between sloths, moths and algae will help tease apart the exact nature of these linkages.