On the move: sloths and their epibionts as model mobile ecosystems - PubMed (original) (raw)

Review

. 2021 Dec;96(6):2638-2660.

doi: 10.1111/brv.12773. Epub 2021 Jul 26.

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Review

On the move: sloths and their epibionts as model mobile ecosystems

Maya Kaup et al. Biol Rev Camb Philos Soc. 2021 Dec.

Abstract

Sloths are unusual mobile ecosystems, containing a high diversity of epibionts living and growing in their fur as they climb slowly through the canopies of tropical forests. These epibionts include poorly studied algae, arthropods, fungi, and bacteria, making sloths likely reservoirs of unexplored biodiversity. This review aims to identify gaps and eliminate misconceptions in our knowledge of sloths and their epibionts, and to identify key questions to stimulate future research into the functions and roles of sloths within a broader ecological and evolutionary context. This review also seeks to position the sloth fur ecosystem as a model for addressing fundamental questions in metacommunity and movement ecology. The conceptual and evidence-based foundation of this review aims to serve as a guide for future hypothesis-driven research into sloths, their microbiota, sloth health and conservation, and the coevolution of symbioses in general.

Keywords: algae; arthropods; epibiont; fungi; fur; hair; microbiome; movement ecology; mutualism; symbiosis.

© 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

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Figures

Fig 1

Fig 1

Phylogeny of sloths and their xenarthran relatives, anteaters and armadillos, with approximate timescales for branches. Dashed lines indicate extinct lineages or species. Main geological periods are shown (P = Pleistocene). Timescales are in millions of years (Mya). Synthesized from Delsuc et al. (2019) and Presslee et al. (2019), with indicated branch point timings being the averages of those reported by these two studies: (1) 33 Mya, (2) 21 Mya, (3) 26 Mya, (4) 31 Mya, (5) 27 Mya, (6) 22 Mya, (7) 24 Mya, (8) 17 Mya, and (9) 6 Mya. Recent molecular phylogenetic data suggests that Bradypus torquatus may be better assigned to a different genus (Scaeopus) and that Bradypus variegatus may represent two distinct species (trans‐Andean and cis‐Andean), although further studies are needed to clarify formal species distinctions (Ruiz‐García et al., 2020).

Fig 2

Fig 2

Distributional range of extant two‐fingered (2F) and three‐fingered (3F) sloth species across Central and South America. Synthesized from data of Chiarello & Plese (2014), Plese & Chiarello (2014), Chiarello & Moraes‐Barros (2014_a_,b), Voirin et al. (2014) and Moraes‐Barros, Chiarello & Plese (2014) available at

https://www.iucnredlist.org/

. The population of trans‐Andean B. variegatus sloths located north and west of the Cordillera Oriental mountain range in Colombia (dashed line) is believed to represent a distinct species (Bradypus ephippiger) although this awaits formal confirmation (Ruiz‐García et al., 2020).

Fig 3

Fig 3

Dry and wet sloth hair. Hair on the back of the hand of (A) a dry Bradypus variegatus (brown‐throated three‐fingered) sloth, and (B) the same hand 10 s after wetting reveals a rapid greening and the presence of otherwise visually cryptic green algae/cyanobacteria.

Fig 4

Fig 4

Scanning electron micrographs of sloth hairs. (A) Bradypus variegatus (brown‐throated three‐fingered sloth) hair at three different stages of development (scale bar = 0.6 mm). The bottom hair is from a young sloth in which transverse cracks are only beginning to develop. The middle hair is from an adult sloth displaying larger cracks. The top hair is from an old sloth and shows deep transverse cracks. (B) Choloepus hoffmanni (Hoffmann's two‐fingered sloth) hair showing longitudinal ribs or grooves, at 6× higher magnification than in A. Photographs reproduced from Aiello (1985) with permission (Smithsonian Institution Press).

Fig 5

Fig 5

Morphology of green algal clusters, presumably of Trichophilus welckeri, found in sloth hair. (A) Trichophilus welckeri ‘fronds’ as described by Weber‐van Bosse (, fig. 15). s, sporangia; e, empty sporangial cells. (B, C) _Trichophilus_‐like alga from a hair of the pygmy three‐fingered sloth, Bradypus pygmaeus. (D) Hair with _Trichophilus_‐like alga from a Hoffmann's two‐fingered sloth, Choloepus hoffmanni. Modified from a figure in Suutari et al. (2010). Scale bars, 20 μm.

Fig 6

Fig 6

Colour and shape similarities of sloths. (A) A female Bradypus variegatus (brown‐throated three‐fingered sloth) with green fur coloration, taken during the wet season; (B) an Azteca ant carton nest that looks similar to a hanging sloth; (C) a dry B. variegatus sloth and (D) a dry Choloepus hoffmanni (Hoffmann's two‐fingered) sloth with similar coloration as the branches, vines, and bark of the trees they inhabit. Photograph of Azteca ant nest by Solar (2014) used with permission under Creative Commons License CC BY‐NC‐SA 2.0.

Fig 7

Fig 7

The sloth‐associated scarab beetle “Uroxys gorgon Arrow, 1933.” (A) Collected live from the fur of a Bradypus variegatus (brown‐throated three‐fingered sloth), and (B) a mounted specimen (Larsen, 2015), used with permission under Creative Commons License CC BY‐NC 3.0.

Fig 8

Fig 8

The sloth moth, Cryptoses choloepi, on a Bradypus variegatus (brown‐throated three‐fingered sloth). (A) Moths often swarm the sloth's face, especially orifices such as the nose and eyes, and (B) appear well camouflaged on the sloth's grey‐brown fur.

Fig 9

Fig 9

Sloths and fungi. (A, B) The back of the heads of two Choloepus hoffmanni (Hoffmann's two‐fingered sloth) with visible growth on the fur of (A) black fungi and (B) algae. (C, D) Facial photographs of (C) a Bradypus variegatus (brown‐throated three‐fingered sloth) with a severe fungal infection that causes scabs of hair to fall off, and (D) a healthy B. variegatus sloth for comparison.

Fig 10

Fig 10

Photographs showing the (A) canopy of a Cecropia obtusifolia tree, (B) mutualistic ants, Azteca constructor, harvesting food bodies from a Cecropia petiole/stalk, (C) Azteca ants attacking an encroaching vine to protect a Cecropia tree, and (D) a brown‐throated three‐fingered sloth, Bradypus variegatus, eating fruit from a Cecropia tree, seemingly unbothered by ants. A, B, and C reproduced from Marting et al. (2018) with permission under Creative Commons License CC BY 4.0.

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