Physico-chemical characteristics of the study site and whale carcass description

The whale fall was located ca. 700 km from the Brazilian coast at the base of the São Paulo Ridge (SPR; 28° 31.1191′ S, 41° 39.4097′ W) at a depth of 4204 m (Fig. 1). The surrounding area was characterized by a thin layer (<20 cm) of sediments overlying basaltic rocks. During our study, the area was under the influence of the Antarctic Bottom Water (AABW)37 with a temperature of 0.4 °C and salinity 34.7.

Figure 1 Location of the whale carcass found at the base of São Paulo Ridge at 4204 m depth. The map was created using the QGIS software, bathymetric data from CleanTOPO2 (http://www.shadedrelief.com/cleantopo2/index.html) and Word borders from Thematic Mapping (http://thematicmapping.org/downloads/world_borders.php). QGIS Development Team, 2015. QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org. The World Borders Dataset and the data obtained from the QGIS Open Source Geospatial Foundation Project is licensed under the Attribution-Share-Alike 3.0 Unported license. The license terms can be found on the following link: http://creativecommons.org/licenses/by-sa/3.0/. Full size image

Mitochondrial COI analysis revealed that the carcass belonged to an Antarctic Minke whale (Balaenoptera bonaerensis) (99% identity). The sequence was deposited in the DNA Databank of Japan (DDBJ) under the accession number LC106302. This partial carcass was composed of nine small vertebrae, seven of which were standing side by side. Among those, five vertebrae were loosely joined by intervertebral discs (vertebrae 1–5) (Fig. 2). Additionally, five intervertebral discs were scattered around the skeleton. No soft tissues were present on the bones, which were all exposed to the surrounding water (i.e. not covered by sediment). All vertebrae were similar in shape and dimensions (ca. 11.5 cm in diameter) and their anatomical characteristics suggest they belong to the caudal portion of the animal. The sediment underneath bones and discs was dark in color suggesting anoxia.

Figure 2 Partial Antarctic Minke whale skeleton (Balaenoptera bonaerensis) found at 4204 m in the Southwest Atlantic Ocean using the manned submersible Shinkai 6500. (A) Caudal vertebrae lying on a thin layer of fine sediment over basaltic rocks; (B) Schematic view of the whale skeleton reconstructed from Shinkai 6500 videos. The nine vertebrae are numbered and shown in pale yellow color, while the round intervertebral discs are darker. Vertebrae were numbered from the posterior end of the animal towards the head. Full size image

Qualitative and quantitative analysis of the macrofauna assemblage and species distributions

Only epifaunal organisms larger than ca. 5 mm could be identified and counted in videos. Five phyla were recovered from the study area comprising at least 41 species (Table 1). Nematoda occurred in large numbers both inside bones and in the surrounding sediments and may be represented by more than one species. Nematodes are currently being quantified and will be treated in detail in a later publication.

Table 1 Species collected at the SW Atlantic whale fall site at 4204 m depth. Full size table

Polychaetes were the most speciose taxon on both whale bones and soft sediments, with at least 28 species (≈68%), most of which are probably new to science. Among these was a new species of the bone-eating worm Osedax (Fig. 3C,D). We found at least eight morphotypes of the dorvilleid Ophryotrocha and the new species Capitella iatapiuna38 boring into the bones, with the latter also found inhabiting the surrounding sediment sampled with a slurp gun. Three species of polynoid polychaetes, indistinguishable in video analyses, occurred on the surface of bones and sediments (Figs 3E and 4H), with a higher abundance on the former. Interestingly, antagonistic behavior could be observed in videos, where two polynoids were fighting, possibly for space or food resources (see supplemental video material). Five species of Hesionidae (Hesiocaeca sp. nov., Microphthalmus sp. nov., Pleijelius sp. nov. 1 and 2 and Vrijenhoekia sp. nov.) (Fig. 4I) and two species of cirratulids (Raphidrilus and Tharyx) were also present in both sediment and bone, except for both species of Pleijelius which were found only on bones. Another important species occurring in bones was the chrysopetalid Vigtorniella.

Figure 3 Distribution of epifauna on the whale fall and surrounding sediments and rocks. A) General view of the SW Atlantic whale carcass vertebrae 1–7. Note the abundant fauna and the bacterial mats on vertebrae 1–5. A dark echinoid (Echinoidea sp. 1) can be seen on top of vertebra 2; (B) Black basaltic rocks around the whale fall were heavily colonized by dense carpets of anemones (arrow) (up to 10 ind. cm−2). The large gastropod Rubyspira sp. nov. lies behind the red palps of Osedax sp. nov. Note also the small unidentified gastropods attached to the bone; (C) Red palps and gelatinous tubes of several Osedax sp. nov. in vertebra 8. Note the ampharetid polychaete tubes (arrow) and the bone degraded area (arrowhead); (D) Clusters of Osedax sp. nov. in vertebrae 6 and 7. On the surrounding sediment, Rubyspira sp. nov. and a tube of an ampharetid polychaete (arrow). The small lysianassoid amphipod Stephonix sp. lies on the top of the bone (arrowhead); (E) Dense bacterial mats covering vertebrae 2 and 3. Here we can see the small and the large Munidopsis and a polynoid polychaete (arrow); (F) The eyeless nereid polychaete Neanthes sp. nov. climbing the surface of vertebra 6 (arrow). Full size image

Figure 4 Some of the most abundant organisms collected at the 4204 m depth whale fall in the São Paulo Ridge, Southwest Atlantic Ocean. (A) Unidentified sea anemone inhabiting the rocks surrounding the whale skeleton; (B) Large Munidopsis sp.; (C) The amphipod Stephonix sp.; (D) Rubyspira sp. nov.; (E) Osedax sp. nov.; (F) Neanthes sp. nov.; (G) cf. Grassleia sp.; (H) Bathykurila cf. guaymasensis; (I) Vrijenhoekia sp. nov. Full size image

Some polychaetes were found exclusively in sediments surrounding the bones. Among them, one species of Ampharetidae resembling the genus Grassleia (Figs 3C,D and 4G) and a new species of eyeless nereid from the genus Neanthes were abundant (Figs 3F and 4F). Ampharetids dwelt in tubes that were widespread in sediments close to the bones and were only less abundant in videos than Osedax sp. nov. (Table 1) (Fig. 3C,D). Neanthes sp. nov. could not be counted in videos, however it was observed in videos in the anoxic sediment under bones and intervertebral discs coming out the sediment and climbing the bones, without totally leaving its gallery of burrows (Fig. 3F) (supplemental video material).

Among mollusks, a new species of the abyssochrysoid gastropod Rubyspira was present in large numbers (Figs 3B,D,F and 4D) and individuals were quite large in size, attaining up to 3–4 cm in length. The other gastropod was a small species found on the surface of bones (Fig. 3B). Preliminary molecular data place this small gastropod in the family Raphitomidae (Conoidea). Around the skeleton we also found many large empty shells of Rubyspira. No empty shells of the small unidentified gastropod were registered.

Seven species of crustaceans occurred on bones and surrounding sediments (Table 1), including a species of copepod parasitic on Osedax. Munidopsis spp. were found in large numbers being widely distributed up to 1 m away from the carcass (Figs 2, 3E and 4B). We found two morphotypes of Munidopsis, one large and one small, which probably represent different species. A total of 295 individuals of both species were counted in videos (Table 1) and observations suggest these organisms feed on bacterial mats (supplemental video material). However, some of the galatheid crabs were also seen processing sediments in their mouthparts. One ovigerous female of the large morphotype was collected, which suggests that at least one of the galatheid species is reproducing on site. The amphipod Stephonix sp. (Figs 3D and 4C) occurred mainly on bones, frequently coming out of the bones or entering into cracks and holes in degraded areas of bones probably produced by Osedax activity (supplemental video material).

A small species of anemone (polyps ca. 1–2 mm in size) was observed forming extensive carpets of thousands of polyps on rocks around the carcass (Figs 3B and 4A). It was probably the most abundant epifaunal organism, with photographs suggesting a density of ca. 10 ind. cm−2. However, these anemones could not be counted since they could not be resolved in video analyses due to their small size. This anemone was not observed on rocks far from bones.