Impact assessment using a formal “BACI” (Before-After-Control-Impact) or “Beyond BACI” sampling design25 was not possible in this study owing to the lack of pre-DSTP benthic community data. We used the geography and bathymetry of the Lihir and Misima study areas to overcome this handicap, selecting stations with differing levels of tailings input and with the potentially confounding effects of water depth closely controlled. In this deep-sea setting, manipulative experiments generating direct cause-and-effect evidence26,27,28 are extremely difficult to perform and impact assessment therefore rests on inference and correlation between infaunal community structure and sediment tailings content. Nevertheless, our results from an active and a closed mine are consistent with each other, with published data on coastal tailings disposal and from analogous large-scale sedimentation events in the deep sea and it is reasonable to conclude that the observed patterns are attributable to the effects of DSTP.

Our results demonstrate clearly that ongoing DSTP at Lihir is associated with greatly reduced infaunal abundance and changes in higher-taxon composition. The scale of impact on metazoan meiofauna and calcareous forams declines with depth (and thus, distance from the tailings outfall) but is still significant down to 1700 m. Macrofauna and organic-walled forams are severely impacted to at least 2000 m. These patterns are consistent with published studies reporting substantial loss (or disappearance) of benthic forams29, metazoan meiofauna30 and macrofauna31,32,33 in coastal sediments exposed to mine tailings deposition. Deep-sea analogues also support this interpretation of the Lihir results. In the Cassidaigne Canyon (French Mediterranean slope) used for long-term disposal of aluminium smelting waste (“red mud”), meio- and macrofaunal densities were much lower at stations in the main canyon axis compared with peripheral stations receiving lower sediment input34. In the South China Sea, deposition of 6–8 cm of ash from the 1991 Mount Pinatubo eruption resulted in mass mortality of benthic forams35. Physical smothering is considered to drive the loss of both macrofauna31,32,33,34 and benthic forams29,35, whose upward mobility is severely curtailed by superficial deposits >2 cm in thickness36. Nevertheless, the thick surface tailings layer at stations L1-L3 was not completely azoic, some metazoan meiofauna always being present. In shallow-water experiments, harpacticoid copepods began to recolonise defaunated tailings in as little as 40 days, with numbers returning to background levels after 97–203 days28. Nematode recolonisation was slower, possibly reflecting the lack of a dispersive larval stage in this phylum. The copepod-dominated meiofauna found at the impacted Lihir stations may therefore be maintained by a continuous input of drifting propagules onto the freshly-deposited tailings.

The effects of DSTP at Lihir are detectable up to ~20 km east of the discharge point and to at least 2000 m water depth, but the full spatial and bathymetric extent of impact remains to be determined by a broader-scale survey. Our results mark the first essential step in mapping the benthic ecological “footprint” of the Lihir mine and for monitoring changes in its extent as tailings discharge continues.

At Misima, metazoan meiofauna, macrofauna and benthic forams all showed a clear contrast between stations with high (M1-M3) and low or no (M4-M6) tailings content. Data for the latter two infaunal groups suggest some recovery in total abundance, but with persistent effects on community structure. Benthic foram communities exposed to mine tailings29 and volcanic ashfall35 show very rapid (<1 year) return to background abundance once sediment deposition has ceased, but remain at low diversity and characterised by a few opportunistic taxa for up to 10 years29. In the Cap Breton Canyon (Bay of Biscay), foram assemblages 6–9 months after turbidite deposition were dominated by species rare or absent in undisturbed open slope sediments37. Low diversity and dominance by two species also characterised foram communities close to the “red mud” outfall in the Cassidaigne Canyon38. In such physically unstable environments the early recolonisation state may persist more or less indefinitely37. Data from coastal26,31,32 and deep-sea34 case studies also suggest recovery of macrofaunal abundance and species richness within three years after the end of tailings deposition, but with sediment instability again having a confounding effect. In a Canadian fjord used for tailings disposal, macrofaunal recovery was disrupted by slope failures and resuspension events, the impacts of which could equal or exceed those of the original tailings deposition39. Recovery rates may also be taxon-specific, with amphipods, for example, reported to be highly sensitive to sediment instability32. Foraminiferan and macrofaunal data from stations M1-M3 3.5 years post-DSTP are therefore consistent with a degree of community recovery (from an impacted state resembling the active DSTP stations east of Lihir), but with the successional process slowed or interrupted by physical disturbance. In this seismically-active region, periodic slumps of accumulated sediment down the steep Bwagaoia Basin slope would be expected and are likely to have generated the disturbed bedforms observed at M1.

Meta-analysis of published case studies shows that trace metals (and other classes of contaminants) reduce the richness and evenness of marine communities40. However, without controlled experiments it can be difficult to separate the effects of chemical toxicity and physical instability in contaminated sediments41. The sensitivity of metazoan meiofauna to porewater copper has been observed in the field30 and confirmed by laboratory bioassays27,42 where abundance and diversity were significantly reduced above a threshold of 50 μg Cu L−1. Porewater copper concentrations at M1, where metazoan meiofauna were extremely sparse, were substantially above this threshold across most of the upper ~4 cm of the sediment column and consistently higher than at stations M3, M4 and M6 (Supplementary Fig. S1a). Values for cadmium, another ecotoxic trace metal, were also much higher at Bwagaoia Basin stations M1 and M3 than outside; lead showed no consistent difference, while dissolved arsenic levels were highest at the low/no tailings stations M4 and M6 (Supplementary Fig. S1b-d). With respect to macrofaunal recovery in tailings-affected sediments, residual contaminants have generally been considered less important than physical stability26,31,32,39. However, 15 years after the end of tailings discharge at the Black Angel mine (Greenland), dominance by opportunistic species at stations above a threshold value (200 mg kg sediment−1) for solid-phase lead was interpreted as evidence for a persistent trace metal contaminant effect43. Results of coastal field studies or laboratory bioassays must be applied with caution to the very different environment of Misima, but they suggest that tailings-derived contaminants may compound the effects of physical disturbance on rates of community recovery in the Bwagaoia Basin depocentre.

For all infaunal taxa sampled, station M4, where geochemical evidence indicated some tailings input, grouped with the tailings-free stations M5 and M6 rather than with the higher-tailings stations in the Bwagaoia Basin (M1-M3). This suggests the possible existence of a threshold level of tailings input required to drive detectable changes in infaunal communities. Future work should aim to test this hypothesis and identify any key sediment parameters involved (e.g. particulate deposition or ecotoxic metal content).

The level of taxonomic resolution needed to detect environmental impacts has been much debated, with recent literature focusing on the application of “Taxonomic Sufficiency” (TS)44 (identification to higher-taxon level only) to benthic faunal samples. Several coastal and shelf studies support community analysis at Family, Order or Class level45,46,47, while others caution against the potential loss of information in comparison with full species-level identification48,49. In the deep sea, species-level identification is often difficult and the environmental tolerances of individual species largely unknown, making the efficacy (or otherwise) of TS a particularly important issue50. Our results show that significant effects of DSTP are apparent at Family (Polychaeta) or higher-taxon level (Phylum, Class or Order for other faunal components). The benthic “footprint” of the Deepwater Horizon oil spill has recently been mapped from samples analysed at a similar level of taxonomic resolution51, suggesting that TS may be an effective tool for detection of large-scale pollutant impacts in the deep sea.

With interest in commercial seabed mining growing rapidly52,53 and continuing use of DSTP in developing nations, a better understanding of the impacts of large-scale anthropogenic disturbance on deep-sea benthic ecosystems is an essential step towards effective stewardship of these environments54,55. Our results show that significant community effects of DSTP are apparent even at a coarse level of taxonomic resolution and provide the basis for future monitoring of recovery rates in impacted deep-sea sediments.