Global nutrient transport in a world of giants

Abstract

The past was a world of giants, with abundant whales in the sea and large animals roaming the land. However, that world came to an end following massive late-Quaternary megafauna extinctions on land and widespread population reductions in great whale populations over the past few centuries. These losses are likely to have had important consequences for broad-scale nutrient cycling, because recent literature suggests that large animals disproportionately drive nutrient movement. We estimate that the capacity of animals to move nutrients away from concentration patches has decreased to about 8% of the preextinction value on land and about 5% of historic values in oceans. For phosphorus (P), a key nutrient, upward movement in the ocean by marine mammals is about 23% of its former capacity (previously about 340 million kg of P per year). Movements by seabirds and anadromous fish provide important transfer of nutrients from the sea to land, totalling ∼150 million kg of P per year globally in the past, a transfer that has declined to less than 4% of this value as a result of the decimation of seabird colonies and anadromous fish populations. We propose that in the past, marine mammals, seabirds, anadromous fish, and terrestrial animals likely formed an interlinked system recycling nutrients from the ocean depths to the continental interiors, with marine mammals moving nutrients from the deep sea to surface waters, seabirds and anadromous fish moving nutrients from the ocean to land, and large animals moving nutrients away from hotspots into the continental interior.

Keywords: anadromous fish; biogeochemical cycling; extinctions; megafauna; whales.

Fig. 1.

Lateral nutrient distribution capacity (km²⋅y⁻¹) by terrestrial mammals. Lateral diffusion capacity (Φ; Eq. 1) of nutrients by all mammals as it would have been without the end-Pleistocene and Holocene megafauna extinctions and extirpations (Top), as it is currently (Middle), and as the percentage of the original value (Bottom).

Fig. 2.

Horizontal and vertical nutrient distribution capacity by great whales. Lateral movement capacity (Φ, km²⋅y⁻¹; Eq. 1) by great whales (listed in SI Appendix, Table 3) for past whale densities before widespread human hunting (A), current whale densities (B), and the percentage of the original value (i.e., current values divided by past values) (C). Vertical movement of nutrients by marine mammals (listed in SI Appendix, Table 4), log₁₀ kilograms of P per square kilometer per year (kg⋅Pkm⁻²⋅y⁻¹), for past marine mammal densities before widespread human hunting (D), current marine mammal densities (E), and the percentage of the original value (F).

Fig. 3.

Nutrient movement of P from ocean to land by anadromous fish and seabirds. (Top) Global estimates of historical P (kg⋅km⁻²⋅y⁻¹) moved by the bodies of anadromous fish in the past. Nutrient movement by anadromous fish may be underestimated in tropical regions due to a lack of data. (Bottom) Global estimates of guano movement to coastal land by all seabirds, assuming 20% of the guano arrives on land (measured in kg⋅km⁻²⋅y⁻¹) and assuming theoretical population densities of seabirds based on body mass population density scaling relationships (43).

Fig. 4.

Potential interlinked system of recycling nutrients. The diagram shows a potential route of nutrient transport of the planet in the past. Red arrows show the estimated fluxes or diffusion capacity of nutrients listed in Table 1. Grey animals represent extinct or reduced population densities of animals.