Biosphere Integrity

Myriad interactions with the geosphere make the biosphere a constitutional component of Earth system and a major factor in regulating its state. The planetary functioning of the biosphere ultimately rests on its genetic diversity, inherited from natural selection not only during its dynamic history of coevolution with the geosphere but also on its functional role in regulating the state of Earth system. Genetic diversity and planetary function, each measured through suitable proxies, are therefore the two dimensions that form the basis of a planetary boundary for biosphere integrity. As applied here, “integrity” does not imply an absence of biosphere change but, rather, change that preserves the overall dynamic and adaptive character of the biosphere.

Rockström et al. (1) defined the planetary boundary for change in genetic diversity as the maximum extinction rate compatible with preserving the genetic basis of the biosphere’s ecological complexity. We retain the boundary level of <10 E/MSY (extinctions per million species-years). The extinction rate control variable is challenging to apply in operational contexts, but data and methods for directly assessing the genetic diversity component of biosphere integrity are emerging [(23) and the Supplementary Materials]. Although the baseline rate of extinctions (and of new species’ evolution) is both highly variable and difficult to quantify with confidence through geological time, the current rate of species extinctions is estimated to be at least tens to hundreds of times higher than the average rate over the past 10 million years and is accelerating (24). We conservatively set the current value for the extinction rate at >100 E/MSY (24–26). Of an estimated 8 million plant and animal species, around 1 million are threatened with extinction (16), and over 10% of genetic diversity of plants and animals may have been lost over the past 150 years (23). Thus, the genetic component of the biosphere integrity boundary is markedly exceeded (Fig. 1 and Table 1).

Previously, Steffen et al. (2) proposed using the Biodiversity Intactness Index (BII) (27), an empirically based metric of human impacts on population abundances, as an interim proxy for functional biosphere integrity. It was noted, however, that the link of BII to Earth system functions remains poorly understood and BII cannot be directly linked to the planetary biogeochemical and energy flows relevant for establishing Earth system state. In addition, BII relies on expert elicitation to estimate temporal changes in species abundances/distributions, and this knowledge is not readily available for many regions, including the oceans. Martin et al. (28) have also recently suggested that BII only partially reflects human impacts on Earth system.

We therefore now replace this metric with a computable proxy for photosynthetic energy and materials flow into the biosphere (29), i.e., net primary production (NPP), and define the functional component of the biosphere integrity boundary as a limit to the human appropriation of the biosphere's NPP (HANPP) as a fraction of its Holocene NPP. NPP is fundamental for both ecosystems and human societies as it supports their maintenance, reproduction, differentiation, networking, and growth. Biomes depend on the energy flow associated with NPP to maintain their planetary ecological functions as integral parts of Earth system. NPP-based energy flows into human societies should therefore not substantially compromise the energy flow to the biosphere (30). The proxy complements the diversity-based dimensions of biosphere integrity, covered by the genetic component, which captures the importance of variability in living organisms for the functioning of ecosystems. The suitability of NPP and HANPP for defining a planetary boundary has previously been discussed by Running (31) and Haberl et al. (32).

We determine the terrestrial biosphere’s Holocene NPP to have been 55.9 Gt of C year−1 (2σ) and exceedingly stable, varying by not more than ±1.1 Gt of C year−1 despite regional variations in time (see the Supplementary Materials). Our model analyses suggest that NPP still had a Holocene-like level in 1700 (56.2 Gt of C year−1 for potential natural vegetation and 54.7 Gt of C year−1 when land use is taken into account). By 2020, potential natural NPP would have risen to 71.4 Gt of C year−1 because of carbon fertilization, a disequilibrium response of terrestrial plant physiology to anthropogenically increasing CO2 concentration in the atmosphere, whereas actual NPP was 65.8 Gt of C year−1 due to the NPP-reducing effects of global land-use (see the Supplementary Materials).

HANPP designates both the harvesting and the elimination or alteration (mostly reduction) of potential natural NPP (32), mainly through agriculture, silviculture, and grazing. Terrestrial HANPP can be estimated both as a fraction of potential natural NPP [15.7% in 1950 and 23.5% in 2020; inferred from (33) and the Supplementary Materials] and of Holocene mean NPP (30% or 16.8 Gt of C year−1 in 2020; see the Supplementary Materials). We argue that an NPP-based planetary boundary limiting HANPP should be set in relation to preindustrial Holocene mean NPP and not the current potential natural NPP. This is because the global increase in NPP due to anthropogenic carbon fertilization constitutes a resilience response of Earth system that dampens the magnitude of anthropogenic warming. Hence, the NPP contribution to a carbon sink associated with CO2 fertilization should be protected and sustained rather than considered as being available for harvesting. Examples of large land areas under human use with declining carbon sinks, some even turning into carbon sources, i.e., due to human overexploitation of biomass, are already being observed, for example, in some Amazonian regions (34) and northern European forests.

As NPP is the basis for the energy and materials flow that underpins the biosphere’s functioning (30), we argue that today’s planetary-scale impact of HANPP is reflected in the observation that major indicators of the state of the biosphere show large and worrisome declines in recent decades (16). This suggests that current HANPP is well beyond a precautionary planetary boundary aiming to safeguard the functional integrity of the biosphere and likely already into the high-risk zone. We therefore provisionally set the functional component of the biosphere integrity planetary boundary at human appropriation of 10% of preindustrial Holocene mean NPP, shifting into the zone of high risk at 20%. The boundary thus defined was transgressed in the late 19th century, a time of considerable acceleration in land use globally (35) with strong impacts on species (27), already leading to early concerns about the effects of this large-scale land transformation.

Thus, while the climate warming problem became evident in the 1980s, problems arising in functional biosphere integrity due to human land use began a century earlier. Since the 1960s, growth in global population and consumption further accelerated land use, driving the system further into the zone of increasing risk. HANPP has always sustained humanity’s need for food, fiber, and fodder, and this will continue to be the case in the future, as well as for sustainable societies. The NPP required to support future societies must, however, increasingly be generated through additional production of NPP above the Holocene baseline, not including the NPP generated for biology-based carbon sinks. Feeding 10 billion people, for example, is theoretically possible within planetary boundaries but requires a number of far-reaching transformations to improve the impacts of production and regulate demand (36).

To develop a deeper foundation for the HANPP-based planetary boundary for functional biosphere integrity, we need an improved understanding of how ecological dynamics generate the functions of the biosphere in Earth system. Analysis of NPP should be spatially explicit and augmented by computable metrics of ecological destabilization due to climate and land use pressures, e.g., a metric of biogeochemical disruption (37).

HANPP can also be quantified for marine systems. About two-thirds of the ocean area where HANPP is >10% is found above the shallow shelf areas (38) where ecosystems are most intensely exploited. Regionally, fish catches exceed thresholds of sustainable exploitation (39). However, in contrast to land, where most HANPP occurs in the form of plant material, i.e., at the lowest trophic level, HANPP in the ocean tends to take place at higher trophic levels. This means that while HANPP reduces the absolute amount of energy available to higher trophic levels on land, much of the energy fixed through NPP is used in marine ecosystems before HANPP occurs. When the abundance of organisms at the highest trophic levels is reduced, changes in marine ecosystem structure may change energy flow in these ecosystems (40). Thus, in the marine realm, HANPP likely changes the flows rather than the amount of energy available. More information about the impacts of HANPP in the marine realm is necessary to integrate consideration of the marine systems in the functional biosphere integrity planetary boundary.