Are the effects of biodiversity on ecosystem functioning being underestimated? – A synthesis on the current consensus of biodiversity importance.
Species extinctions are currently occurring at rates that greatly outpace those predicted from the fossil record1. It has been suggested that a sixth mass extinction (a period of intense species loss, whereby > 75% of species are lost within a geologically short time interval), may be either currently underway or on the near horizon1. This has prompted a surge in studies examining the effect of biodiversity on ecosystem functioning2. However, despite extensive research, the importance of biodiversity for ecosystem functioning, in terms of multifunctionality and compared to other factors of ecosystem change, remain contested and unclear.
The term ecosystem functioning incorporates ecosystem processes carried out by biota (bioturbation, decomposition, etc.), and fluxes of materials and energy (primary production, nutrient cycling, etc.). Bioturbation, for example, is the disturbance of sedimentary deposits by living organisms and plays an important role in sediment oxygen uptake3. Species diversity has long been theorised as a major determinant of ecosystem functioning4, with hundreds of studies, spanning a range of ecosystems5,6,7, demonstrating that high diversity systems are approximately twice as productive as monocultures4.
However, the importance of biodiversity for integrated ecosystem functioning remains unclear due to the majority of experimental analyses focussing on individual functions, as opposed to the many that appear in natural systems8. Thus, ecosystem multifunctionality is currently at the forefront of biodiversity-ecosystem function (BEF) research. Multifunctionality is the ability to maintain multiple ecosystem functions simultaneously9, and it suggests that the effect of biodiversity on ecosystem function becomes increasingly significant as more functions are considered8.
Soil communities, for example, are complex and highly diverse, so focussing BEF research on a singular group of organisms disregards the complex food webs in which soil organisms interact10. Agricultural and land-use intensification has reduced the biodiversity and altered the composition of soil communities, prompting an investigation into its effect on ecosystem functions10. Soil biodiversity loss was found to impair multiple ecosystem functions, such as decomposition and nutrient cycling, with the average response of all measured functions exhibiting a strong positive linear relationship with soil biodiversity10. This implies that biodiversity is critical to highly multifunctional ecosystems and that prior analyses may have significantly underestimated the fundamental importance of biodiversity, by focussing excessively on individual functions or organisms8.
As well as underground, species richness is also positively and significantly related to ecosystem multifunctionality above-ground and under-water9,11. This relationship was observed in drylands and is consistent with experimental results obtained from other terrestrial environments9. The preservation of plant diversity in drylands is crucial to mitigate the negative effects of desertification caused by climate change9. In the marine environment, a meta-analysis revealed that generally, changes to species richness tends to alter the functioning of marine ecosystems, with multiple species treatments enhancing ecosystem function, relative to monocultures11. For example, deep-sea ecosystem functioning has been shown to be exponentially related to biodiversity, across a wide range of deep-sea ecosystems6. Deep-sea ecosystems are the most extensive and represent the largest reservoir of biomass on Earth6, so it is vital to evaluate and understand the consequences of biodiversity loss in this system.
However, the majority of BEF studies have strongly relied upon controlled experiments to formulate their conclusions. For example, the very first BEF experiment – the ‘Ecotron’ – utilised a mesocosm approach, with sixteen chambers of identical environmental conditions and differing biodiversity levels, to determine the effect of biodiversity on primary production12. These experiments have substantially advanced our understanding of the relationship between biodiversity and ecosystem functioning, by revealing the underlying mechanisms of biodiversity dynamics13. Nevertheless, they have been subject to intense criticism14.
The controversy regarding the use of controlled experiments stems from the argument that they do not characterise the complexity of ecosystems, nor the large spatial and temporal scales experienced under natural environmental conditions. Their results are therefore argued not to be truly representative of natural conditions14, however, this view is widely refuted by BEF experts. The criticism that these experiments overestimate the importance of biodiversity in order to justify conservation policies, as argued by Thompson and Starzomski15, has also been largely overstated.
Under controlled experimental conditions, the dominant influence of individual species on ecosystem functioning is largely a consequence of the simplified environments and the single functional response variables considered. Thus, experiments on this level are more likely to have underestimated the importance of biodiversity on ecosystem functioning in natural settings, rather than overestimating it14. The reality is that the experimental evidence for BEF is generally consistent and represents a practical method for the study of biodiversity importance to ecosystem functioning.
Additionally, the effects of biodiversity loss on ecosystem functions, such as productivity and decomposition, are comparable to the effects of many other environmental changes2. For example, an intermediate species loss of 21-40% induced a decrease in primary production of 5-10%, comparable to that of climate warming and ultraviolet radiation. Higher levels of species loss (41-60%) induced effects rivalling those of ozone, acidification and elevated CO22. Thereby, the ecosystem consequences of changes in local biodiversity are as quantitatively significant, if not more significant, as the direct effects of environmental change stressors2; many of which have gained wide media coverage as major international concerns.
It is therefore imperative that the biodiversity of ecosystems be preserved to maintain effective ecosystem functioning. Future requirements primarily consist of improvement to the understanding of biodiversity loss impact, through taking observed experimental BEF relationships and linking ecosystem functions to the provisioning and regulating of ecosystem services16 (ecosystem functions on which human welfare depends17). This, in turn, will increase international interest and concern; therefore, expanding the focus of BEF research to better mimic real-world circumstances, and improve predictions through the development of models that scale experimental results to whole systems16 (Figure 1).
Biodiversity-loss mitigation strategies may also be incorporated into future BEF research, for example, through the use of assisted colonisation18. Assisted colonisation is the planned introduction of taxa to sites beyond their historical distribution range, with the principle that relocating species will help to restore ecosystem processes18. Despite wide discussion of the risks related to this method, including the possibility that the relocated taxa may have detrimental effects on native species19, ecologists have once again underestimated the potential benefits that species introductions may pose for the restoration of ecological functioning. It is therefore regarded that assisted colonisation may be a key adaptation strategy to restore ecological function18, though more research and experimental trials are required to develop a sufficient understanding of the potential consequences, and to confirm this19.
In conclusion, the accumulation of evidence that biodiversity loss will negatively affect ecosystem functioning is indeed a cause for global concern. It is therefore imperative not to overlook biodiversity as an important factor of ecosystem functioning, and thus methods for the mitigation of species loss must be addressed and pursued without delay.
1 Barnosky, A. D. et al. Nature. 471, 51-57 (2011).
2 Hooper, D. U. et al. Nature. 486, 105-109 (2012).
3 Solan, M. et al. Science. 306, 1177-1180 (2004).
4 Tilman, D. et al. Annu. Rev. Ecol. Evol. Syst. 45, 471-493 (2014).
5 Tilman, D. et al. Nature. 379, 718-720 (1996).
6 Danovaro, R. et al. Curr. Biol. 18, 1-8 (2008).
7 Mora, C. et al. PLoS Biol. 9, e10000606 (2011).
8 Lefcheck, J. S. et al. Nat. Commun. 6, 6936 (2015).
9 Maestre, F. T. et al. Science. 335, 214-218 (2012).
10 Wagg, C. et al. PNAS. 111, 5266-5270 (2014).
11 Gamfeldt, L. et al. OIKOS. 124, 252-265 (2015).
12 Naeem, S. et al. Nature. 368, 734-737 (1994).
13 Loreau, M. et al. Science. 294, 804-808 (2001).
14 Duffy, J. E. Front. Ecol. Environ. 7, 437-444 (2009).
15 Thompson, R. & Starzomski, B. M. Biodivers. Conserv. 16, 1359 (2007).
16 Cardinale, B. J. et al. Nature. 486, 59-67 (2012).
17 Luck, G. W. et al. Trends Ecol. Evolut. 18, 331-336 (2003).
18 Lunt, I. D. et al. Biol. Conserv. 157, 172-177 (2013).
19 Ricciardi, A. & Simberloff, D. TREE. 24, 248-253 (2009).