Recently in How perfect are natural ecosystems? Category

In the comments to a recent post, Timothy Crews writes:

"The reason Denison cited the Vitousek and Reniers model in the first place was to point out that late successional ecosystems might lose nutrients more than earlier successional ecosystems. But given that agriculture involves removal of moderate to large amounts of biomass in the harvest, there is good reason to believe that perennial agroecosystems would never reach the mature (and leaky) equilibrium stage of succession, but instead would be arrested in the aggrading biomass or nutrient sink stage indefinitely (where biomass production exceeds total respiration)."

This seems plausible. But if we have to intervene, by harvesting the right amounts at the right time, to keep further succession from increasing nutrient losses, that supports my main point:

"succession does not improve ecosystem function consistently enough that we can safely copy the overall organization of even late-successional ecosystems without extensive testing."

On the other hand, it's great if the intervention needed is something we want to do anyway.

Succession, predator-prey interactions, nutrient transformations by soil microbes... each of these ecological processes can be beneficial, from an agricultural perspective, but not always. So let's study them in nature and in agriculture, then apply what we learn, rather than blindly copying what we see in nature.

I'm using "nature" here as shorthand for "ecosystems with relatively little active management by humans." OK, Clem?

Also keep in mind that nutrient retention is only one of agriculture's goals. Its main goal is nutrient export as grain, milk, etc. Many natural ecosystems have demonstrated sustainability, in the absence of significant nutrient export. How would they do if we start harvesting as much food as we do from agricultural ecosystems? Could they export the same amount of food over decades, with fewer inputs? Any data?

In a guest post, Timothy Crews quotes two representative statements from my book in which I argue that (in contrast to natural selection's improvement of individual adaptations) neither natural selection nor other natural processes have improved the overall organization of natural ecosystems over millennia. My doubts about "other natural processes" were based on actual data comparing the productivity and stability of natural and managed ecosystems. Dr. Crews argues that shorter-term ecological processes, specifically succession, may improve "ecosystem function with respect to agricultural goals." He doesn't seem to be claiming longer-term improvements, such as succession improving ecosystems more today than it did millions of years ago, which would be analogous to the longer-term improvement of individual adaptations by natural selection.

I don't doubt that some successional changes in some ecosystems qualify as improvements by criteria relevant to agriculture. So I agree that agriculture might "benefit from studies of niche complementarity" etc. As I wrote on page 1:

"Once we drop the assumption of perfection, however, we can learn much from studying natural communities."

"The assumption of perfection" may be an exaggeration of the viewpoint I intended to criticize. I could rephrase as "Once we drop the assumption that there are ecological processes that consistently improve the overall organization of natural ecosystems in ways that would make it safe for agriculture to copy their organization without first testing all the effects of that organization", but that seemed a bit lengthy for page 1.

But how consistently do successional processes improve productivity, stability, nutrient retention, etc.? If there's a good recent review of this question, I'd appreciate hearing about it. The papers I've found do not support the hypothesis that these measures of ecosystem performance consistently improve with succession.

Gower et al.(Gower et al. 1996) analyzed 13 datasets for forests around the world and reported that "Aboveground net primary production (ANPP) commonly reaches a maximum in young forest stands and decreases by O-76% as stands mature." In agriculture, productivity is arguably our most-important criterion, even for environmentalists, as it reduces the amount of land needed to grow a given amount of food. But other measures of performance are also important.

Crews' guest post emphasizes nutrient retention. Vitousek and Reiners (Vitousek and Reiners 1975) presented data compared nitrate loss in streams from younger versus older forests. The older forests lost more nitrate. They also discussed similar data from other forests. Similarly, Lamb (Lamb 1980) found higher nitrate levels in soils of older rather than younger tropical rainforests.

Comparisons among ecosystems are complicated by the possibility of differences unrelated to succession. The closest thing I know to a controlled comparison is that of Wardle et al.(Wardle et al. 1997) They compared islands whose differences in successional stage depended on how recently they had been struck by lightning and burned. This depended mostly on their size. Species diversity was greatest on islands in later successional stages, but "ecosystem process rates were lowest on those islands," perhaps because microbial biomass was greatest at early successional stages. The effects of succession on overall productivity and stability were apparently not measured, unfortunately.

Until I see some data to the contrary -- more than an isolated example or two -- I conclude that succession does not improve ecosystem function consistently enough that we can safely copy the overall organization of even late-successional ecosystems without extensive testing.

References

Gower, S. T., R. E. McMurtrie, and D. Murty. 1996. Aboveground net primary production decline with stand age: potential causes. Trends in Ecology & Evolution 11:378-382.

Lamb, D. 1980. Soil nitrogen mineralisation in a secondary rainforest succession. Oecologia 47:257-263.

Vitousek, P. M., and W. A. Reiners. 1975. Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25:376-381.

Wardle, D. A., O. Zackrisson, G. Hornberg, and C. Gallet. 1997. The influence of island area on ecosystem properties. Science 277:1296-1299.

I don't promise to post everything people send me, but Timothy Crews (of the Land Institute) has obviously put a lot of thought into critiquing one of the main points in my book. I disagree with many of his conclusions and will respond via comments or another post, but here's what he wrote:

The following two quotes illustrate one of the most central, important and repeated points that R. Ford Dennison makes in his book Darwinian Agriculture.

p. 8 Natural selection "has bequeathed many sophisticated adaptations to individual plants and animals, but it has not consistently improved the overall organization of the natural communities where they live." The available evidence suggests that no other natural process has optimized natural communities either.(italics mine)

p. 43 "Some landscape-scale patterns in natural ecosystems have demonstrated their sustainability by persisting for millennia. However, only individual adaptations have been tested by competition among plants or animals with alternative adaptations. ...So ideas inspired by landscape-level patterns of even ancient ecosystems will require more testing, relative to ideas inspired by the competitively tested individual adaptations of wild species."

Contrary to Denison's evaluation of the available evidence, I argue that there are natural processes other than natural selection that "improve" upon native ecosystem function with respect to agricultural goals. In recent decades, ecologists have worked to understand "assembly rules" to clarify what we know and don't know about the forces that shape ecological communities (Diamond 1975, Weiher and Keddy 1999). This topic has received a lot of attention in recent years, and is complex and contentious (HilleRisLambers et al. 2012), and no one suggests that there are hard and fast "rules". But many would agree on some processes that are not natural selection, which occur predictably and consistently at the aggregate community level, and, I will argue, result in attributes that are worthy of consideration to improve agriculture.

The gradual development of niche partitioning in plant community development is a good example. Early in primary or secondary succession, when species are colonizing a new parent material or a recently disturbed site, it is common for a few (usually annual) plant species to establish and dominate the community. Whatever the composition of the initial community, propagules of new species will arrive and become established to the extent that unused soil and light resources remain, or the new species can appropriate resources better than already established ones. This process generally results in species turnover, or succession, and perennial growth forms almost always overtake annual forms. With time,later successional plant communities are commonly made up of species with differentiated niches that utilize slightly to largely different pools of resources in time and/or space.

The remarkably different plant co-existing growth forms that can be found in the desert grass and shrub lands of southern Arizona illustrate resource partitioning in a late successional community. Extremely deep rooted mesquite trees with C3 photosynthesis are found growing in close proximity to shallow rooted perennial grasses, like Bouteloua gracilis, that employ C4 photosynthesis, which can be found near cacti such as cholla, that maintain CAM photosynthetic pathways. Burgess (1995) described three functional categories that encompass the three species I mention here, 1) extensive exploiters (mesquite)--deeply rooted woody plants that exploit deep water resources, typically recharged by winter precipitation, 2) intensive exploiters(Bouteloua gracilis)--shallow rooted grasses and shrubs that rely on erratic summer rainfall and can persist for long durations in a drought-induced dormancy, 3) water storers (cholla)--cacti and succulents that maintain relatively low leaf surface area, tend to lose out to intensive exploiters in competition for water, but re-hydrate effectively during moderate to high rainfall events, and transpire water slowly. Ecologists believe the plants with these different water uptake strategies experience less head to head competition, and therefore have a greater likelihood of co-existing than groups of species from a common functional group. A similar diversity of resource use strategies have been found to exist for other resource axes, such as soil nitrogen (Weigelt et al. 2005, Kahmen et al. 2006). An ecosystem-level outcome of greater niche partitioning through succession is that plant resources (nutrients, water, light) are more completely utilized. More complete resource utilization should, ceteris paribus, result in greater productivity, and, importantly, less leakage or loss of water and nutrients from the ecosystem.

It is also important to point out that community composition is never static-- the environment is constantly changing, and new species are constantly being introduced from the outside. New arrivals of potential community members effectively "test" the resource uptake efficiency of the extant community. In some cases, the new arrival may be able to go deeper for water, or persist at a lower soil matric potential during drought. Such advantages can lead to species replacement, and a more productive and resource efficient community as a whole.

How might agriculture benefit from studies of niche complementarity or resource partitioning in native plant communities? The somewhat obvious but nevertheless important idea is one that has interested agroecologists for some time--the deployment of diversity in space through polycultures. While Denison seems to prefer the deployment of diversity in time through rotations, the potential to substantially improve uptake of soil resources, increase productivity and reduce vulnerability to weed invasions through crop mixtures in space is worthy of further attention. Even more interesting is the potential to improve on these ecological functions when the perennial growth form that is dominant in native systems is included in the polycultures.

In Darwinian Agriculture, Dennison identifies numerous significant shortcomings of modern agriculture. Many, if not most of them involve ecological functions above the species level, such as leakiness of nitrogen or soil erosion, and thus are not easily addressed by improvements in the performance of individual annual crops. Does it make sense to look at native community and ecosystem attributes to inform how we might make improvements? Absolutely. Especially when the functioning of native ecosystems appears to be superior with respect to attributes of interest (e.g., nutrient retention), and there are no alternative human constructed systems that provide models superior to the native systems from which to learn. If native ecosystem patterns and processes can be improved on with respect to desirable agricultural goals, then all the better--those projects are worthy of funding.

References
Burgess, T. 1995.Desert grassland, mixed shrub savanna, shrub steppe, or semidesert scrub?pp. 31-67 In: The Desert Grassland. M.P. McClaran& T.R. Van Devender (eds). University of Arizona Press, Tucson, Arizona
Diamond, J. 1975.Assembly of species communities. Pp. 342-444 In: Ecology and Evolution of Communities. M.L. Cody & J.M. Diamond (eds). Harvard University Press, Cambridge, Mass.
HilleRisLambers, J. P.B. Adler, W.S. Harpole, J.M. Levine & M.M. Mayfield. 2012. Rethinking community assembly through the lens of coexistence theory. Annual Review of Ecology, Evolution, and Systematics 43:227-248
Kahmen, A., C. Renker, S. B. Unsicker& N. Buchmann. 2006. Niche complementarity for nitrogen: An explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244-1255
Weigelt, A. R. Bol& R. Bardgett. 2005. Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627-635
Weiher, E. & P. Keddy. 2001. Ecological Assembly Rules: Perspectives, Advances, Retreats. Cambridge University Press, Cambridge, UK.

Still no reviews of my book on Amazon (except in the UK), but two more in leading scientific journals.

The first review is in Evolution, and written by Duur Aanen, from the University of Wageningen. He's best known for his research on "agriculture" by nonhuman species, particularly fungus-growing termites, including mechanisms that limit the evolutionary success of "cheater" strains of fungi. I also liked his recent commentary on weeding vs. intercropping in the algal gardens of damselfish.

Professor Aanen's review summarizes and apparently accepts the main arguments in my book, only faulting me for not citing recent work by Piter Bijma, relevant to my suggestion that improving the collective performance of fields and flocks will often require reversing the effects of past individual selection. Looks like his work might stretch my math ability and that of some of my readers.

The second review is by Peter Thrall, of CSIRO, and published in Evolutionary Applications. He has published extensively on coevolution of legumes and rhizobia and on the application of evolutionary principles to agriculture.

This review is more critical, though constructive. Thrall doesn't seem to disagree so much with my scientific hypotheses as with my characterizations of the views of others. Maybe he's right that "the world has moved on", both in rejecting natural ecosystems as a model for agriculture to copy, and in the tendency of biotechnologists to ignore tradeoffs. I hope I gave enough examples of promising work by agroecologists (such as Jacob Weiner) and biotechnologists to make it clear that the habits of mind I criticize are not universal. I agree that agronomists often think about tradeoffs and whole-crop performance and credited Colin Donald, an Australian agronomist, as a key source of my ideas.

Thrall is more optimistic about developing C4 rice than I was in the book, but maybe I'll change my views after visiting the International Rice Research Institute in March.

He writes that "there is a bibliography, but individual statements are not consistently referenced." That was my main objection to Diamond's otherwise excellent Collapse, so I tried to provide specific references for points that I thought might be controversial, except for those that were clearly matters of personal opinion. Apparently I missed some. In closing, he writes:

"I don't agree with everything in it, and there are many other topics that could have been included, but it has certainly got me thinking, and that is really all one can ask of a book such as this."

That was my intent. If disagreements with my book inspire more smart people to work at the interface of evolution and agriculture, it will have served its purpose.