Rice, fish, and the planet.

I n 2002, the United Nations Food and Agriculture Organization launched a program to recognize “globally important agricultural heritage systems” (1). However, so far, only eight systems have been included (1). In PNAS, the work by Xie et al. (2) reports the results of a 5-yr study of one of the systems, a farming system in south China, where for over 1,200 y, farmers have grown an indigenous species of common carp in their rice paddies. The methods used in this study are impressively thorough, but the purpose of the research is only incidentally to document an exotic agricultural heritage (2). Instead, the main goal is to discover whether features of this traditional agricultural system could contribute to innovations in sustainable agriculture at the global scale by unpacking the ecological interactions between fish, rice, and the environment (2). The study focuses on two questions: synergies between rice and fish that contribute to high and stable rice yields and the effects of the presence of the carp on the need for chemical inputs (fertilizer and pesticides) (2). Farms in 31 villages in Zhejiang province are randomly selected for a comparative study of rice monoculture vs. rice–fish coculture (2). Later, two experiments are conducted varying pesticide and fish feed while comparing rice monoculture, rice–fish polyculture, and fish monoculture (2). Results indicate that the presence of the fish benefits the rice by reducing insects, diseases, and weeds (2). The researchers notice that, when the fish bump into the rice stems, insects like planthoppers often fall into the water and are eaten (2). Video recordings quantify this effect, indicating a removal rate of planthoppers by fish of about 26% (2). The hitting activity of the fish also shakes dew drops from the plants in the early morning, reducing the risk of spore generation and mycelium penetration of rice blast disease in the leaves. The carp also eat or uproot many weeds, resulting in an almost weed-free paddy (2). If the fish are beneficial to the rice, the converse is also true. The presence of the rice plants attracts insects, which become a food source for the fish, and the leaves of the plants provide shade that reduces water temperature in the hot season. Rice also moderates the aquatic environment. It acts as a nitrogen sink and helps reduce the concentration of ammonia in the water and total N in the soil. Overall, paddies with fish require 68% less pesticide and 24% less fertilizer than rice monoculture. As Xie et al. (2) note, the wider significance of these results has to do with the global importance of rice agriculture, both as a source of food and because of the large and growing impact of fertilizers and pesticides on the environment. Rice–fish cocultures are not unique to China but have been reported in Egypt, India, Indonesia, Thailand, Vietnam, the Philippines, Bangladesh, and elsewhere (3, 4). Today, rice is the main ingredient in the daily diets of about 3 billion people. More than 90% of worldwide rice production occurs in developing nations, which are also the regions with the highest rates of population growth, and therefore, rice production is expected to increase (5). However, paddy rice is also the leading agricultural source of greenhouse gases, partly because of excess fertilizers but also because of the unique ability of rice paddies to pump methane into the atmosphere. When paddies are submerged, methanogenic bacteria become active, and the rice stalks enable the gas to vent into the atmosphere. This effect is unique to rice. Currently, methane accounts for about 20% of the global greenhouse effect, of which about one-half comes from flooded rice paddies (6). As a greenhouse gas, methane is ∼25 times more potent than carbon dioxide (7). However, this finding underestimates the contribution of methane to the climate problem, because its interaction with aerosols increases its activity; also, its relatively short residence time in the atmosphere makes it especially sensitive to corrective intervention (8). There is also a synergistic effect, because increased amounts of atmospheric CO2 are predicted to stimulate methane emissions from rice paddies (9). Because the soil methanogens quickly become dormant when the paddies are drained, emissions can be reduced by decreasing the amount of time that the paddies are submerged. However, this method has not been widely adopted. The overfertilization of rice with nitrogen also releases another greenhouse gas, nitrous oxide, which is roughly 300 times more potent than CO2 and also depletes stratospheric ozone. Enormous quantities of excess nitrogen fertilizer have been applied to rice paddies since the 1970s (10). Why excess? Beginning in the 1970s, fast-growing hybrid Green Revolution rice seeds replaced slower-growing native rice varieties in much of Asia. The nitrogen requirements of traditional rice were satisfied by symbiosis with nitrogenfixing bacteria supplemented by organic manure. However, the new rice required chemical fertilizers. To achieve rapid results, nations like Indonesia created crash programs to produce enormous quantities of nitrogen and phosphate fertilizer, which were sold to farmers at deeply discounted prices. Typically, all of the nitrogen and phosphate needed for each crop cycle was supplied to the farmers on credit. The cost of these inputs was deducted from the payment to the farmer when the crop was sold. In Indonesia, average grain yield rose from 1.53 ton ha in the 1960s to 4.2 ton ha in 2000 (11). However, much of the fertilizer was not used by the plants. A recent study used changes in the ratio of stable nitrogen isotopes to investigate the health of coral reefs around the island of Bali. Offshore from agricultural drainages, cores taken from Porites coral track a massive increase in N fertilizer coinciding with the onset of the Green Revolution in the 1970s (12). Obviously, none of the N fertilizer that wound up on the reefs was used by the rice. The same is true of phosphate, a mineral that is abundant in the volcanic soil of Bali, as it is in most of Indonesia. Phosphate leached from the landscape by the rains is conveyed to the paddies in centuries-old irrigation canals, replenishing the paddy soil. Consequently, most of the phosphate Fig. 1. Rice terraces of Zhejiang, China. Modified from Xie et al. (2).