Disregarding agroecological principles can lead to collapse. Florida citrus growers learned this lesson the hard way. Researchers in California are trying to prevent a rerun.

Huanglongbing, or HLB for short, is a disease of citrus that was originally recognized by farmers in southern China. It causes blotchy yellowing of leaves, sour deformed fruit, and — most devastating — premature fruit drop. The cause is apparently the bacterium Candidatus Liberibacter asiaticus (CLas), but as the incomplete italicization of the name indicates, this bacterial species cannot be grown in the lab, and therefore it has not been subjected to the steps necessary to confirm it as the pathogen. The CLas bacterium is transmitted to citrus leaves and stems by the Asian citrus psyllid, a tiny winged sucking insect similar to an aphid. The bacterium lives quite happily in the psyllid’s gut, but it can only be passed on to the insect’s offspring when they feed on an infected plant. This is where the citrus tree comes it.

The psyllid makes sure it injects some of its gut bacteria when it feeds on a leaf in order to provide its offspring with a meal of the beneficial bacteria they will need for survival, notably a species called Wolbachia. The CLas bacterium accompanies the Wolbachia, and in a fascinating case of bacterial genetics, can only survive in the presence of the Wolbachia. CLas at some point in its evolution was attacked by a virus that incorporated its own DNA into the bacterium’s DNA, and this internal virus is always poised to start replicating and burst out of the CLas cell, killing it. When scientists try to grow CLas in a Petri dish, this is what happens. However, in the environment where CLas normally grows, the virus is kept in check by a molecule that the Wolbachia produces. This psyllid-Wolbachia-CLas relationship has led researcher Georgios Vidalakis to call CLas a microbe of the Asian citrus psyllid, with citrus as just a transient host.

Once CLas is inside its transient plant host, it can spread only very locally within the plant, causing the leaves on just one branch tip to yellow. This gives a very patchy appearance of yellowing on a tree during the early stages of an epidemic. The only way that CLas can spread to the rest of the tree is when the psyllid juveniles grow up and fly to other locations on the tree, as well as other trees in the orchard. One unfortunate consequence for the localized distribution of the bacterium on the tree is that pre-symptomatic infections cannot be detected by monitoring programs that test tree sap unless the sap sample happens to come from a twig that is infected, and therefore there is usually widespread disease before the presence of CLas is confirmed.

The Florida citrus industry was slow to respond to the emerging threat of HLB disease. Where a comprehensive program for early eradication of the disease would have been an order of magnitude more costly than a program of strict quarantine to keep the disease out in the first place, once the disease becomes well established it is yet another order of magnitude more costly to try to manage it, in terms both of treatments and lost income. At this point Florida citrus production has fallen to the level of the 1940s. At least one commentator would like to blame the decline on venom from Anita Bryant, the 1950s-era singer who leveraged her fame to become both spokesperson for the Florida citrus industry and the leader of a nasty campaign to deny civil rights to gay people. Either way, there is a certain level of blame that the industry deserves.

What were the agroecological principles that were violated, allowing HLB’s destructive march across the state? Extensive monocropping allowed psyllids to move unimpeded from tree to tree, orchard to orchard, and county to county. A narrow genetic diversity insured that every citrus tree in the state is a susceptible host for CLas and a reservoir for additional infection. Basic sanitation was not adequately prioritized, with growers unwilling to destroy infected trees and orchards for the benefit of the greater landscape-level agroecosystem. Greater plant diversity might have supported populations of natural enemies against the psyllid, and plant diversity plus a healthy level of soil organic matter might have supported a microbial community with antagonistic capacity toward CLas. Only now are Florida growers looking for alternative crops, going as far as trials of the dry-climate crop pomegranate, an effort that was plagued with fungal wood canker diseases.

Of course the economic system played a role. Industrial production demands low diversity, high uniformity, concentrated resources, and substitution of capital intensive inputs over agroecological management. Growers will maximize individual benefit by retaining infected trees and harvesting sour deformed fruit for the juice market in order to recoup some of their investment. And in a perverse dynamic of the system, there are rich landowners who will retain unproductive trees on their property in order to classify their land as agricultural and qualify for government benefits. These growers are uninterested in the wellbeing of their trees or the industry as a whole, and from the perspective of industry itself they are wrecking any coordinated plan for eradicating the psyllid through spraying. With just one non-compliant grower, the psyllid finds refuge and can re-establish in the surrounding orchards, and thus the economics beats even conventional agriculture’s trump card.

The Asian citrus psyllid has already become established across a wide swath of California, but so far only a couple instances of HLB have been discovered in the Los Angeles area, out of ten thousand samples tested last year alone. The infected trees were destroyed, and movement of citrus material out of the zones of quarantine surrounding them is strictly prohibited, but unfortunately the psyllids will not be observing the quarantine boundaries. Researchers are scrambling to find resistant citrus germplasm for breeding resistant crop genotypes. New diagnostic tools are being developed for early detection that will register infection in sap samples from any part of an infected tree. Proponents of genetic engineering are scolding that their technology will have to be deployed to address conventional agriculture’s colossal wipeout on the technology treadmill it was already on.

One bright spot in the efforts to protect citrus in California is the work of the aforementioned Dr. Vidalakis. He is in charge of clearing all the citrus imports that are held in quarantine. Thanks to the foresight of policy makers in the 1930s, direct importation of citrus into the US is prohibited. Instead, all citrus material that someone wants to bring to the US passes through Vidalakis’ facility. From every sample of budwood his technicians painstakingly collect the microscopic growing tip, a piece of tissue out of reach of the plant’s sap and therefore of CLas or any sap-inhabiting viruses. They graft the tip onto a test plant, where it grows out and gets tested for all known viruses and bacterial pathogens, and also grafted to very susceptible plants that would presumably show symptoms in case of unknown viruses. Within a matter of months the importer receives certified virus- and CLas-free budwood, and citrus trees across the state are protected from devastating epidemics.

An admirable aspect of Vidalakis’ work is that he takes all comers. Immigrants from Asia can collect cuttings from their favorite citrus tree growing in their grandmother’s garden and submit them for high-tech cleanup. Vidalakis is not an agroecologist or social equity campaigner, but as a plant pathologist he recognizes that small-scale and backyard citrus growers are a legitimate component of the otherwise highly capitalized statewide citrus agroecosystem. If the small growers were marginalized, they would become the weak link in the protection of an entire industry.

Will the California citrus industry escape destruction from huanglongbing? It’s a cliffhanger. If industrial citrus production is able to overcome this agroecological reckoning, will it continue to present a sea of low diversity vegetation, a ready resource for the next intractable pest or pathogen from overseas or newly evolved domestically? Or will visionaries, a movement, and socioeconomic change arise and incorporate citrus production into a sustainable agricultural system designed using agroecological principles? There is never a bad time to turn to agroecology.

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