Undercooked hamburgers contami- nated with f. Coli 0157:H7 were respon- sible for a major outbreak of intestinal illness in 5 western states in 1993. Ground beef is unlike most other raw meats in that microbial contaminants are distributed throughout the product by grinding. Ham- burger cooked rare or medium-rare can still contain viable organisms on the inside. Research and reason can minimize foodborne and waterborne illnesses

Dean 0. Cliver u Edward R. Atwill

Several outbreaks of foodborne Recent outbreaks of foodborne and E. coli 0157:H7 (Bell et al. 1994). More and waterborne illness have di- waterborne disease in the United than 700 people in five western states rected the nation’s attention to in- States have heightened concerns about were made ill with bloody diarrhea or testinal pathogens that are threats several specific pathogens and kidney failure, at least four died, and to public health. Among fhese prompted actions by federal, state and several survivors lost part or all of pathogens are Cryptosporidium local agencies that could have serious their large intestines or kidneys. parvum and Escherichia coli implications for agriculture. Two In October 1996, another outbreak 0157:H7, which are known to in- pathogens in particular - the proto- of illness caused by E. coli 0157:H7 fect and to be spread by not only zoan Cryptosporidiurn parvurn and the was traced to fresh, unpasteurized humans, but also livestock and bacterium Esckerickia coli 0157:H7 - apple juice. A total of 66 cases was re- ported from three states and British various species of wildlife. New have caused major disease outbreaks in the past few years. Columbia. One child died of kidney regulations aimed at controlling In April 1993, C. parvurn contami- failure caused by the illness. these pathogens are being imple- nated the public water supply in Mil- The 1993 outbreaks caused wide- mented, despite a shortage of sci- waukee, Wis., causing 403,000 cases of spread public concern and prompted entific information about their diarrhea and more than 100 deaths regulatory actions at federal, state and ecology, how they contaminate (MacKenzie et al. 1994). It was the local levels. In 1996, the U.S. Depart- food and water supplies, and how largest outbreak of waterborne disease ment of Agriculture (USDA) an- to detect and eliminate such con- ever documented in the United States. nounced a sweeping reform of federal tamination. Research is needed to In January 1993, an outbreak of food safety rules for meat and poultry, address these issues and to de- intestinal illness first detected in while the Environmental Protection velop better technologies for Washington state was traced to Agency (EPA) issued new rules and pathogen detection, water treat- undercooked fast-food hamburgers amendments to the Safe Drinking ment and food processing. contaminated with the bacterium Water Act.

8 CALIFORNIA AGRICULTURE, VOLUME 51, NUMBER 2 ness, but the evidence has seldom been conclusive. Although we know that both C. parvum and E. coli 0157:H7 can be shed by mammalian sources other than humans and cattle, such sources are rarely explored dur- ing outbreak investigations. Several UC researchers and others are work- ing to develop tests that would make it easier to trace the source of contami- nation in such outbreaks. Foodborne disease outbreaks caused by E. coli 0157H7 and similar agents have been associated with con- taminated ground beef, roast beef, dry Italian-style salami, raw milk, apple juice, cantaloupe, lettuce and other Surveys indicate that Cryptosporidiumoocysts are common in surface waters through- vegetables. Ground beef is the most out North America, but the limitations of current tests make it difficult to learn where significant hazards lie. Although drinking water is treated, no test is available that can commonly implicated vehicle of trans- rapidly and sensitively detect C. parvum in treated water. mission in foodborne outbreaks of E. coli 0157:H7 infection (Armstrong The new regulations call for, among These pathogens can spread in a va- et al. 1996). Beef may become contami- other things, increased sampling and riety of ways, but always through fecal nated if intestinal contents contact the testing and improved control mea- matter. They may pass directly from meat during slaughter or processing. sures for foodborne and waterborne host to host (e.g., among children in Bacteria present on the surface of the pathogens. On a local level, some pub- day-care centers or among young ani- meat are distributed throughout the lic water districts are considering mals in a holding pen), as well as via meat by grinding. changes in watershed management. In fecally contaminated food and water. some cases, owing to the level of pub- Although people usually defecate in lic concern, regulatory action has pre- toilets, if they don't wash their hands ceded scientific understanding. Little carefully afterward they may convey is known about the medical ecology of pathogens to food. Surface water can these organisms, their sources, and become contaminated from uninten- how best to detect and control them. tional discharges of raw or inad- Several studies, funded in part by the equately treated sewage or from run- UC Division of Agriculture and Natu- off of domestic and wild animal ral Resources, are now under way to wastes. address these issues. In some outbreaks of foodborne or waterborne disease, the contamination Common features has clearly had a human origin, such Both E. coli 0157:H7 and C. parvum as a food handler with an intestinal in- infect the intestines and are shed in fe- fection or a swimmer shedding the ces. E. coli 0157:H7 is a virulent strain pathogen into water. There have been of the harmless E. coli bacterium that cases of both cryptosporidiosis and E. normally inhabits the intestines of hu- coli 0157:H7 infection acquired from mans and other warm-blooded ani- swimming in lakes, and some cases of mals. This pathogenic strain is known cryptosporidiosis have been linked to to infect and to be shed by humans, swimming pools. cattle, sheep, deer and possibly other The source of the contamination of ruminants. C. parvum infects about 80 Milwaukee's water supply, which is species of animals, including humans, drawn from Lake Michigan, was never cattle, sheep, goats, pigs, horses, dogs, determined. Possible sources consid- cats and various wildlife species, such ered by investigators included cattle as deer, raccoons, opossums, pigs and along two rivers that flow into the Mil- rabbits. Both organisms have been waukee harbor, slaughterhouses, and found throughout the world, wher- human sewage (MacKenzie et al. ever researchers have looked for 1994). Cattle have been implicated in them. several outbreaks of waterborne ill-

CALIFORNIA AGRICULTURE. MARCH-APRIL 1997 9 It is not known how people typi- cally become infected with Crypto- sporidium. Drinking water was clearly the primary transmission vehicle in Milwaukee and in other major out- breaks of cryptosporidiosis. In general, however, the relative importance of various possible transmission routes is unclear. Food-related outbreaks have involved raw milk, possibly raw sau- sage, tripe, kefir and apple juice. Dur- ing the Milwaukee outbreak, Crypto- sporidium carried in tap water was suspected of contaminating salad dressings, dairy products and sausages, so the suspect foods were recalled. Illness in humans No drug is known to be effective in treating the infections and illnesses caused by these pathogens. E. coli 0157:H7 and several other, less com- mon strains of E. coli produce a toxin similar to Shiga toxin of Shigella dysenteriae and cause severe bloody di- arrhea in humans. The infection can lead to kidney failure (hemolytic ure- mic syndrome) and death. Shiga toxin-producing E. coli are notably more resistant to acid condi- tions (as in apple juice) than non- pathogenic strains of E. coli. E. coli 0157:H7 can survive a pH as low as 2.0 under certain circumstances (Armstrong et al. 1996). The bacteria can multiply in foods and elsewhere in the environment under some condi- tions, as well as in the host’s body. They can be killed by heat, chlorine or UV light. An internal temperature of 155°F during cooking is sufficient to kill more than 99% of organisms in ground beef (Bell et al. 1994). The largest documented outbreak of foodborne illness caused by E. coli 0157:H7 occurred in Japan in 1996, when more than 9,000 people became ill and at least 11 died. The source of the outbreak was never determined. Cryptosporidium infection causes watery diarrhea associated with ab- dominal cramping, nausea, vomiting and fever. In people with normal re- sistance, cryptosporidiosis is a self- limiting illness from which most pa- tients recover after a few days or weeks. Those with compromised im- mune systems, however, develop

10 CALIFORNIA AGRICULTURE, VOLUME 51, NUMBER 2 long-term infections and may die from the illness. People at greatest risk from cryptosporidiosis include organ transplant recipients, AIDS patients and some cancer patients. Cryptosporidium is transmitted among hosts in the form of ”oocysts,” which cannot multiply in foods or elsewhere in the environment. The oo- cysts are very resistant to chlorine but Each Cryptosporidium oocyst, about probably not to heat or UV light. Each 4-micrometers in diameter, contains four oocyst contains four ”sporozoites” that sporozoites. emerge and infect a new host’s intes- tines after the oocyst is swallowed. There are several species of Crypfo- sporidium that infect animals, but only C. parvum is known to infect humans. Studies indicate that very few vi- able cells of E. coli 0157:H7 or oocysts of C. parvum need to be ingested with food or water to produce infection. For example, an infectious dose of 132 calf- derived oocysts caused crypto- sporidial infections in 50% of healthy Cryptosporidium sporozoites infect a Wildlife, including black-tailed deer, may host’s intestines, causing watery diarrhea, be significant sources of cryptosporidial human volunteers (Dupont et al. abdominal cramping, nausea, vomiting contamination of surface water. 1995). The lowest infectious dose suffi- and fever. cient to induce cryptosporidiosis was 30 oocysts. In outbreaks of E. coli the 1996 reforms known as the ”Final were at least partly inspired by the 0157:H7 infection, the infectious dose Rule on Pathogen Reduction and Haz- Milwaukee outbreak of crypto- has been estimated to be fewer than 50 ard Analysis and Critical Control sporidiosis. Under proposed changes bacteria and, in some cases, as few as 5 Point (HACCP) Systems” (USDA to the Surface Water Treatment Rule, (Armstrong et al. 1996). 1996). The new regulations require all public water systems that use surface slaughter and processing plants to water sources may be required to treat Regulatory actions implement HACCP plans. The specifically for Cryptosporidium (EPA In response to the 1993 disease out- HACCP (pronounced “hassip”) con- 1994). break caused by E. coli 0157:H7 in cept originated in the space program Cryptosporidium oocysts are resis- fast-food hamburgers, the Clinton ad- to ensure food safety for astronauts. It tant to chlorine and may not be elimi- ministration mandated safe-handling requires food processors to identify nated by disinfection procedures de- labels for raw meat and poultry prod- ”critical control points” where hazards signed to remove other protozoan ucts, declared E. coli 0157:H7 an adul- such as microbial contamination can pathogens, such as Giardia. Even a terant in raw ground beef (making the occur, establish controls to prevent or well-run water-treatment system can- sale of contaminated meat unlawful) reduce those hazards, and maintain not ensure that drinking water will be and initiated a testing program for good records. completely free of the parasite. Because that pathogen. Ground beef is unlike In addition, the new rules require no available test can rapidly and sensi- most other raw meats in that microbial slaughter plants to conduct microbial tively detect Crypfosporidium in treated contaminants are distributed through- testing of carcasses for generic E. coli water, water-treatment plants can only out the product by grinding, rather to verify that their procedures are monitor water-quality indicators such as than being concentrated on the sur- working to prevent fecal contamina- turbidity and try to maintain a level of face. As a result, a hamburger cooked tion. New performance standards for water quality (through filtering and rare or medium-rare (as preferred by Salmonella require slaughter plants and other procedures) that makes the about one-fourth of the U.S. popula- producers of raw ground meat to en- presence of oocysts unlikely tion) still contains viable organisms on sure that their Salmonella contamina- (MacKenzie et al. 1994). The EPA the inside. This is a particular concern tion rates are below the current na- may require some water systems us- given the extremely low infectious tional baseline. And finally, all plants ing unfiltered surface water to dose of E. coli 0157:H7. must adopt standard operating proce- implement filtration procedures. The 1993 outbreak also set in mo- dures for sanitation. The EPA has acknowledged that tion a major revision of the USDA’s Similarly sweeping reforms of the numerous scientific uncertainties must food safety program, culminating in EPA’s drinking water regulations be resolved before it can establish

CALIFORNIA AGRICULTURE, MARCH-APRIL 1997 11 ers who graze 1,990 E. coli 0157H7 infection is also cattle on city-owned more common in calves than in older land surrounding two cattle. Estimates of the prevalence of reservoirs in Alameda shedding among cattle range from 0 to County. 4%, with adults at the lower end and Studies have not calves at the upper end of this range. shown a clear link, E. coli 0157:H7 has a wide geographic however, between distribution in the United States, oc- cattle grazing and the curring in 63% of feedlots in one large presence of C. parvum survey (Armstrong et al. 1996). Rela- oocysts in surface wa- tively few studies have looked at its ter. Cryptosporidium prevalence in other animals. A survey oocysts are common of a single flock of 35 sheep in Idaho in surface waters found that the prevalence of shedding throughout the ranged from 0 to 31%, depending on United States, but the the season. In Texas, researchers found limitations of avail- that 2 out of 108 deer were shedding Researchers have been trapping wild pigs able testing procedures make it diffi- the bacterium. in coastal California to monitor them for cult to determine where significant The fate and distribution of manure C. parvurn. hazards exist. from cattle and other livestock, and its specific safety standards for Crypto- potential to contaminate food and sporidium. To gather data needed to re- Prevalence in animals water depend on the type of live- solve these issues and guide the In California beef cattle, clinical stock operation. In cow-calf opera- agency’s modifications of current cryptosporidiosis and shedding of C. tions, rangeland sheep herding and regulations, the EPA promulgated the parvum are usually limited to calves other ”extensive” livestock operations, 1996 Information Collection Rule up to 4 months of age. Older calves manure is left where it falls. In inten- (ICR). Among other things, the ICR re- and adult cattle do not appear to shed sive operations, such as feedlots and quires large, public water systems to appreciable amounts of C. parvurn in dairies, manure may be composted for collect information on the presence their manure. In selected populations, use as bedding or it may be applied to and levels of microbial contamination such as dairy calves, clinical crypto- agricultural land as fertilizer. (including Cryptosporidium) and the ef- sporidiosis and shedding of C. parvum Although composting is likely to fectiveness of various treatment tech- occur primarily within the first month kill any pathogens, uncomposted nologies. Unfortunately, available tests of life. In contrast, humans and several manure that is applied to land for Cryptosporidium may not produce species of wild animals can be infected where crops are grown for human meaningful data. The reagent used in and shed C. parvum at all ages. Conse- consumption or that enters surface the immunofluorescent assay to detect quently, if we were to find that on a waters destined for human water C. parvum cross-reacts with other spe- specific watershed beef calves were a supplies may contain pathogens. cies of Cryptosporidium that are not in- significant source of viable C. parvum, C. parvum cannot multiply outside fectious to humans. In addition, the the risk of contamination could be the host and may be killed by heat, tests are unable to distinguish between greatly reduced if ranchers prevented drying, freezing or UV light, but not viable oocysts and dead ones. To ad- young calves from grazing near water by chlorine. E. coli 0157:H7, on the dress these problems, the EPA is un- or if they grazed older animals. other hand, may multiply in the en- dertaking supplemental surveys using Wildlife may be significant sources vironment under some conditions, more sophisticated analyses. of cryptosporidial contamination of but can be killed by chlorine as well While the EPA is making an effort surface water. In a survey of 100 rac- as by heat or UV light. to gather data before establishing new coons, 13 juveniles had oocysts in their regulations, other agencies have been feces (Snyder 1988). Cryptosporidial Pressure on agriculture less inhibited by the lack of scientific infection has been confirmed in gray Consumer and regulatory concerns information. For example, the San squirrels and mule deer. Thirty per- about food and water safety are gra- Francisco Water District is considering cent (35/115) of wild mice trapped at a dually being directed toward produc- a ban on cattle grazing within its wa- dairy shed oocysts (Klesius et al. 1986). tion agriculture. There is increasing tersheds. Alternatively, the water dis- Sixty-three percent of wild brown rats pressure to impose on-farm measures trict may continue to allow grazing have been found to shed C. parvum that will eliminate pathogens so that while requiring new management (Webster and McDonald 1995). In sur- processors and consumers do not have practices designed to guard against veys we have conducted, 5% of feral to worry about them. Although the Cryptosporidium and other waterborne pigs trapped in coastal California were current focus of USDA regulations is pathogens. The final decision, which is found to be shedding what we believe on slaughter and processing plants, expected in May, will affect 15 ranch- are C. parvum oocysts. the agency is also considering a com-

12 CALIFORNIA AGRICULTURE, VOLUME 51, NUMBER 2 prehensive food-safety strategy that The most generally applicable and refrigerated after slaughter directly addresses hazards at other points means of decontaminating foods is affects the numbers of bacteria present “from farm to table.” This could even- with heat, by pasteurization or cook- on the finished product and may com- tually put the onus on farmers to ing. Consumers must use proper pletely nullify any preharvest efforts di- eliminate pathogens from their herds, food preparation and cooking prac- rected at food safety. even though the means to do so may tices to minimize foodborne disease. It is not known whether most of the not be available. At the same time, producers and E. coli 0157:H7 that occasionally con- When outbreaks of foodborne ill- processors should adopt manage- taminates beef carcass surfaces comes ness occur, regulatory efforts are often ment practices that minimize the lev- from the animal’s intestines or from directed upstream, beginning with the els of pathogens present on the prod- the hide. Much research -being con- distributor, leading back to the proces- uct. However, agriculture can only ducted at several universities, includ- sor and, if possible, finally reaching adopt such practices once they have ing UC Davis, and USDA - is cur- the original producer. Pathogens can been identified through research. rently aimed at identifying critical contaminate food products anywhere Moreover, we know very little about control points at slaughter to decon- along the line from producer to con- the ecology of foodborne pathogens taminate the surface of a carcass. Most sumer. In many cases, the contamina- at the farm level. methods being tested are based on tion occurs at centralized processing washing the carcass surface with wa- facilities or from improper handling Research in progress ter or solutions containing organic by consumers. For instance, foodborne Research is under way - in part acids, hypochlorous acid, hydrogen bacterial pathogens can multiply from funded by the UC Division of Agricul- peroxide, or trisodium phosphate. a harmless level to one high enough to ture and Natural Resources -to esti- Although several of these methods cause illness in humans if the product mate the prevalence and to identify look promising, there is some doubt is not refrigerated or is otherwise im- risk factors for shedding of a variety of that any will guarantee the absence of properly handled. possible foodborne bacterial and pro- pathogenic E. coli, generic E. coli, or If established management prac- tozoal pathogens in livestock popula- Salmonella. tices can eliminate a pathogen at the tions. If, for instance, we find that beef With respect to dairy cows and production level, there may be justifi- calves being produced by California’s milk production, we find very few cation for holding producers respon- 700,000 to 950,000 beef cows are not cows shedding C. parvum in their ma- sible for its presence. However, there significantly infected by major nure, but we cannot explain why we are many emerging foodborne patho- foodborne pathogens, then devising find C. parvum in the flush water corn- gens about which we know almost management practices that focus on ing from the wash pen for lactating nothing. In the case of E. coli 0157:H7, cow-calf production will likely have cattle, nor can we say what level of for example, we have very little infor- little impact on reducing the incidence shedding results in an appreciable risk mation about how the bacterium is in- of foodborne illness associated with of milkborne transmission. Does the troduced into a dairy or cow-calf op- beef products. If, on the other hand, widespread occurrence of C. parvum eration or why it often appears to calves coming off of California’s infection in dairy calves pose any risk suddenly leave the herd. rangeland are an important entry to the veal market or to lactating cattle? While it is entirely reasonable that point for a foodborne pathogen, then The answers to these critical questions we expect food to be safe and whole- through research, extension and work- will show where on-farm or on-ranch some, some consumers and public offi- ing closely with the industry we can problems exist - and just as impor- cials have expressed zero tolerance for develop management plans that mini- tant, where they do not exist. Only then risk. It will be extremely difficult, if mize risk of foodborne disease. can we devise effective solutions. not impossible, to implement public Preliminary data suggest that less We and other researchers are also policy that will satisfy them. Society’s than 1% of rangeland beef calves are working to develop new detection growing detachment from how food is shedding E. coli 0157:H7 and an methods for pathogens such as raised results in the unreasonable ex- equally low proportion of calves are C. parvum. Better tests will help clarify pectation that farms or ranches can be shedding C. parvurn at time of wean- where actual risks exist, allow us to run as microbe-free, sterile environ- ing, 6 to 9 months of age. A more sen- evaluate different water-treatment and ments. We often can raise and grow sitive test for detecting E. coli 0157:H7 food-processing methods for inactivat- food with a minimum of pathogenic probably would have found more in- ing pathogens, and help prevent false microorganisms on the product, but it fected cattle. What we cannot say at alarms resulting from detection of is not a sterile commodity. this time is whether these low pathogens that are already dead be- Both C. parvum and E. coli 0157:H7 prevalences of shedding pose a risk to cause of food processing practices or can be killed in food by irradiation, al- the consumer and what is the relative other mechanisms. Finally, a group of though this is not a widespread prac- importance of animal shedding UC researchers is taking a multidis- tice. The U.S. Food and Drug Adminis- postweaning, during stock operations, ciplinary approach to understand how tration does not permit irradiation of in the feedlot, or at the time of slaugh- oocysts travel through a watershed red meats. ter. How meat products are handled from land to water.

CALIFORNIA AGRICULTURE, MARCH-APRIL 1997 13 Research, education needed Recent outbreaks of foodborne in- fectious disease caused by E. coli 0157H7 and C. parvurn have gotten the public’s attention. Food safety so- 4 Composted lutions will come only with a detailed “greenwaste” mulch was ap- understanding of how and why patho- plied in the vine gens enter the food supply; better de- row for weed con- tection and processing technologies; trol. The wood chips cost more working cooperatively with produc- than the other ers, processors and distributors; and treatments, but educating consumers through such they controlled means as UC Cooperative Extension weeds well and half the chips on how to prepare and cook their food were still in the properly and safely. vineyard after the second year. D.O. Cliver is Professor, and E.R. Atwill is Extension Veterinarian and Assistant Professor, Department of Population Health and Reproduction, School of Vet- Four weed management systems compared.. . erinary Medicine, UC Davis. References: Mulch plus herbicides Armstrong GL, Hollingsworth J and Morris JG Jr. 1996. Emerging foodborne pathogens: Escherichia coli 0157:H7 as a model of entry of a new pathogen effectively control vineyard into the food supply of the developed world. Epidemiol Rev 18(1):29-51. Atwill. ER. 1996. Assessing the link between range- land cattle and waterborne Cryptosporidiurnparvurn infection in humans. Rangelands 19(2):48-51. Bell BP, Goldoft M, Griffin PM, et al. 1994. A Clyde L. Elmore o John Roncoroni o Layne Wade multistate outbreak of Escherichia coli 0157:H7- Paul Verdegaal associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: the Washington expe- Mulches have been used for many Weed management with herbicides in rience. JAMA 272(17):1349-53. years to control weeds by smoth- the vine row has been very successful Dupont HL, Chappell CL, Sterling CR, et al. 1995. ering the weed seedlings. A 2-year for the control of annual weeds and The infectivity of Cryptosporidiurnparvurn in healthy volunteers. N Engl J Med 332:855-9. study in a Lodi grape vineyard some perennial weeds. However, weed species change as herbicides in different [EPA] Environmental Protection Agency. 1994. Na- compared the weed-control effec- tional primary drinking water regulation: enhanced tiveness of herbicides, cultivation, families are used, and unless different surface water treatment requirements. Federal Reg- cover crop biomass and wood- herbicides are used a weed species ister 59(145):38832-58. chip mulch and the cost of these may become more severe than before Klesius PH, Hayes TB and Malo LK. 1986. Infectiv- practices. The most effective and herbicides were used. When annual ity of Cryptosporidiurnsp. isolated from wild mice weeds are controlled, some perennial for calves and mice. J Am Vet Med Assoc least expensive treatment over the 189:192-3. 2 years was the use of preemer- weeds become more common and are more difficult to control. Herbicide MacKenzie WR, Hoxie NJ, Proctor ME, et al. 1994. gence herbicides and a post- costs have increased as new herbicides A massive outbreak in Milwaukee of crypto- emergence herbicide as needed. sporidium infection transmitted through the public become available. In addition, there is water supply. N Engl J Med 331(3):161-7. Growing cover crops, chopping interest in reducing pesticide inputs Snyder, DE 1988. Indirect immunofluorescent de- the biomass and placing it into into the vineyard and in managing tection of oocysts of Cryptosporidiurnparvum in the the vine row was very effective feces of naturally infected raccoons (Procyon lotor). vegetation in the row by other meth- J Parasitol 74:1050-5. the second year, when more bio- ods, while at the same time growing mass was produced and weeds [USDA] US. Department of Agriculture, Food cover crops between the vine rows. Safety and Inspection Service. 1996. The final rule were controlled prior to mulch Mulches have been used for many on pathogen reduction and hazard analysis and placement. The mulch was persis- years to control weeds by smothering critical control point (HACCP) systems. Background tent in the field and should give Papers, July 1996. the weed seedlings. Mulches are com- long-term weed-control benefits, monly used in the landscape to sup- Webster, JP and McDonald, DW. 1995. Cryptospori- diosis reservoir in brown rats (Rattus norvegicus) in which were not evaluated in this press emergence and growth of weeds. the U.K. Epidemiology and Infection 115:207-9. study. At the same time that weeds are con-

14 CALIFORNIA AGRICULTURE, VOLUME 51, NUMBER 2