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thrive under the conditions required to maintain mid-1990s were applied for grub control but were healthythrive under turfgrass the conditions and are so required adaptable to maintain that cul- alsomid-1990s acutely were toxic applied to earthworms for grub (14).control Most but of were the turalhealthy manipulations turfgrass and alone are soare adaptableunlikely to that resolve cul- olderalso acutely worm-toxic toxic topesticides earthworms can no (14). longer Most be of used the castingtural manipulations problems. Physical alone are removal unlikely of to casts resolve by onolder turf, worm-toxic and presently pesticides no pesticides can no longerare labeled be used for brushing,casting problems. switching Physical or dragging removal is laborious of casts and by earthwormon turf, and control presently in theno pesticidesUnited States. are labeled for Theofbrushing, only temporary switching worm benefit or dragging (8). is laborious turns: and earthworm control in the . of only temporary benefit (8). Peter Lees’ invention Chemical control PeterAn approach Lees’ invention widely used used for earthworm earthwormChemicalDuring control the past 20 years the problem of exces-castandAn cast approach suppression reduction widely from used the used early for 20th earthworm century siveDuring earthworm the past castings 20 years interfering the problem with of play exces- on untiland cast about suppression 1960 involved from the the early use 20th of chemical century ongolfsive earthworm courses, golf sport castings fields interfering andcourses other with recreational play on expellantsuntil about that 1960 were involved applied to the irritate use of the chemical worms, turfgolf venuescourses, has sport become fields more and serious other recreational and wide- causingexpellants them that to were come applied to the to surfaceirritate thewhere worms, they Aspread.turf byproduct venues Why? has Pesticides become of historicallythe more serious usedtree and to wide- maycon- providewerecausing swept them oran to raked comeorganic up to andthe discardedsurfacesolution where (8). tothey The trolspread. earthworms Why? Pesticides included historically mercuric chloride used to (alsocon- method,were swept pioneered or raked by up British and discarded greenkeeper (8). Peter The acalledtrol long-standing earthworms corrosive sublimate), included andmercuric lead arsenate vexing chloride and (alsoproblemeven W.method, Lees faced during pioneered theby by1890s, British was greenkeeper so effective Peterthat golfsodiumcalled corrosivecourse cyanide sublimate),and superintendents. have long lead since arsenate been and banned even itW. had Lees become during the the mainstay 1890s, was for soearthworm effective sup-that becausesodium cyanidethey were and highly have longpoisonous since been (8). bannedDuring pressionit had become on European the mainstay and U.S. for golf earthworm courses by sup- the Thethebecause “The1950s following they 12th and were 1960s, greenarticle highly has awas single been poisonousoriginally application infested published(8). with of During chlor- thou- in the1920spressionplaying September (3,4,9,10,11). onon surfacesEuropean 2011 that(Authors’ and are U.S. more note: golf mud Leescourses than provides by turf. the issuesandsdane,the 1950s ofand at GCM. that thousandsand 1960s,time Reprint of the a earthworms. singlepermission mainstay application forThe by white Oceanworm of chlor- grub cast-Organics. a1920sCompacted fascinating (3,4,9,10,11). earthworm account (Authors’ of casts his reduce experimentingnote: Leeswater provides infiltra- with ingscontrol,dane, were at wouldthat so prolific time kill the that earthworms mainstay mowing for and was white not eliminate possible grub thisation fascinating methodand provide on account pages ideal seedbed of37-43 his of experimenting conditions his seminal for book with weed withoutcastingcontrol, problems dispersing would killfor them. as earthworms long … Theas seven turf and years.was eliminateextremely But the “Carethisestablishment. method of the on Green,” Casts pages also 37-43 available blunt of his onlinemower seminal atblades http:// book set shallow-rootedcasting problems and for about as long 60% as seven of the years. bentgrass But theon “Careat low cutting of the Green,”heights, availableand they may online be so at numer- http:// EPA cancelled chlordane registration for turfgrass archive.lib.msu.edu/DMC/turfgrass/PDF/care-Article continued from last issue. theinEPA 1983 green cancelled because had died. chlordane of itsWhat buildup canregistration clubsin the with environment, for (excessive) turfgrass ofthegreen.pdf).archive.lib.msu.edu/DMC/turfgrass/PDF/care-ous that putting greens cannot be mowed without earthwormharmin 1983 to because wildlife casts doof and itsto overcomechronicbuildup human inthis the problem?” environment, health risks. ofthegreen.pdf).firstLees’ physically method dispersing involved them. applying Earthworm powdered casts Manyharm— toturfgrass USGA wildlife Green pesticides and chronic Section used human Senior from the Agronomist’shealth 1970s risks. to mowrahon Lees’the surface meal method (made of greens involved from and applyingtees of mayBassia also powdered latifolia affect, emailMany to turfgrass D. Potter pesticides used from the 1970s to mowrahtheplayers’ perceptions meal tree (made of India, of from course after seeds quality. the of Bassia edible In 2009latifolia had the, beentheSports butter pressed Turf tree Research out) of and India, Institutewatering after itreceived the in. edibleNatural more oil com- que- had Excessive earthworm casts — small mounds of ponentsbeenries about pressed in mowrahearthworms out) and meal watering than irritated any it in.theother Natural earthworms, turf com-man- -rich fecal matter — are a worldwide problem causingponentsagement themin problem. mowrah to come meal to irritated the surface, the earthworms, where they on golf courses and sports fields when they dis- werecausingEarthworms raked them into to piles, playcome shoveled a to vital the rolesurface, into in wheelbarrows naturalwhere they and rupt the playability, aesthetics and maintenance of andweremanaged hauled raked grasslands intooff the piles, site. where shoveled they into literally wheelbarrows plow the playing surfaces (8,13). A single worm can pro- andsoilLees’ byhauled burrowing method off the is throughsite. regarded it (7).as among Earthworm the most tun- duce its own weight in casts in 24 hours. In Great importantnelsLees’ reduce method historicalsoil compaction is regarded innovations and as amongprovide in turf the passage- man-most Britain, estimates of the quantity of earthworm agement,importantways through in historical part which because air innovations and it allowed water incan expansion turf percolate, man- of casts deposited on the surface range from 16 to Britishagement,enhancing golf in penetrationcourses part because on upland and it growthallowed , areasof expansion that . pre- of 20 tons per acre [40-50 tons/hectare] per year viouslyBritishEarthworm golfhad coursesbeenfeeding ill-suited on activity upland for stimulates soils,golf becauseareas microbial that earth- pre- on sports turf pitches, and more than 2 tons per wormsviouslydecomposition had made been the of ill-suited puttinggrass clippings greensfor golf unplayableand because thatch earth- (4).and year on a typical 5,000-square-foot [465-square- USGAwormsaccelerates madebulletins nutrient the described putting recycling greens mowrah (12). unplayable mealAn acre as (4). an of meter] push-up golf green (8). “outstandingUSGAturf can bulletins support efficacious more described than treatment” a mowrah quarter of meal and a million asa “very an Casts adversely affect ball roll and muddy and effective“outstandingearthworms earthworm that efficacious collectively eradicator” treatment” eat 4 when tons and ofapplied a clip- “very smother the grass when smeared or compacted by ateffectivepings the andrate earthwormother of 15 plant pounds debris, eradicator” to 1,000and turn whensquare over appliedfeet 15 tonsof tires or foot traffic so that golfers find themselves greenatof topsoil.the andrate Awateredof moderate 15 pounds liberally level to of afterward1,000 earthworm square (10,11). activity, feet Atof onegreen time, and atwatered least aliberally dozen proprietaryafterward (10,11). fertilizers At andone other time, products at least acontaining dozen proprietary mowrah meal fertilizers were marketedand other productsfor earthworm containing control mowrah on golf meal courses were (11).marketed Use offor the earthworm method declined control inon the golf late courses 1940s and(11). 1950sUse of withthe method development declined of in chlordane the late 1940s and otherand 1950s earthworm-toxic with development synthetic of pesticides. chlordane and otherMowrah earthworm-toxic meal is rich synthetic in pesticides., natural soaps or surfactantsMowrah meal found is richin the in leaves saponins and, naturalseeds of soaps oats, spinach,or surfactants , found chickpeas, in the leaves soybeans, and seedsginseng, of oats, tea andspinach, hundreds alfalfa, ofchickpeas, other soybeans, (6,15). , Saponins tea haveand hundreds antifungal of and other antibacterial plants (6,15). activity Saponins and (Top left) In the 1890s Peter Lees, head greenkeeper at Mid-Surrey GC in England, introduced mow- formhave part antifungal of the plant’s and antibacterial natural defenses activity against and Danielrah(Top meal leftA.) asInPotter, thea means 1890s ofPh.D. Peter controlling Lees, headearthworms greenkeeper on golf at courses. Mid-Surrey (Top GC right in )England, Watering introduced in the mowrah mow- form part of the plant’s natural defenses against meal.rah meal (Bottom as a means) One of of three controlling wheelbarrow earthworms loads onof earthwormsgolf courses. removed (Top right from) Watering a putting in thegreen mowrah treated disease. Plant saponins are used in manufacture of Carl withmeal.T. Redmond,mowrah (Bottom meal.) One Photos of Ph.D. three published wheelbarrow by R.loads Beale of earthworms in 1908 (3) removed and reprinted from a byputting J. Beard green (4) treated naturaldisease. soapsPlant andsaponins shampoos, are used cosmetics, in manufacture and even of Davidwith W. mowrah Williams, meal. Photos Ph.D. publishedDry byearthworm R. Beale castings in 1908 on(3) a and push-up reprinted creeping by J. bentgrass Beard (4) green. Photosnatural by D. Pottersoaps and shampoos, cosmetics, and even

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as a component of the foamy “head” of . Back to the future Although saponins were never confirmed as the In 2007, the first author attended a sports turf earthworm-active component in mowrah meal, it conference in Beijing, , where he learned of is highly likely that their detergent-like irritation a natural substance used in that country to con- of earthworms’ mucus membranes was the basis trol snails and slugs in vegetable fields and to sup- for its effectiveness. Mowrah meal is no longer press earthworms and casting on sports fields. The marketed for earthworm management, but are method involves applying a byproduct of tea oil there other sources of plant saponins that could be manufacture. Tea oil pressed from seeds of developed for that purpose? the oil plant, oleifera, is used for cooking and in soaps and shampoos, marga- rine and other products. Tea seeds, fruits and oil are rich in antioxidants and are used in Chinese . After the seeds are crushed to extract the oil, the residue is ground into meal or pressed into “cake” or pellets. Tea seed meal is used as a component of animal feeds, as an organic fertilizer and for other purposes. Websites of many Chinese tea oil manufactur- ers (for example, www.camellia-oil.com) claim that tea seed meal can be used to control earth- worms on sports turf and lawns. A 2007 search of the worldwide scientific literature, however, found no references or data supporting that claim, and no information concerning rates, timing, effec- tiveness or other aspects of using tea seed meal to manage earthworms and casts. But like mowrah meal, tea seed meal is high in natural saponins (5,13) and therefore worth evaluating as a possible substitute for Peter Lees’ historical remedy for cast reduction. Testing for cast suppression, 2007-2008 We started researching tea seed meal in autumn 2007 to determine whether it could be used to reduce earthworm casts on playing surfaces. Most of the early trials were done on a large, predominantly Penncross creeping bentgrass push-up green at the University of Kentucky’s A.J. Powell Jr. Turfgrass Research Center near Lexington. The site had high numbers of actively casting earthworms (>95% Apporectodea species). Other trials were done in fairway-height creeping bentgrass and on a perennial ryegrass fairway. A full account of the experiments was published in a peer-reviewed international scientific journal (13). Our initial tests were with crude tea seed meal pellets (3.2 millimeters diameter; 5–8 (Top) Earthworms expelled from 1 square meter of a push-up green after tea seed meal was millimeters long) and powder obtained from a applied. (Bottom) This desiccated earthworm was found the morning after the turfgrass was source in China. The powder, essentially a dust, treated with tree-seed meal. Photos by D. Potter proved awkward to apply, so later work focused on the pellets. Application of the pellets at 6 or 12 pounds/1,000 square feet (2.93 or 5.86 kilo- grams/100 square meters) followed by irrigation, quickly expelled as many as 200 worms/10 square 16 Thru The Green • JANUARY/FEBRUARY 2012

90 GCM September 2011 research

feet (0.93 square meter) on the push-up green. Cast reduction, April 2008 Most of the expelled worms dried up and died on the turf surface; other experiments indicated relatively few worms that burrowed back down 12 pounds 6 pounds Untreated survived. Expelled worms appeared flaccid and 40 quickly desiccated, evidently because their mucus coating had been disrupted. A single tea seed meal application in early April 2008 reduced castings in replicated plots on the push-up green by >95% 30 for at least five weeks (Figure 1). In another trial on the push-up green, application of tea seed meal in early October reduced casts by 98% after two days and 83% after 30 days (Figure 2). Finally, a 20 sequence of lab trials, called bioassay-guided frac- tionation, confirmed that the chemical basis for tea seed meal activity on earthworms is the natu- ral triterpene saponins found in tea seeds. 10 We tested two methods for removing the

Average no. of casts/10 square feet Average no. expelled worms from putting green surfaces (13). Locations of expelled worms were marked with dabs of orange turf paint. The following morning 0 1 8 15 35 a single pass with a greens mower removed about 66% and one pass with turf sweeper removed Days after treatment 40% of the cadavers. In other tests, the tea seed meal pellets did not Figure 1. Reduction in earthworm (Apporectodea species) casts on a creeping bentgrass push-up provide any control of white grubs or cutworms green after applying crude tea seed meal (12 or 6 pounds product/1,000 square feet) in April 2008. in field plots (13). Unlike earthworms with their mucus-covered skin, insects have an exoskeleton that seems to protect them from being dried out Cast reduction, October 2008 from exposure to saponins. On the plus side, the pellets also did not harm the tiny soil-inhabiting insects and mites that help to decompose thatch Treated Control 80 and grass clippings. Non-native (invasive) earthworm species 60 The first and second authors began a system- atic survey of the earthworms on Kentucky golf courses in spring 2011 to clarify which species are associated with surface casts. Several thousand 40 specimens were collected from a total of 18 fair- ways on six different courses. We also sampled worms on push-up greens. All of the culprits appear to be non-native, invasive species. At least 20 seven species have been identified, the most com-

Average no. of casts/10 square feet Average no. mon by far being Apporectodea species. The Ken- tucky earthworm surveys will continue for at least another year. Nightcrawlers, which also are inva- 0 sive, seem to be responsible for most of the casting 1 9 16 23 30 problems in the Pacific Northwest (1). Days after treatment A natural organic fertilizer Figure 2. Reduction in earthworm casts following application of crude tea seed meal (6 pounds After hearing about our earthworm research at product/1,000 square feet) on a perennial ryegrass golf fairway in October 2008. an educational seminar, representatives of a devel- oper and manufacturer of natural fertilizers and biorational materials for turf, ornamental horti-

THE GOLF COURSE SUPERINTENDENTS ASSOCIATION OF NORTHERN CALIFORNIA 19 92 GCM September 2011 research

culture and specialty agriculture (Ocean Organ- ics Corp., Ann Arbor, Mich./Waldoboro, Maine) expressed interest in developing an organic fer- tilizer based on tea seed meal. They formulated the raw meal into a finer, proprietary blend of tea seed meal, kelp extract and composted , called Early Bird 3-0-1 Natural Organic Fertilizer, suited for golf course use. Caveats and limitations The goal of this research was to facilitate devel- opment of a natural product that can be used to alleviate the problem of excessive earthworm cast- ing on golf courses and sports fields. Early Bird is not labeled for earthworm control, although registration as a biological pesticide is being pur- sued. Since tea seed meal is a natural product, it is subject to variation in content related to genotype of the source plants, growing location, and how the raw material was processed, handled and stored (5). Early Bird is, to our knowledge, the only turfgrass fertilizer with tea seed saponins for which quality is monitored. Saponins are distributed in diverse plant spe- cies including many cultivated regularly consumed by humans (6,15). The saponins in tea seed meal have low acute oral and dermal toxicity for vertebrates including mammals and birds (15). Biodegradation is rapid, within three to five days in the field. High concentrations of saponins are toxic to fish, but tea seed meal is considerably less toxic to fish than some other products (for example, pyre- throid insecticides) regularly used on golf courses (13). With sensible guidelines (for example, buf- fer zones around ponds and streams, and no treat- ment of saturated soils where runoff could occur), it should be possible to use a tea seed meal-based product without harming aquatic organisms. An issue with earthworm expellants such as tea seed meal or mowrah meal is the unsightly nuisance and temporary odor when large num- bers of worms die on the surface. In our experi- ence, the expelled worms dry up relatively quickly and most of them are removed by mowing. The dried-up worms are less evident on fairways than on greens. Superintendents who tried Early Bird report removing expelled worms by mowing, with a backpack blower, vacuum, water hose or combi- nations thereof. The ideal remedy would provide economical long-lasting suppression of casting without killing the earthworms, but such a prod- Top: Crude tea seed pellets. Photo by D. Potter uct has not yet been found. Bottom: Early Bird fertilizer. Note the finer granules of the refined product.Photo courtesy of Ocean Organics Conclusions This research indicates that tea seed meal, a

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natural byproduct of tea oil manufacture contain- tion Green of the USGA 4:115–116. http://turf.lib.msu.edu/ ing natural surfactants called saponins, is effective gsr/1920s/1924/2405115.pdf (verified July 26, 2011). for expelling earthworms and suppressing casting 11. Piper, C.V., and R.A. Oakley. 1921. Earthworms. Bulletin of on playing surfaces. The mode of action is similar the Green Section Green of the USGA 1:75–82. http://turf. to that of mowrah meal, a mainstay for manag- lib.msu.edu/gsr/1920s/1921/210575.pdf ing earthworms on golf courses a century ago. Tea 12. Potter, D.A., A.J. Powell and M.S. Smith. 1990. Degrada- seed meal has been formulated into an organic fer- tion of turfgrass thatch by earthworms (Oligochaeta: Lum- tilizer (Early Bird 3-0-1) suitable for use on fair- bricidae) and other soil invertebrates. Journal of Economic ways and putting greens by Ocean Organics Corp. Entomology 83:203–211. Early Bird has been available since 2010. 13. Potter, D.A., C.T. Redmond, K.M. Meepagala and D.W. Wil- Most of the casting problems on North Ameri- liams. 2010. Managing earthworm casts (Oligochaeta: can golf courses are caused by non-native, invasive Lumbricidae) in turfgrass using a natural byproduct of tea earthworm species. Saponin-rich natural products oil (Camellia sp.) manufacture. Pest Management Science such as tea seed meal have promise as an alter- 66:439–446. native to off-label use of synthetic pesticides for 14. Potter, D.A., P.G. Spicer, C.T. Redmond and A.J. Powell. V alleviating the problems caused by excessive earth- 1994. Toxicity of pesticides to earthworms in Kentucky blue- v worm casts on low-cut playing surfaces. grass turf. Bulletin of Environmental Contamination & Toxicol- ogy 52:76–181. v Acknowledgments 15. Sparg, S.G., M.E. Light and J.V. Staden. 2004. Biological The authors thank A.J. Bixby-Brosi, C. Brady, J. Condra, C.P. activities and distribution of plant saponins. Journal of Eth- The research says Keathley, R. King, K. Meepagala, A.J. Powell, L. Williams and S. nopharmacology 94:219–243. Vanek for technical assistance; T. Bowyer and E. Lee for samples 16. Tennesen, M. 2009. Invasive earthworms denude forests in ➔ Earthworm casts create a of crude TSP used in preliminary tests; and W. Middleton and G. U.S. Great Lakes region. Scientific American Online. www. serious management problem in Seaver (Ocean Organics) for providing refined TSP formulations scientificamerican.com/article.cfm?id=invasive-earth- turfgrass on golf courses and sports and EarlyBird fertilizer for later trials. worms-denude-forests (verified July 26, 2011). fields, particularly under cool, moist 17. Williamson, R.C., and S.C. Hong. 2005. Alternative, non- conditions. Literature cited pesticide management of earthworm casts in golf course ➔ Cultural methods do not 1. Backman, P.A., E.D. Miltner, G.K. Stahnke and T.W. Cook. turf. International Turfgrass Society Research Journal adequately control the earthworms or 2001. Effects of cultural practices on earthworm cast- 10:797–802. their casts, and no chemicals are cur- ing on golf course fairways. International Turfgrass Society rently approved for earthworm control GCM Research Journal 9 :3 –7. in the U.S. 2. Baker, S.W., S.J. Firth and D.J. Binns. 2000. The effect of ➔ In the 1890s, British green- mowing regime and the use of acidifying fertilizer on earth- Daniel A. Potter ([email protected]) is a professor of keeper Peter Lees discovered that entomology, Carl T. Redmond is an entomology research worm casting on golf fairways. Journal of Turfgrass Science when mowrah meal, made from seeds specialist II, and David W. Williams is an associate professor of 76:2–11. of the butter tree of India, was applied plant and soil science at the University of Kentucky, Lexington. 3. Beale, R. 1908. The Practical Greenkeeper, 1st ed. J. Carter to turf and watered in, it acted as an and Co., London. expellant, forcing the worms to the 4. Beard, J.B. 2002. The art and invention era in the early evo- surface, where they were raked up lution of turfs 1830–1952. International Turfgrass Bulletin, and removed from the site. Sports Turf Research Institute 217:32–43. ➔ Recently, Chinese tea seed 5. Chaicharoenpong, C., and A. Petsom. 2009. Quantitative meal pellets, made from the seeds thin layer chromatographic analysis of the saponins in tea of the tea tree, have been shown to seed meal. Analysis 20:253–255. be effective in expelling earthworms 6. Cherian, K.M., V.M. Gandhi and M.J. Mulky. 1996. Toxico- and suppressing casting on turfgrass logical evaluation of mowrah (Madhuca latifolia Macbride) playing surfaces. Like mowrah meal, seed meal. Indian Journal of Experimental Biology 34:61– the pellets are made from a plant rich 65. in saponins, which may irritate the 7. Edwards, C.A., and P.J. Bohlen. 1996. Biology and Ecology earthworms’ skin. of Earthworms, 3rd ed. Chapman & Hall, London. ➔ Tea seed meal is now avail- 8. Kirby, E.C., and S.W. Baker. 1995. Earthworm populations, able in the U.S. as an organic turf- casting and control in sports turf areas: A review. Journal of grass fertilizer suitable for fairways the Sports Turf Research Institute 71:84–98. and putting greens. 9. Lees, P.W. 1918. Care of the Green. Wilcox, New York. Online. http://archive.lib.msu.edu/DMC/turfgrass/PDF/ careofthegreen.pdf (verified July 26, 2011). 10. Oakley, R.A. 1924. Earthworms. Bulletin of the Green Sec-

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