In search of allelopathy: an eco-historical view of the ... · During the second half of the ... isms, including their own species. Understand- ... ning of a renaissance for allelopathy

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Journal of the Torrey Botanical Society 131(4), 2004, pp. 343–367

In search of allelopathy: an eco-historical view of theinvestigation of chemical inhibition in California coastal

sage scrub and chamise chaparralRichard W. Halsey1,2

Southern California Chaparral Field Institute, P.O. Box 545, Escondido, CA 92033

RICHARD W. HALSEY (Southern California Chaparral Field Institute, P.O. Box 545, Escondido, CA 92033). Insearch of allelopathy: an eco-historical view of the investigation of chemical inhibition in California coastalsage scrub and chamise chaparral. J. Torrey Bot. Soc. 131. 343–367. 2004.—Allelopathy between plants, where-by one species influences another by chemical means, has been speculated upon since the Greeks. During thesecond half of the twentieth century, southern California was the focal point of allelopathic research by severalinfluential investigators. Frits Went suggested Encelia farinosa, a common desert shrub, inhibited annuals fromgrowing under its canopy by chemical inhibition. Reed Gray and James Bonner conducted further investigations.Cornelius H. Muller questioned the allelopathic explanation for Encelia, but later felt chemical inhibition wasthe cause for vegetation patterns found in both southern Californian coastal sage scrub, primarily around Salvialeucophylla and Artemisia californica, and Adenostoma fasciculatum (chamise) chaparral. Various investigatorschallenged Muller’s conclusions, but Muller remained convinced allelopathy was an important ecological variablein southern California’s shrublands. Muller’s passionate belief in his scientific models led him to ignore contraryevidence, yet his dedication to science and the education of his students inspired many. Allelopathy remains acontroversial topic today despite hundreds of investigations because of the difficulty in isolating all the possiblevariables affecting plant growth.

Key words: allelopathy, seed dormancy, coastal sage scrub, chamise chaparral, bare zone, chamise-fire cycle,multiple working hypotheses, bioassay.

Plants and microorganisms produce a varietyof chemicals, as byproducts of their metabolicprocesses, capable of either inhibiting or en-couraging the biological actions of other organ-isms, including their own species. Understand-ing allelopathy is an attractive research goal, es-pecially when considering its potential applica-tion to the commercial production of naturalherbicides.

The notion of plants influencing their neigh-bors has been around since the ancient Greeks.By the mid 1800’s, the hypothesis that plantsinfluenced each other by chemical means be-came widely accepted, especially after the workof French botanist, A.P. DeCandolle in 1832.Hans Molisch, an Austrian plant physiologist,introduced the term ‘‘allelopathy’’ to identify theprocess in 1937. The word is based on the Greekallelo meaning ‘‘one another’’, and path for

1 With sincere appreciation I would like to thank JonE. Keeley, Bruce Haines, and Robert Muller for pro-viding critical information for and editorial review ofthis manuscript. William Howell, Tom Chester, andMichael Barbour offered both assistance and encour-agement on previous drafts. I am also especially grate-ful to all those quoted within whom willingly offeredtheir personal recollections and perspectives on C.H.Muller’s investigations.

2 E-mail: [email protected] for publication February 2, 2004, and in

revised form April 29, 2004.

‘‘suffering’’ or ‘‘disease.’’ Molisch (1937) ap-plied a broader definition by including both neg-ative as well as positive impacts of chemical in-teractions occurring between plants, as well asmicroorganisms. However, by the time Molischcoined the word, the idea had lost considerablescientific support in favor of a different hypoth-esis explaining the causes of vegetation patterns;the depletion of soil nutrients by competition.Allelopathy became a troublesome variable forthe soil depletion model because it created anintolerable degree of uncertainty. It is difficultenough to develop conclusions about plant com-petition based on soil nutrients without worryingabout some unknown chemical interaction influ-encing experimental results. Consequently, thenotion of chemical influence was generally ig-nored. Yet the subject continued to be of interestto many and was given a new life in the desertsof southern California.

Desert Symbiosis. During field trips intosouthern California’s deserts, Caltech botanistFrits Went noticed there was a strong tendencyfor annual plants to locate themselves under ornear larger, woody species. For desert wildflow-ers, he felt physical factors, such as shading orsoil conditions, did not adequately account forthe germination and vegetation patterns he ob-served. Went decided to quantify his ideas in

344 [VOL. 131JOURNAL OF THE TORREY BOTANICAL SOCIETY

1942 with a study of two small shrubs. One, thedusty-gray Ambrosia dumosa (burro-weed) withlow growing, brushy stems, harbored an abun-dant array of annuals under its shady canopy.The other, Encelia farinosa (brittlebush), was anerect, sparsely stemmed shrub with little morethan bare ground below. If Encelia shrubs weredead, however, the frequency of annual growthbeneath its skeletal frame increased dramatical-ly. In discussing his observations, Went (1942)wrote,

. . . there is a specific effect of shrubs,which must be ascribed to specific materi-als given off by them. These materials seemto be produced especially by the livingshrub and they determine the specific oc-currence of definite annuals. No guess as tothe nature of these materials will be given;this can safely be postponed until experi-mental evidence is available.

The Substance. In 1948 Went’s investigationattracted the interest of plant physiologist JamesBonner, a Caltech colleague of Went. Bonnerpursued his interest by accepting a student’s re-search proposal to investigate the chemicalcause of Encelia’s inhibiting qualities. Workingin Bonner’s lab, Reed Gray analyzed the plant’sroots, leaves and chemical extracts in an effortto identify the toxic principle’s source.

Gray and Bonner (1948a) first tested the rootsby growing barley, tomatoes and Parthenium ar-gentatum (guayule) in sand next to Encelia. Nosignificant effects were observed. The next testinvolved placing various quantities of choppedEncelia leaves on the surface of sand in potscontaining young tomato plants. This time, afterwatering through the leaves for eleven days, in-hibition was observed. The greater the concen-tration of Encelia leaves, the less the tomatoplants grew. Interestingly, when the same ex-periment was tried with garden soil instead ofsand, the level of inhibition was reduced. In afinal test, 12-day-old tomato seedlings were ex-posed to an aqueous extract made from wholeEncelia leaves. All the plants died within threedays. When chopped leaf extract was used,three-fourths of the plants died within 24 hours.A comparable tomato leaf extract proved to havelittle affect on seedlings.

Gray and Bonner wrote, ‘‘The results pre-sented above show conclusively that there is apowerful inhibitor of growth of tomato seedlingscontained in Encelia leaves.’’ Adding later,

‘‘The presence of the growth inhibitor in theleaves of Encelia, may have ecological impor-tance in relation to the fact that only a few spec-imens of desert annuals are to be found growingin close relationship with the Encelia shrub onthe desert.’’

After further work, Gray and Bonner (1948b)isolated and synthesized the shrub’s toxic prin-ciple, 3-acetyl-6-methoxybenzaldehyde. Thesynthesized material demonstrated the same in-hibitory effects as the natural product. However,despite experimental results indicating a toxicaffect, the scientists maintained a healthy skep-ticism. They made clear that actual ecologicalapplications in the field remained untested.

A Paradox. With the soil nutrient depletionmodel dominating plant ecology, the notion ofallelopathy being responsible for desert vegeta-tion patterns attracted very little attention exceptfrom a young botanist named Cornelius H. Mull-er from the University of California, Santa Bar-bara. Based on his own experiences, Muller re-garded Gray and Bonner’s conclusions as ridic-ulous and decided to conduct a detailed study ofhis own with the intent of demonstrating thattheir laboratory results were artificial and did notapply to the field (Bruce Mahall, pers. com. June03). After extensive work, Muller published hisexperimental results and conclusions in 1953.Ironically, the young man’s decision to chal-lenge Gray and Bonner would mark the begin-ning of a renaissance for allelopathy and per-manently attach his name to the field.

C.H. Muller received his B.A. and M.A. inbotany at the University of Texas, Austin in1932 and 1933 and his Ph.D. in 1938, from theUniversity of Illinois. He established his earlyreputation by focusing on the genus Quercus(oaks), doing most of his work on species foundwithin Texas and northern Mexico. He was oneof the first investigators to recognize the pro-pensity for the genus to hybridize. Muller thor-oughly enjoyed collecting specimens and study-ing plants where they grew and placed a highvalue on detailed field observations. For him,understanding the individualistic environmentaltolerances and characteristics of species in na-ture was a fundamental part of any botanical in-quiry. Consequently, he saw Gray and Bonner’sreliance on sophisticated chemical and analyticallaboratory methods as overly narrow and too re-moved from the real world of plants to providemuch insight (Mooney 1999).

To produce evidence for his interpretation,

2004] 345HALSEY: HISTORICAL INVESTIGATION OF ALLELOPATHY

Muller (1953) expanded Gray and Bonner’s lab-oratory studies. In addition to watering tomatoseeds with Encelia extract, he included a com-panion experiment with an extract from the oth-er plant Went studied, Ambrosia dumosa (burro-weed). His results confirmed the toxicity of En-celia, but revealed an interesting paradox. Theextracted chemicals from Ambrosia, the plantharboring large numbers of desert annuals, weremore injurious to seedlings than the compoundsfrom Encelia. How could one species producingextremely toxic substances support ‘‘a miniatureflower garden’’ beneath its canopy whereas an-other, less harmful plant successfully inhibit allundergrowth?

Muller proposed a simple explanation for theinconsistency between lab observations andwhat was actually occurring in the field. Annualsfailed to grow under Encelia because of poorsoil conditions, not due to chemical toxins. Onthe other hand, Ambrosia encouraged annualsbecause of humus-rich soil that was producedfrom the accumulation of leaves dropping fromthe plant’s low hanging branches. Muller alsosuggested that toxic chemicals leaching into theground were irrelevant since soil microorgan-isms likely destroyed them before having an im-pact on germination. Gray and Bonner men-tioned the denaturing role of microbes in richsoils as well, but considered it unimportant sinceEncelia only grows in sandy, well-drained lo-cations. ‘‘Since shrub-dependent herbs will notgrow in the open except upon decaying remainsof former shrubs,’’ Muller wrote, ‘‘there is noreason to expect them to grow upon soil coveredby, but little changed by, Encelia.’’

In concluding his discussion of results, Mullerwrote an eloquent statement reflecting the diffi-culties in studying plant ecology.

The natural habitat, even in a relativelysimple community of the desert, is far toointricate a system of influences and factors,physical and biological, to hope that theremay be found a single factor controlling thecomplicated life of a perennial species. Anexplanation, when it is arrived at, will beat least as intricate as the situation it seeksto describe.

Muller’s paper was dramatically differentfrom Gray and Bonner’s in both objective andtone. While Gray and Bonner were following upWent’s investigations and narrowly focusing onone species, Muller widened the inquiry in orderto disprove a hypothesis. In doing so, he con-

tributed an important component of the scientificprocess: clarifying the reasons for an observedphenomenon by pointing out other variables ef-fecting experimental results. With the systematicprecision of a well-prepared district attorney,Muller presented his case and supported his hy-pothesis; soil conditions rather than plant toxinsdetermined the distribution of annuals. However,his prosecutorial style was not helpful in con-vincing others of his viewpoint. By implyingGray and Bonner were overly simplistic andfailed to understand the true complexities of thenatural world, Muller diverted attention awayfrom the scientific merits of his paper and to-ward personalities. It revealed an approach hewould use many times in the future when re-sponding to those with whom he disagreed, sub-tly characterizing their viewpoints as less thanenlightened.

‘‘Oh yeah, I remember him,’’ Reed Gray saidwhen reflecting upon his career in 2003. After abrief pause, he let out a soft laugh. ‘‘Yes, he wasthe guy who said we were all wet.’’

Unfortunately neither Gray nor Bonner pub-lished a response to Muller, but both men vig-orously disagreed with his conclusions (ReedGray, pers. com. July 03). Bonner’s opinion isespecially significant because of his reputationfor being open minded and willing to change ifpresented with convincing evidence. Frank Sal-isbury (1998), who went on to become a suc-cessful plant physiologist himself wrote, ‘‘Somescientists develop a hypothesis and defend it totheir deaths without flinching and in spite of anycontrary evidence that might appear. James wasnot cast in that mold. For him, only the truthmattered.’’

C. H. Muller published a follow up manu-script on desert allelopathy with a close, but un-related colleague, Walter Muller (Muller andMuller 1956). Their paper described further fieldresearch and experimental results confirming thepresence of toxins in desert plants but also theirineffectiveness as growth inhibitors in the field.Refining the statements Muller made in 1953about the importance of understanding the com-plexity of nature they wrote,

It should be emphasized that the naturalhabitat is a complex of physical and bio-logical factors that influence growth. Eventhough distributions may give the impres-sion of an antibiotic effect by some of theindividuals, careful investigation may in-dicate that the situation cannot be explained


in such a fashion. Environmental influencesand the metabolic activities of organismsare complex factors which are variously in-termingled, and in most cases it is doubtfulwhether any one factor would be distin-guishable as the primary causative influ-ence.

So it appeared allelopathy was once again rel-egated to its status as a rejected hypothesis. Itwould be a very short period of exile.

A New Set of Circumstances. Between1957–58 inquisitive students from the Univer-sity of California, Santa Barbara kept askingtheir botany professor about unusual bare zonesthey saw around stands of Salvia leucophylla(purple sage) during field trips to a coastal sagescrub plant community in the Santa Ynez Valley,northwest of campus. The ‘‘halos’’ of nakedground were so striking it was as if they hadbeen created by herbicide. Bare areas were ob-served around Artemisia californica (Californiasagebrush) as well. What was preventing plantsfrom growing in these zones? Could Salvia orArtemisia themselves be responsible?

The students’ professor was in a unique po-sition to evaluate the possibility because he wasalready familiar with allelopathy. He had justcompleted a major paper on the subject con-cluding it was not responsible for vegetation pat-terns elsewhere. But this was different. It was anew setting, a different group of plants. So dem-onstrating a remarkable level of intellectual flex-ibility, he decided to re-examine the possibilityand let the data speak for itself. The professor’sname was C. H. Muller.

As he had done with Encelia, Muller begancollecting large amounts of data from the fieldwith special attention to surrounding environ-mental conditions. But demands of the new en-deavor and his responsibilities at the universitywere consuming an inordinate amount of time,keeping him away from his family on weekends.So with the gentle urging of his wife Katherine,and recently available grant money, he hired anassistant, Bruce Haines, a friend of the familywho had just transferred to the University ofCalifornia at Santa Barbara as an undergraduate.Haines’ primary task was to travel out to thebare zone sites each weekend and collect data.Every Monday morning, Haines appeared inMuller’s office and was quizzed in detail abouthis observations.

‘‘The game became one of me trying to an-

ticipate all of his questions and come up withanswers before we met,’’ Haines (pers. com.May 03) recalled. ‘‘I would think it all throughwhile driving back from fieldwork on Saturdayor Sunday. It was pretty stressful at times, buthe really coached me well on how to become asuccessful observer and thinker. He taught mehow to do science, something I will always begrateful for.’’

Along with demanding accurate record keep-ing and directing his students to solve their ownproblems, Muller stressed Chamberlin’s modelof multiple working hypotheses, a process de-signed to help prevent personal attachment to afavored theory. ‘‘After awhile, I realized Mullerwasn’t interested in telling me what to do. Hewanted me to figure everything out for myself,’’Haines added. ‘‘He was constantly drilling intomy head Chamberlin’s model, reminding me thatI needed to keep emotions out of my work.’’

In a paper read before the Society of WesternNaturalist in 1889, Thomas C. Chamberlin(1890) described the critical role played by for-mulating multiple working hypotheses in dis-covering ‘‘new truths.’’ Chamberlin’s basic pointwas that if an investigator focuses on a single,original hypothesis, which seems to be satisfac-tory for a particular phenomenon, he has a ten-dency to view the explanation paternalistically.It becomes his ‘‘intellectual child.’’ Affectionsfor such a favored hypothesis become a blindinginfluence.

‘‘Love was long since represented as blind,’’Chamberlin wrote, ‘‘and what is true in the per-sonal realm is measurably true in the intellectualrealm. Important as the intellectual affections areas stimuli and as rewards, they are neverthelessdangerous factors, which menace the integrity ofthe intellectual process.’’ With experimental datain mind, he added, ‘‘There is an unconsciousselection and magnifying of the phenomena thatfall into harmony with the theory and support it,and an unconscious neglect of those that fail ofcoincidence. There springs up, also, an uncon-scious pressing of the theory to make it fit thefacts, and a pressing of the facts to make themfit the theory.’’

Muller’s rejection and then decision to re-ex-amine allelopathy as a cause for vegetation pat-terns demonstrated an important application ofChamberlin’s advice. He had not permanentlydiscarded the allelopathic model, but rather re-tained it within his own quiver of multiple work-ing hypotheses.


The Results. With Haines collecting in thefield, Muller finalized laboratory tests in thegreenhouses at UCSB. The experimental designwas not the same as his effort in 1953 with de-sert plants because he was hypothesizing a dif-ferent delivery system for toxic agents; evapo-rates into the air rather than rain-drip off leaves.

To set up appropriate germination tests or bio-assays to measure possible toxic effects, leavesof both Salvia and Artemisia were crushed andplaced in separate dishes. Moist filter paper rest-ing on a wire mesh an inch and a half above theleaves was sprinkled with cucumber seeds. Theentire arrangement was then covered and sealed.Two days later Muller et al. (1964) observed,‘‘In every instance volatile materials emanatingfrom the crushed leaves radically inhibited seed-ling root growth.’’ Bioassays using sliced in-stead of whole leaves on Cucumis sativus (cu-cumber) and Avena fatua (wild oat) seedsshowed similar results.

Muller recognized sealed containers in a labcould not replicate natural conditions in thefield, so he attempted to design a delivery path-way more closely resembling the natural distri-bution of volatile materials into the soil. He sug-gested dew formation.

By using cooling coils, dew was condensedfrom an atmosphere in which Salvia was grow-ing. The dew was then collected and used tosoak cucumber seeds. After several unsuccessfultrials, Muller was able to show reduced rootgrowth. He concluded, ‘‘Although field experi-mentation is still to be performed, it appears thatwhole plants of Salvia leucophylla release a vol-atile substance that condenses in dew and thatsignificantly inhibits the growth of cucumberroots.’’

The effect Muller was classifying as an alle-lopathic response in the field was dramatic. Hesuggested that the volatile substances from thesearomatic species appeared to be responsible forinhibiting growth of plants as far as 27 feetaway. If true, allelopathy in coastal sage scrubwould be considered one of the most remarkableecological interactions on earth.

The coastal sage scrub ‘‘bare zone’’ modelwas presented in Science under the title, ‘‘Vol-atile Growth Inhibitors Produced by AromaticShrubs.’’ The paper was considered importantenough to be the subject of the magazine’s coverphoto (Fig. 1). The picture is an aerial shot ofcoastal sage scrub stands of Salvia leucophyllaand Artemisia californica bordering grassland.Surrounding the clumps of sage were the char-

acteristic ‘‘halos’’ of bare ground. The photo’stitle read, ‘‘Chemical Plant Competition.’’

Along with Walter Muller, Bruce Haines waslisted as a coauthor to the 1964 paper, a signif-icant accomplishment for a young undergradu-ate.

Cowpaths. It was not long before others be-gan examining the data and making their ownconclusions, as Muller had done with Gray andBonner’s work several years before. In May,four months after publication, Philip Wells(1964) from the University of Kansas wrote acritique listing several alternative explanationsfor the bare zones, using details of the Sciencecover photo as a focal point. ‘‘The intercon-necting and in part rectilinear character of thenetwork of white lines does not suggest originby chemical inhibition,’’ Wells suggested. ‘‘Anequally good explanation is that most of themare cattle trails.’’

In referring to Muller’s suggestion that theshrubs were invading the grassland by way ofinhibiting grass plants, Wells pointed out the topcenter of the photo where there were over 100smaller shrubs scattered in the open grasslandwithout grassless ‘‘halos.’’ Why would isolatedbushes be without bare zones? Wells wondered.This suggested the halos actually appeared longafter Salvia had expanded into the grassland notas a preparatory step to their initial invasion.

Wells also noted what he saw as failures inMuller’s experimental design such as use of cu-cumber seeds instead of natives, testing proce-dures remote from field conditions, and ignoringthe impact of herbivores in bare zone creation.Ironically, the same criticisms Muller had lev-eled at Gray and Bonner. Wells concluded bysaying the idea of chemical inhibition emanatingfrom the sages was an interesting idea, ‘‘but itseems premature to imply that antibiosis rankshigh in the complex of ecological factors deter-mining the vegetation patterns depicted in thecover photograph.’’

As is often the case with criticisms of pub-lished papers, Muller and Muller (1964) weregiven the opportunity to write a response andhave it printed immediately below Well’s letter.The two men dismissed several of Wells’ criti-cisms as not pertinent and repeatedly made thepoint that their paper was only an initial reportproviding ‘‘scant space for monographic com-pleteness.’’ They also discounted concerns overthe lack of data relating to the role of cattle andherbivores because to include such information


FIG. 1. Cover Photo of Science, January 31, 1964. Mosaic pattern created by bare zones around Salvialeucophylla, S. apiana, and Artemisia californica. Reprinted with full permission from 1964 Science 143, cover.Copyright AAAS.


adequately would ‘‘require several pages and isbeing saved for the summary treatment, whichwill not be submitted until all possible factorshave, so far as is practical, been investigated,evaluated, and fitted into the complex.’’

Muller and Muller were not, however, willingto ignore the comment about cowpaths. They de-scribed observations comparing the presence ofcow droppings between grassland and barezones revealing more per square meter in ‘‘re-mote uninhibited grassland’’ than any other lo-cale. ‘‘It is clear from these figures,’’ they wrote,‘‘that cows go where grass is and that they donot linger about shrub patches trampling downdepauperate herbs over wide areas. . . The greatbroad white zones of bare ground both insideand outside the shrubs are curved (not ‘‘rectilin-ear’’) and can scarcely be explained except asinhibition.’’ The roles of smaller herbivores suchas sparrows were dismissed as well because‘‘never do they produce a bare area unaided byinitial biochemical inhibition’’ (italics added).

In their response, Muller and Muller weretreating biochemical inhibition as a forgone con-clusion. According to their interpretation, inhi-bition was the only reasonable explanation forbare zone formation, a pattern that ‘‘never’’ oc-curs without it. In defending their hypothesiswith such determination, they were demonstrat-ing a confidence unjustified by available data.‘‘The criticism,’’ they continued, ‘‘that cowpathsare visible within the shrub zone and may there-fore be responsible for the patterning involvesthe most surprising failure to observe. Steps arebeing taken to preserve an area of the more in-structive patterning. We are desirous of showingthis to anyone who will look.’’

Wells had looked and came away with a dif-ferent viewpoint. What was not revealed was theintimate awareness Wells had with not only thesite but also Muller’s investigation. Wells (pers.com. May 03) had been Muller’s sabbatical re-placement in 1958. He spent time in the summerof 1959 with Muller in Happy Canyon, the SantaYnez Valley study site, debating the cause of thebare zones and the role of herbivores.

‘‘He playfully asked me why the bare areassurrounded the soft chaparral,’’ Wells remem-bered. ‘‘From the start I said it was due to ani-mal activity, and he just smiled in his fatherlyway. He had a good four years to think aboutthe role of animals, but chose to ignore it.’’

Although the ‘‘cowpath’’ explanation wouldultimately prove to be wrong, the possibility ofother animal activity was important enough to

warrant more consideration than Muller accept-ed. Muller also neglected factors he suggestedin 1956 as capable of eliminating the effective-ness of inhibiting chemicals such as ‘‘microbialactivity, adsorption to soil colloids, or inactiva-tion under xeric (dry) conditions.’’ The omis-sions are especially curious in light of his criti-cism of Gray and Bonner’s work, suggesting, ashe said, a ‘‘single factor’’ capable of controllingvegetation patterns under Encelia. By discussingonly chemical variables in his paper, Muller’sscientific methodology and conclusions werevulnerable to the same weaknesses he criticizedeleven years before.

Further Clarification. Muller (1965) contin-ued his research by isolating the volatile terpenecompounds in Salvia and identifying them ascineole and camphor. He realized the artificialdew technique was not the best model for thenatural deposition of these compounds so hesearched for another. Since both cineole andcamphor have a high affinity for oils, Muller hy-pothesized the compounds could adsorb or col-lect on the surface of the fatty cuticles of nearbyseedlings directly from the atmosphere, inhibit-ing or terminating their growth. This contrastswith absorption, where a substance is pulled intosome region rather than remaining on the sur-face. He experimented by exposing paraffin waxto crushed Salvia leaves and found the solid waxreadily adsorbed the volatile terpenes from theair. The direct adsorption model appeared morerealistic because volatile compounds would bemuch more concentrated during warm tempera-tures in the summer than during cooler, dew-producing periods.

However, with additional research, Muller re-jected this hypothesis as well. In a paper coau-thored with Roger del Moral in 1966, it was sug-gested the volatile compounds were adsorbed bycolloidal particles in the soil first. The toxinswere then dissolved by the first winter rains andadsorbed by the seedlings. Their supporting ex-periments were straightforward and clearly dem-onstrated soil adsorption of terpenes releasedfrom Salvia leucophylla. Muller and del Moral(1966) hypothesized that during late spring andsummer months, when the aroma of sage is mostobvious, toxic terpenes collect on the surfacesof soil particles and remain unchanged untilmoisture dissolves them. As seedlings germi-nate, the toxins are transported through cellmembranes and into the plant body, inhibiting


or terminating growth, possibly through the sup-pression of mitosis.

In contrast to the response to Wells and morein keeping with the multiple working hypothesismodel, Muller and del Moral included a clearstatement regarding the impact of variables otherthan allelopathy.

It must be emphasized, however, that inhi-bition by ‘last year’s’ terpenes may be onlyone of a series of factors subtly interplayingto produce the observed patterning of herbsabout Salvia shrubs. Perhaps a combinationof several factors is necessary to producethe phenomenon. We have a high degree ofconfidence that Salvia terpenes are a man-datory condition, but we would not be sur-prised if small animal activity, soil type,semi-arid climate, and the like proved atleast significant contributors to the phe-nomenon.

Muller published his full description of sagescrub allelopathy in the fall of 1966, providingan excellent summary of his work thus far. Hepresented detailed descriptions of both labora-tory and field work and speculated upon the or-igin of allelopathic compounds. As a testamentto his resourcefulness, Muller was able to obtainthe first gas chromatograph on campus, normallythe domain of the chemistry department. Thisallowed chemical analysis of the vapors pro-duced by Salvia. Factors concerning bare zonepatterns were also delineated. The width of eachzone on the uphill side of a Salvia thicket wasabout equal to those on the downhill side. Thiswas considered evidence supporting vapor trans-port of allelochemicals rather than moisture be-cause water would wash toxins off the plant andsend them down slope.

Unfortunately, the precise techniques used tomeasure the effects of animals continued to re-main vague despite reassurances they remainedan ongoing research focus. After describing asimple transect observation showing minimal ef-fects from grazing, Muller (1966) briefly con-cluded, ‘‘although grazing by small animals mayaugment the effect of differential inhibition, it isnot capable of initiating or maintaining unaidedthe observed phenomenon. Our study of animalinfluences continues with increased emphasis.’’

In speculating upon the evolutionary historyof inhibitory mechanisms, Muller suggested‘‘that all, or at least most’’ of plant-producedinhibitors, ‘‘originated as metabolic by-productsof the plants in which they are found, regardless

of what functional role they may now play.’’ Inorder to rid themselves of such by-products,plants such as Eucalyptus and Salvia producehighly volatile compounds that are released intothe atmosphere in large quantities. The possibil-ity of inhibiting a competitor, resisting a patho-gen, or repelling a browsing animal with suchexcretions is an ‘‘added advantage.’’

Volatile substances released by Salvia andother aromatic shrubs in coastal sage scrub arecomplex compounds. In terms of energy re-quired for a plant to produce them, they are quiteexpensive. This suggests there may be reasonsother than simple excretion of wastes to accountfor their presence (Bruce Mahall, pers. com.June 03). Proving original causation for anyplant or animal trait, however, is extremely dif-ficult if not impossible. Such thoughts wouldseem to be relatively unimportant when consid-ering the entire allelopathic model, but Mullerwas willing to mount a passionate defense whenquestioned. Dennis Breedlove and Paul Ehrlich(1969) experienced Muller’s intensity when theybriefly referenced his view discounting ‘‘the pri-mary role of plant biochemicals as herbivorepoisons’’ in a short article discussing predationon lupine flowers by butterfly larvae.

After calling Breedlove and Ehrlich’s notationof his idea ‘‘irrelevant’’ to their article, Muller(1969a) added, ‘‘I appreciate their publicizingmy viewpoint on this basic evolutionary ques-tion, but I feel that the isolation of this referencein a report on a subject so slightly related mustnecessarily have left most readers wonderingwhy it was included at all.’’

After discussing evidence supporting hisviewpoint, Muller concluded, ‘‘. . . the toxicityto animals of these metabolic wastes, no matterhow important eventually, is subsequent andsecondary to their elimination from protoplasm.No useful purpose is served by simplifying thisexplanation beyond the limits of reality.’’

Finding Allelopathy in the Chaparral.Convinced allelopathy accounted for vegetationpatterns in coastal sage scrub, Muller and twoof his students, Ronald Hunawalt and James Mc-Pherson (1968) turned their attention to anotherfamiliar phenomenon, the lack of herbs undermature stands of chaparral and the sudden surgein seed germination after fire. ‘‘It is quite clear,’’they wrote, ‘‘that, except for the bulb-formingperennials, the explosive herb growth withwhich we are concerned has its basis in tempo-


rary relief from some control of seed germina-tion.’’

For Muller’s team, the ‘‘control’’ was mostlikely chemical because the bare zone phenom-enon found in coastal sage scrub also appearsunder and adjacent to chaparral shrubs. In ref-erencing an unpublished study from his lab oftwo common manzanita species, Muller et al.wrote, ‘‘Among the non-aromatic chaparralshrubs, Arctostaphylos glauca and A. glandulosahave recently been studied in detail and shownto inhibit herbs for a distance of 1 to 2 m fromthe edge of the drip lines of their canopies.’’

However, instead of merely inhibiting growthof herb and shrub seedlings as hypothesized forbare zone allelopathy in sage scrub, Muller et al.proposed a distinctly different model for chap-arral, the suppression of seed germination by al-lelopathic compounds. Since chaparral shrubs donot release volatile chemicals into the air, as isthe case for coastal sage scrub species like Sal-via, another mechanism was needed to accountfor the transport of toxins. Muller and his stu-dents found it in water-soluble compounds onthe foliage of dominant chaparral shrubs likeAdenostoma fasciculatum (chamise) and Arcto-staphylos glauca (Eastwood manzanita). Theyproposed the same delivery system Gray andBonner suggested for Encelia, water falling offleaves and stems during rainstorms. They sug-gested that toxic compounds washed off plantsand accumulated in the soil, thereby chemicallyinhibiting seeds from germinating. When fireswept through chaparral, toxin-producing shrub-bery was removed, toxic leaf litter burned away,and accumulated soil toxins were denatured byheat. No longer chemically restrained, seedswere free to germinate as soon as water was de-livered during the next rainstorm, causing thepost burn environment to explode with wild-flowers and shrub seedlings.

In reviewing their preliminary findings, Mull-er et al. wrote, ‘‘The chaparral fire cycle thusemerges as a sequence of events consequent tothe destruction of toxins and their shrub sourcesby fire. This is followed by the germination ofseeds no longer inhibited by shrub toxins.’’ Af-ter reviewing additional details, they concludedconfidently ‘‘allelopathy is the primary basis ofthe herb fire cycle in California chaparral.’’ Mc-Pherson and Muller (1969) published a completereport on what later became known as the‘‘chamise-fire cycle’’ model the followingspring.

McPherson and Muller’s first task was to

eliminate variables other than chemical. Afterconducting experiments and concluding nutrientdepletion, shading, moisture and oxygen levelsin the soil were not significant factors in pre-venting germination, they turned their attentiontoward fire. Soil under chamise shrubs was col-lected (with leaf litter removed) and heated atvarious temperatures then watered. As temper-ature levels were raised, more seedlingsemerged, with the greatest increase in germina-tion appearing between 80–908 C (175–1958 F).‘‘Since heating of the soil and litter mass whichcontains the seeds brings about increased ger-mination,’’ McPherson and Muller concluded,‘‘it is strongly suggested that the heat degradessome substance in the soil which otherwise sup-presses germination.’’

To eliminate soil as a variable and test theeffect of heat alone, seeds of nine native specieswere heated in ovens and allowed to germinateon wet sponges covered with filter paper. Afterrunning experiments at three different tempera-tures (708, 808, 908C, plus a control), McPhersonand Muller wrote, ‘‘No species found to be stim-ulated to germinate in the soil heating experi-ment could be so stimulated by direct heating ofits seeds.’’

The largest portion of their study focused onestablishing the level of toxicity of suspectedchamise allelochemicals. Bioassays were con-ducted in a manner similar to those used in pre-vious experiments. All parts of the plant weretested, but leachate of intact aerial portions(leaves on branches) provided the most positiveresults. The solutions were prepared by sprin-kling water over chamise foliage and concen-trated to various strengths. Although seeds treat-ed with normal leachate and then concentrated1.3 times did show slightly depressed growthpatterns, the results failed to demonstrate statis-tically significant differences when compared toseeds moistened with plain water. However,when concentrated 4 to 10 times, leachate col-lected during natural rainfall reduced growth ofBromus diandrus (rip-gut grass) seedlings 34%to 75% respectively. Since B. diandrus (speciesnames reflect current taxonomy after Jepson1993) is non-native and typically not foundwithin undisturbed sites, additional bioassayswere attempted with native herbs but the testswere rendered meaningless by mold growth.

The important question of whether or notleachate actually inhibited germination, as Mull-er’s hypothesis suggested, was not resolved.

To measure the effect of shrub cover removal


Table 1. Seedling data collected under shrub cover from exclosure experiments to examine animal effects.Adapted from McPherson and Muller (1969).

SiteInside fenced control

plots under shrubsOutside fenced area

under shrubs

Large exclosure Site IIISmall exclosures Site IIILarge exclosure Site IV

71 seedlings/m2

70 seedlings/m2

20 seedlings/m2

11 seedlings/m2

11 seedlings/m2

4 seedlings/m2

without fire, a clearing test was conducted. Four6 3 6 meter quadrants of chamise were carefullypruned all the way to the ground. The clearingswere fenced to prevent small animals from en-tering. Adjacent to each clearing was anotherfenced plot with undisturbed brush to act as acontrol. After the first rains Muller and Mc-Pherson said they observed an ‘‘explosivegrowth of native herbs’’ in the clearings, aver-aging 1000/m2, ‘‘presenting an aspect strikinglysimilar to that of first-season herb growth fol-lowing a burn.’’ In the control plots under theshrubbery, few seedlings were found, averaging40/m2. McPherson and Muller concluded the re-sults fit in well with their chamise-fire cyclemodel; due to the removal of the chamise, toxinswere no longer added to the soil and their effec-tiveness was drastically reduced by ‘‘mild heat-ing or by passage of time and simple exposureto rain and sun.’’

Unfortunately the clearing data was only pre-sented as a list of species rather than a quanti-tative measure of abundance. Disturbed areasalong roadsides can have similar densities of an-nual species with occasional post fire endemics,but their composition has no relationship to fire.It is impossible to tell if the ‘‘explosive growth’’was dominated by only a few weedy species likeFilago californica and Conyza canadensis(horseweed) or some other combination (Jon E.Keeley, pers. com. July 03). Without quantita-tive data, the actual impact of artificial shrubclearing remained ambiguous.

The test did provide, however, some insightconcerning another variable, animal activity. ‘‘Asurprising feature of the clearing experiment,’’they wrote, ‘‘was the relatively large number ofherbs in the fenced control areas where theshrubs were intact.’’ The description ‘‘relativelylarge’’ was used in reference to their expectationthat ‘‘none would be present.’’

To examine the effects of animals, samples ofherb populations were taken both inside and out-side the fenced control areas. The data showeda significant difference between the two areas.At one site in an eleven year old stand an av-

erage of seventy seedlings were found persquare meter within the fenced plots as opposedto eleven seedlings per square meter in unpro-tected areas. Investigating further, they set up anadditional experiment with five small exclosures(160 3 160 3 80) between chamise shrubs. Un-like the larger exclosures, these were completelyenclosed with mesh hardware cloth on top aswell as along the sides. After an unspecified pe-riod of time, seedlings were counted, showingremarkably similar results to the first data set(Table 1).

It was clear, McPherson and Muller wrote,‘‘that small animals have an impact upon seed-ling populations.’’ However, the data were dis-missed as relatively unimportant with a briefsentence. ‘‘The same results show that some ef-fect of the shrubs themselves is by far the pre-dominant influence.’’

Their opinion was based on analysis of datafrom their large exclosure experiments; areascleared of shrubbery and ‘‘poorly protected’’against little animals produced over 1000 herbsper square meter, whereas ‘‘well protected’’plots under the cover of shrubbery only pro-duced about 70 herbs per square meter ‘‘whichwere stunted, depauperate, and failed to ma-ture.’’ The chaparral shrubbery, they concluded,was responsible for the depressed herb numbers.

While something different was obviously go-ing on to allow so many seedlings to germinatein the clearings, were the exclosure experimentsproperly evaluated? Was fencing effective ineliminating animal activity as a significant var-iable? Were animals spending as much time inthe clearings as they were under the shrub cov-er? Was the composition of plant species in theclearings reflective of actual post-fire flora foundin the local area? Would another investigator, aplant physiologist or mammalogist for example,have interpreted the data in the same way?

It wasn’t long before someone else decided tofind the answers.

The Question of Herbivores. In 1970, BruceBartholomew, a graduate student at Stanford


University, published a short paper in Sciencere-examining the cause of bare zones aroundSalvia in coastal sage scrub. Although Mulleracknowledged animals played some role in themaintenance of these areas, he insisted theywere not involved in their origin; allelopathywas the primary causative agent of the ‘‘halos’’around certain coastal sage scrub species.

Bartholomew (1970) offered an alternativeview. ‘‘In California, the chaparral and coastalsage shrubs form excellent cover for rodents,rabbits, and birds. The adjacent grassland pro-vides poor cover for most of these animals yetfurnishes an excellent food supply for grazersand seedeaters. One would expect then that feed-ing activity of these small animals would beconcentrated in grassland areas immediately ad-jacent to stands of shrubs.’’

To little rodents like Peromyscus californicus(California mouse) and Dipodomys agilis (pacif-ic kangaroo rat) the world is a dangerous place.Cover is critical to their survival since they areon the dietary preference list of local carnivoreslike coyotes and hawks. Consequently, theyhave a tendency to remain under shrubbery withonly occasional, quick forays into the grasslandto nibble on available seeds and new growth.They will stray only as far as they can quicklyleap back to safety. Bare zones, therefore, canbe viewed as ‘‘calculated-risk terrain’’ where ro-dents have a fair chance of grabbing food with-out getting caught. And since boundaries be-tween two different habitats are often the richestin terms of food resources, mammal activity ishighest where shrubbery abuts grassland (Chris-tensen and Muller 1975b).

To test his theory, Bartholomew set up feed-ing stations and traps to determine where ani-mals spent their time within the shrub/grasslandinterface zones of southern California’s Los An-geles County and the more northern county ofSan Mateo. After collecting his data, he foundsignificantly more seed was eaten and animalscaptured in bare zones than in the adjacent opengrassland. To test whether or not there wasenough animal activity to produce or maintainthe ‘‘halos’’, Bartholomew set up various typesof one-foot square exclosures in both grasslandand bare zone areas. Some exclosures were total,excluding herbivores completely, while otherswere open on the sides as controls for the effectsof shading and dew formation caused by exclo-sure materials. After a two-year study, areas pro-tected from herbivore entry showed significantplant growth when compared to unprotected ar-

eas (Fig. 2). ‘‘The extent of the relative contri-bution of chemical and animal inhibition of theformation and maintenance of the bare zone,’’Bartholomew wrote, ‘‘needs further investiga-tion. However, annuals will grow in the barezone with either the presence or absence of vol-atile toxins if animal activity is excluded.’’

Noteworthy, in terms of speculation, is howBartholomew phrased his conclusions. Heavoided saying allelopathy did not exist and thatbare zones were primarily the work of herbi-vores. Rather, he reported his data and left themore general question of causation open to fur-ther debate.

Muller was not impressed. He wrote a letterto Bartholomew’s department at Stanford ques-tioning the appropriateness of permitting a grad-uate student to publish a paper questioning sucha well-known and well-documented case for al-lelopathy. The following summer Muller sub-mitted a formal response in Science with his for-mer student Roger del Moral, who was thenworking at the University of Washington. Theylisted ten additional observations not mentionedin previous papers as supporting a minimal rolefor herbivores, and characterized Bartholomew’sperspective as short sighted. Muller and delMoral (1971) wrote, ‘‘. . . we have tried to dis-suade readers from accepting any simplistic ‘sin-gle-factor’ explanation of the phenomenon, andhave admitted repeatedly that even phytotoxinsfail to control in some situations. We hold thatBartholomew’s and our experiments combinedpermit no definitive characterization of animalroles.’’

Again, reminiscent of Muller’s earlier criti-cism of Gray and Bonner they concluded,‘‘There is no universal solution to a problemwith so many variables, and certainly there is noacceptable simplistic one.’’

Bartholomew had not suggested animals werethe ‘‘universal solution’’ for bare zones. He hadonly presented data showing annuals will growin areas protected from their activity. This wasin contrast with some of the definitive statementsMuller was making, implying the primacy of al-lelopathy above all other variables. Although heclearly did not believe ecological phenomenacould be explained by a single factor, Muller’sspirited defense of his work and zeal to promotechemical inhibition as an important process gavethe impression allelopathy was all that reallymattered in determining chaparral and coastalsage scrub vegetation patterns. The contradiction


FIG. 2. How Fencing Affects Bare Zone Formation. Exclosures preventing entry by herbivores resulted in asignificant increase in herbaceous growth within protected areas. Photo taken in the Santa Ynez Valley, SantaBarbara County, California in 1968. Photo provided by J.E. Keeley.


between these two positions was an issue Bar-tholomew (1971) alluded to in his rebuttal.

Muller and del Moral appear to agree withthe position I expressed in my report: ‘Theextent of the relative contribution of chem-ical and animal inhibition to the formationand maintenance of the bare zone needsfurther investigation.’ It is likely that thisoverall question has no universal answereven for a single kind of shrub at a givenlocality, much less for different shrubs indifferent localities. Thus to insist on, forexample, chemical inhibition as a universalanswer for such a phenomenon would un-doubtedly be unwarranted. Although vola-tile plant toxins might be the main factor inthe production and maintenance of the barezone and inhibition zone adjacent to somespecies of shrubs, an interaction of otherfactors will produce the same results in cas-es such as that of Baccharis pilularis (chap-arral broom) which lacks volatile plant tox-ins.

Bartholomew stressed the importance of hold-ing ‘‘constant as many factors as possible and tomeasure the effect of single variables.’’ Becausehis own data provided evidence this was notproperly done in earlier work he concluded,‘‘All of the points presented by Muller and delMoral as evidence for chemical inhibition couldbe subjected to experimentation. However, aspresented the points are not conclusive evidencefor chemical inhibition.’’

At the invitation of Muller’s students, Bar-tholomew came to UC Santa Barbara to discusshis data and view the study sites on his way toBaja California. Arriving with his major profes-sor Hal Mooney and several other graduate stu-dents in the department’s field van, Bartholo-mew participated in lively conversations com-paring data and perspectives. Muller himselfwas not present during the discussions and tooka dim view of the entire affair, becoming angrywith his students for arranging it. He viewed itas Stanford University questioning the quality ofhis work as a scientist, rather than a theory’svalidity. To the students, the visit marked a turn-ing point in their analysis. After examining theavailable information, consensus was reached.Bare zone formation and maintenance was pri-marily the work of animals, not chemicals.

‘‘I was in Washington when Bartholomewcame down, so I wasn’t part of the discussions,’’del Moral (pers. com. June 03) said later. ‘‘But

looking back, we didn’t fully appreciate the syn-ergistic actions of all the variables.’’

The Turning Point. By the time of Barthol-omew’s research in 1970, Muller and his stu-dents had applied the concept of allelopathy toexplain a wide range of vegetation patterns inCalifornia including:—The succession of grasslands by aromatic

shrub species such as Salvia leucophylla andArtemisia californica through the release ofvolatile inhibitors, known as the coastal sagescrub ‘‘bare zone’’ model. Other commonspecies identified as toxic and capable of in-hibiting growth around them included Salviaapiana (white sage), Salvia mellifera (blacksage), Heteromeles arbutifolia (toyon), Pru-nus ilicifolia (holly-leafed cherry), and Arte-misia tridentata (Great Basin sagebrush)(Muller 1966).

—The ‘‘deteriorated interiors of older stands’’ ofSalvia leucophylla and Artemisia californicacaused by the concentrated release of volatiletoxins (auto-toxicity) (Muller 1966).

—The suppression of germination under thecanopy of Adenostoma fasciculatum (chami-se) chaparral (McPherson and Muller 1969).The dramatic post-fire bloom of herbaceousspecies is the result of heat denaturing alle-lopathic chemicals in the soil and the elimi-nation of toxin-producing shrubbery (Mulleret al. 1968). This explanation has been iden-tified as the ‘‘chamise-fire cycle’’ model.

—The exclusion of certain herb species fromgrasslands by chemical inhibitors released asdecomposition products of grasses like Avenafatua (wild oats) (Muller 1966).

—The invasive nature of Brassica nigra (blackmustard) (Muller 1969). With David Bell, hesuggested rainwater leachate from dead blackmustard stalks and leaf material containingtoxic chemicals could account for the plant’spure stands and the bare zones around them.Their experimental data was based on con-centrated rainwash solutions and bioassays asused in previous investigations (Bell andMuller 1973).After 1970, the swirling controversy over the

significance of herbivore activity and the ques-tionable strength of some earlier experimentaldata forced a more critical examination of alle-lopathy by Muller’s students. Pat Halligan revis-ited the ‘‘bare zone’’ model and Norman Chris-tensen investigated the question of herb sup-pression within chamise chaparral.


Examining the toxicity of Artemisia califor-nica between 1970 and 1972, Halligan (1976)investigated two coastal sage scrub sites nearSanta Barbara; one off the mountainous roadthrough San Marcos Pass and the other at LaPurisima Mission near Lompoc. Studying the‘‘halo’’ areas made famous by Muller’s originalpaper, Halligan focused on four herb species forevidence of chemical inhibition: native Madiasativa (coast tarweed), and non-natives Hypo-choeris glabra (smooth cat’s-ear), Bromus dian-drus (rip-gut grass), and Vulpia myuros (fescuegrass).

The important difference between Halligan’swork and previous efforts was his experimentalmethodology. Six different materials were testedas seedbeds for germination studies as opposedto just one, revealing an important variable pre-viously unexamined, the effect of the growthmedium on seedling health. Halligan discoveredthat the cellulose sponge underlying the filter pa-per used in Muller’s lab was actually toxic toseeds. By replacing the sponge with cheeseclothand rinsing the filter paper before use, Halliganwas able to find a more neutral media. ‘‘All oth-er seedbeds,’’ he reported, ‘‘presented problemsof toxicity or excessive variability with one ormore of the bioassay species.’’

Using animal exclosures similar to Bartholo-mew’s, Halligan (1973) also examined the ef-fects of small herbivores. ‘‘By the end of thegrowing season, the grasses had grown to nor-mal size in the closed exclosures, but had beentruncated at ground level in the open exclosu-res.’’ In an additional test, a 48 3 60 ft. pro-tected zone was set up ‘‘extending from withinthe shrub zone to well within the grassland’’ andwas ‘‘trapped extensively for small mammals.’’After one year, grassland invaded nearly 1½ feetinto the bare zone. Outside the fence, grassesactually regressed from the shrubs, increasingthe bare zone by more than 2 feet. Rabbits lefttheir tell-tale feces in abundance where the barezone widened. ‘‘These experiments and obser-vations,’’ Halligan concluded, ‘‘strongly suggesta central role for small mammals in causing thebare aspect around stands of A. californica.’’ Incommenting on the Muller/Bartholomew contro-versy Halligan suggested both men were correctin their studies regarding the influence of alle-lopathy and herbivores respectively, but bothoversimplified herb distribution patterns andoverrated their individual theories.

Regarding the allelopathic potential of Arte-misia, Halligan’s 1976 data suggested the plant

produced terpene toxins capable of inhibitingherb growth when applied at natural concentra-tions. The hypothesized mechanism of transportof volatile compounds was the same as Muller’s,from leaves to air to soil to seed. His tests alsosupported Muller’s contention that toxic effectswere strongest during the first rain. The toxinsdisappeared entirely by early spring.

‘‘Some plants were difficult to grow in thesoils I collected before the rains,’’ Halligan(pers. com. July 03) recalled, ‘‘but by earlyspring I could grow almost anything.’’

From Halligan’s bioassays, Hypochoeris gla-bra and Madia sativa were much more inhibitedby toxins of Artemisia californica than Bromusdiandrus and Vulpia myuros. In exclosure ex-periments, designed to minimize herbivore ac-tivity, H. glabra and M. sativa also appeared tobe inhibited in the shrub zone. B. diandrus, onthe other hand, grew freely in the shrub zone,especially when protected from grazing (thiscontradicted earlier data from Muller and hisprevious students showing toxins inhibited B.diandrus). From his experimental results, Halli-gan concluded his original hypothesis was cor-rect; some plant species are allelopathically ex-cluded from thickets of A. californica while oth-ers are not.

In narrowing the scope and application of hispaper, Halligan wrote in 1976, ‘‘I have foundgreatly varying responses of bioassay species toalmost every material bioassayed.’’ After listingseveral examples, he continued, ‘‘Knowing thateach species reacts to toxins in its own uniqueway, it would seem to be of paramount impor-tance to use those species which are directly in-volved with the vegetation pattern under study.However, in the literature I find many examplesof the use of irrelevant species being used forbioassays, such as ‘oak leaf’ lettuce, radishesand Cucumis sativus. These species are of rele-vance mainly to farmers, not naturalists. The no-tion that one species’ response can be extrapo-lated to other species is untenable, as indicatedby the great disparity of response between spe-cies in this article.’’

In closing, Halligan acknowledged that al-though his ideas contradicted Muller’s conclu-sions ‘‘regarding the relative importance of graz-ing and allelopathy’’ some of Muller’s ‘‘recentviews are no longer completely opposite thosein this article.’’ The ‘‘recent views’’ referred towere from a paper written by Norman Christen-sen and Muller in 1975.


The Chamise-fire Cycle. Christensen wasone of Neil Muller’s last graduate students. Inre-examining some of the data published by Mc-Pherson and Muller (1969) on chamise chapar-ral, Christensen designed several innovative ex-periments to test variables controlling germina-tion and seedling growth. He also did somethingmissing from the previous investigation, a directcomparison between a burned and unburnedstand of chamise in the Santa Ynez Mountains,northwest of Santa Barbara.

In one series of experiments, eight test plotswere established under the chamise canopy toexamine the effect of four factors: animal activ-ity, soil heating, additional nutrients, and heatingplus nutrients. As had been the case before, theherbivore component presented particular chal-lenges.

‘‘When trying to isolate areas to eliminate an-imal interference,’’ Christensen (pers. com. May03) recalled, ‘‘we kept catching rodents over andover in traps within exclosures designed to keepthem out. Their ability to get over fencing hadbeen completely underestimated.’’

The resulting paper was different from anyother in which Muller participated; animals wereacknowledged as playing a central role. ‘‘Therecan be little doubt from these data,’’ Christensenand Muller (1975a) wrote, ‘‘that animal grazingplays a very significant role in seedling survivalin chaparral. It appears virtually certain that anyunprotected seedling, not succumbing to someother malady, will eventually be eaten.’’

Although allelopathy was still the primary fo-cus, it was no longer being treated in such anexclusive manner, but rather as one of severalvariables.

It may be concluded that numerous ecolog-ical factors associated with the chaparralunderstory result in an extremely low prob-ability of seedling survival. Among theseare animal grazing, low soil fertility, planttoxins, and, perhaps, low light levels. Fol-lowing fire, the negative effect of each ofthese factors is removed or reduced.

In further studies to evaluate the effects of fireon animal grazing, Christensen and Muller(1975b) placed trays of Bromus diandrus seed-lings approximately two inches high in burnedand unburned chamise stands. After 24 hours,seedlings under the chaparral canopy were com-pletely eliminated, grazed to the ground. Thosein the burn area were untouched. A likely ex-planation for the difference is the same as that

which Bartholomew suggested for grass growthoutside the bare zones around Salvia: small an-imals avoid open spaces to limit exposure topredators.

When examining the effects of fire, Christen-sen’s data initially confirmed McPherson’s re-sults by demonstrating, ‘‘heat treatment of soilsignificantly affected overall germination.’’However, in a later set of experiments, whereheat was examined separately from soil, the testresults diverged from McPherson’s. Employinga much wider range of temperatures and heatingtimes, Christensen found two of the nine specieslisted as unresponsive to heat by McPherson ac-tually showed dramatic increases in their ger-mination rates when subjected to both 1008 and1208 C (210 and 2508 F): Lotus scoparius (deer-weed) and chamise.

Christensen’s results indicated heat alone wasmore significant than previously thought. Fur-ther, he revealed an important measurement thatseriously questioned one of the primary assump-tions of the ‘‘chamise-fire cycle’’ model, namelythat heat from fire denatures inhibiting chemi-cals. By using chromatographic analysis, Chris-tensen discovered the concentration of suspectedallelopathic toxins was actually greater inburned soils rather than less.

When preparing leachate from chamise fo-liage to test the effect of suspected allelochem-icals on seeds, Christensen used the same meth-od employed by McPherson and Muller (1969),but only utilized the natural, non-concentratedform rather than 4x–10x concentrated forms. Af-ter employing three different bioassay tech-niques, Christensen found four of eleven plantspecies tested showed depressed or zero germi-nation rates when exposed to natural leachate.Two of these were non-natives. To verify thatleachate was actually suppressing germinationrather than killing the seeds, the un-germinatedseeds were later planted on seedbeds with plainwater. They germinated as well as untreatedseeds.

Interestingly, of the six native fire-followersexposed to chamise leachate, none showed sig-nificant differences in germination rates from thecontrol. More revealing, however, was how theseeds were prompted to germinate in the firstplace. Each had to be carefully pre-treated withscarification, the seed coats being ruptured bylaborious scratching with a sharp scalpel (Table2).

The requirement of pre-treatment demonstrat-ed the presence of innate dormancy in the seeds,


Table 2. Seed Response to Chamise Leachate. The effect of natural chamise leachate on the germination ofseeds of eleven selected species present after a burn. Bromus diandrus was included in experiment to comparewith previous work. Adapted from Christensen and Muller (1975b).

Response to leachate Affected species

Germination inhibited Lactuca serriola (prickly lettuce): non-nativeCentaurea melitensis (tocalote star thistle): non-nativeCyrptantha intermediaErigeron divergens (fleabane daisy)

No significant affect on germination (notfound after burn)

Bromus diandrus (rip-gut grass): non-native

No significant affect on germination andrequiring minor scarification

Lotus scoparius (deerweed)Calystegia macrostegia spp. cyclostegia* (morning glory)

No significant affect on germination andrequiring major scarification

Allopyllum glutinosum (phlox)Emmenanthe penduliflora (whispering bells)Eurcypta chrysanthemifoliaPhacelia grandiflora

dormancy present before coming in contact withany suspected allelopathic inhibitors in the soil.This revealed another critical flaw in the entire‘‘chamise-fire cycle’’ model. If seeds of chap-arral species were already deeply dormant at thetime of dispersal, there was no reason to hy-pothesize the presence of other inhibitors in theenvironment capable of inducing seed dorman-cy. Although Christensen showed shrub-derivedtoxins depressed germination and growth insome plant species, he was careful to describethe results in such a way as not to imply alle-lopathy was the most significant factor in deter-mining natural vegetation patterns.

‘‘It’s one thing to show inhibiting chemicalsare there in the plant,’’ Christensen said later,‘‘it’s quite another to show they have an impactin the field (pers. com May 03).’’

Innate Dormancy Confirmed. By 1976Muller retired and became Emeritus Professor atUCSB. Although he was no longer engaged inactive research, he continued to maintain a pres-ence in the field of plant ecology. Despite theongoing controversy concerning the validity ofthe ‘‘bare zone’’ and ‘‘chamise-fire cycle’’ mod-els, Muller had successfully presented both sothat they were becoming common topics in ecol-ogy textbooks and college biology courses.

‘‘Allelopathy was a concept I felt needed tobe covered in the classes I taught,’’ Jon E. Kee-ley remembered (pers. com. Dec 03). ‘‘Themodels developed for coastal sage scrub andchaparral plant communities were excellent onesto use because I wanted to show my students asmany local examples as I could.’’

Keeley, a professor at the time at OccidentalCollege in Los Angeles, encouraged his studentsto analyze experimental design and actively

challenge assumptions. In doing so, however,they often expressed confusion over some ofMuller’s methodology. ‘‘My student’s kept ask-ing questions like, ‘why did they keep usingnon-native weeds in their tests?’ or ‘why didthey flash evaporate and concentrate suspectedallelochemicals before testing them?’ I couldn’tanswer their questions. It was clear that if wewanted answers, we needed to carry out somegermination studies ourselves and examine theseed dormancy issue under more natural condi-tions.’’

The first results of their investigations werepublished in the Journal of Ecology in 1985.They wrote, ‘‘Part of the confusion surroundingchaparral herb germination behavior is the as-sumption that one mechanism works for all spe-cies as suggested by certain investigators work-ing on single non-native species’’ (Keeley et al.1985). Instead, Keeley and his students feltchaparral plant species with ‘‘a diversity of lifehistories and of seed germination behaviors’’were best examined on a separate basis.

For their study, thirty different native species’seeds were collected in late spring. These in-cluded a wide range of typical fire-followers in-cluding 22 annuals, 6 herbaceous perennials, and2 subshrubs (woody species that die back to nearground level every year). The seeds were heateddry at various temperatures (80, 120, and 1508C) and planted in potting soil. Each species wasthen subjected to three different treatments:aqueous leachate from chamise foliage, pow-dered charred chamise wood, and leachate andcharred wood. Natural level and 4x concentratedleachates were used, both being collected in thesame manner Muller employed, from livingchamise foliage during middle to late summer.In contrast to previous studies, each species was


Table 3. Comparative Results. Species concluded as not being stimulated by heat to germinate (0) by Mc-Pherson and Muller (1969) and compared to later experimental results by others. Cue responsible for stimulatinggermination listed. (—) indicates not tested.

Species tested

McPhersonand Muller

(1969)Christensen

(1975b) Others

Lotus scoparius (deerweed)Helianthemum scopariumVulpia octoflora* (vulpia grass)Calandrinia ciliata (red maids)Phacelia grandiflora

00000

heat———

scarification

heat (5)heat (2)

——

smoke (1)Lotus strigosusSilene multinervia (catch-fly)Oenothera micrantha (camissonia)Adenostoma fasciculatum (chamise)

0000

———

heat

heat (3)smoke (1)

—charred wood (5)

Calystegia macrostegia ssp. cyclostegia* (morning glory)Emmenanthe penduliflora (whispering bells)

——

heatscarification

heat (4)smoke (1)

* Species name has been changed to reflect recent taxonomy in Jepson (1993). Source of information: (1)Keeley and Fotheringham, 1998; (2) Keeley et al., 1985; (3) Westermeier, 1978; (4) Parker, 1987; (5) Keeley,1991.

subjected to multiple tests. ‘‘All treatments werecarried out in combination for a total, includingcontrols, of sixteen treatments per species. Eachwas replicated eight times.’’

In experiments on twenty-two native annuals,only two, Apiastrum angustifolium (wild celery)and Cryptantha muricata (popcorn flower) wereinhibited by chamise leachate. And these resultscould only be obtained by using a concentrated4x solution.

‘‘Even more difficult to reconcile with the the-ory of allelopathy,’’ Keeley wrote, ‘‘is the ob-servation that nine species in this study showedan enhanced germination rate in response to Ad-enostoma leachate.’’

In comparing the species tested by Keeleywith McPherson and Muller (1969) and Chris-tensen and Muller (1975b), it becomes clear thatthe importance of fire cues in germination wasunderestimated in the earlier work. Further in-vestigations have now documented that mostfire-following species produce innately dormantseeds and that some aspect of fire, not allelop-athy, provides the primary cue for their germi-nation (Table 3).

‘‘The best way to do these experiments,’’ JonKeeley explained (pers. com. July 03), ‘‘is toinclude a response curve that covers a widerange of temperatures and durations. For exam-ple, if you hit the right combination with Lotusstrigosus and Helianthemum scoparium, you canget extremely high germination rates, even100%. Also, heat and chemicals can have bothstimulatory and lethal effects dependent on theirlevels. Consequently, failure to find a positive

response can not be interpreted as conclusive be-cause the treatment levels could have been eitherlethal or insufficient to stimulate.’’

After the publication of his 1985 paper, Kee-ley went to UCSB and talked with Muller. ‘‘Hesuggested I may not have examined the rightthings, but that was about it,’’ Keeley remem-bered. ‘‘We really didn’t have any substantivediscussions on the matter.’’

Is it Still a Possibility? For chaparral, it isclear innate dormancy in seeds can account forthe lack of herbs under the community’s canopy.The remarkable post-fire germination cycle canbe explained without invoking environmentallyinduced chemical inhibition. Poor growing con-ditions under mature shrubs selected for traitspostponing germination until those conditionsimproved, such as after a fire, including higheravailable nutrients levels, more space and light,and lower herbivory.

The possibility of environmentally induceddormancy still remains, however. Two fire fol-lowing herbs, Papaver californicum (fire poppy)and Nicotiana attenuata (coyote tobacco), areabsent under the chaparral canopy, yet germinatefreely under lab conditions (Jon E. Keeley pers.com. Dec. 03). ‘‘Rather than these two speciesbeing suppressed by shrubs to reduce competi-tion as described in the ‘chamise-fire cycle’model, I think it may be the other way around,’’Keeley suggested. ‘‘Sensitivity to shrub chemi-cals by some annuals may have been selectedfor by the evolutionary process as a way to timegermination during more desirable post fire con-


ditions. So perhaps in these two cases, allelo-chemicals may be causing an induced dormancy.But without further investigation, we just don’tknow.’’

While factors other than chemical inhibitioncan account for bare zones around Salvia leu-cophylla and Artemisia californica, the possibil-ity of some allelopathic influence remains open.Do volatile compounds in coastal sage scrubever play a significant enough role to make adifference in naturally occurring vegetation pat-terns? ‘‘As far as I know, the question of whygrasses grow within bare zones during wetyears, despite animal activity, has never been ad-equately addressed,’’ Bob Muller said when re-flecting upon his father’s work (pers. com. July03). ‘‘Why don’t animals always eliminate seed-lings, regardless of the level of moisture?’’

The hypothesis favored by Muller to explainthis observation and supported by Halligan’sdata on Artemesia suggests that heavy rainsleach toxins from the soil, removing inhibitorychemicals and thus permitting seedling success.Muller also felt this accounted for the lack ofbare zones on the Santa Barbara Channel Is-lands. The islands’ sandy soils were more sus-ceptible to leaching than the clay soils in theSanta Ynez Valley where bare zones were plen-tiful (V. Thomas Parker pers. com. April 03).Before the hypothesis can be accepted with aconvincing level of confidence, however, repli-cation of Halligan’s data over longer time framesand measurements collected under a wider va-riety of conditions are needed. Unfortunately,there is little interest in pursuing the mattermuch further. Plant ecologists generally view theentire concept of allelopathy with understand-able skepticism because hundreds of investiga-tions have produced little more than ambiguity.As demonstrated in Muller’s work, ecologicalvariables are notoriously difficult to isolate. Incommenting on the need for researchers to rec-ognize this difficulty, John Harper (1975), theprominent plant population biologist from Eng-land, wrote, ‘‘It would be surprising if, amongthe variety of plant interactions in nature, therewere not cases in which toxins played an im-portant ecological role, but it does not help thediscovery of such cases to preach their existenceas though it were gospel.’’

Consequently, due to past errors, a climate ofapprehension has formed a dark cloud over thefield, requiring more stringent levels of proofthan demanded within other areas of ecology(Williamson 1990). ‘‘To my knowledge,’’ wrote

J. H. Connell (1990), ‘‘no published field studyhas demonstrated direct interference by allelop-athy in soil. . . while excluding the possibility ofother indirect interactions with resources, naturalenemies, or other competitors.’’

‘‘The critical issue,’’ Harper (1975) identified,‘‘is to determine whether such toxicity plays arole in the interactions between plants in thefield. Demonstrating this has proved extraordi-narily difficult—it is logically impossible toprove that it doesn’t happen and perhaps nearlyimpossible to prove absolutely that it does.’’

When concentrated, as was done in many ofthe sage scrub and chaparral studies, many bi-ological compounds can inflict damage to livingsystems, including the inhibition of seed ger-mination or growth. Reflecting on this questionwhile studying allelopathy in Illinois, LawrenceStowe (1979) suggested, ‘‘that virtually any spe-cies can be shown to have allelopathic propertiesby testing it in bioassays, and that positive re-sults in bioassays may have nothing to do withthe interactions among plants in the field.’’Stowe also found an unfortunate tendency forsome investigators to ignore the lack of corre-lation between their laboratory bioassay resultsand what they found in nature. Interestingly,Muller pointed out the correlation issue in his1953 study of the two desert shrubs, Encelia far-inosa and Ambrosia dumosa, demonstrating thatinhibition found in the lab did not always trans-late into inhibition in the field.

‘‘Literally hundreds of plant extracts havebeen tested for bioactivity and shown to be ac-tive,’’ Romeo and Weidenhamer (1998) wrote.Because of failure to properly test under naturalconditions, they noted, ‘‘there is both garbageand confusion in the literature. Many reportedeffects are not real, and probably many real oneshave been overlooked simply because the bio-assay used was faulty.’’

The primary cause for faulty conclusionsfrom experimental data rests with poor design ofcontrols allowing more than one variable to af-fect results. This was one of the issues cloudingMuller, Hunawalt, and McPherson’s (1968) con-clusion that seeds were released from inhibitionwhen fire detoxified allelopathic chemicals inthe soil rather than heat itself being the directcausative agent. Investigating resource compe-tition, a hypothesis uncritically accepted bymany ecologists, suffers similar problems.

The question of what happens to suspectedallelochemicals once they enter the soil also re-mains an incredibly complex matter. Soil parti-


cles, moisture content and the multitude of mi-croorganisms soil harbors have dramatic effectson organic chemicals, the details of which arealso extremely difficult to quantify and accu-rately measure over time. Ray Kaminsky (1981),working in the same UCSB facilities Mullerused, concluded ‘‘the allelopathic potential ofAdenostoma fasciculatum may, to a large de-gree, be attributable not to the substances fromthe shrub itself, but to its association to phyto-toxin-producing soil microorganisms.’’ Howev-er, as a testament to the complexity of such stud-ies, Phil Pack, a student at Occidental Collegein Los Angeles working on a Master’s thesiscould not replicate Kaminsky’s data when test-ing native species by using longer time framesfor germination (J.E. Keeley, pers. com. July03).

Some interesting work has been done recentlyon the allelopathic potential of Centaurea ma-culosa (knapweed), an extremely invasive weedin the western United States. Harsh P. Bais andcolleagues (2003) discovered the plant exudes (-)-catechin, a phytotoxic chemical, from its roots.By adding the compound in natural concentra-tions to field soil in pots they found ‘‘the ger-mination and, to a lesser extent, the growth ofFestuca idahoensis and Koeleria micrantha, twonative North American grasses, were sharply re-duced.’’ Strengthening their argument was theobservation that the inhibitory effect was muchless on Eurasian grasses, suggesting an evolu-tionary response within knapweed’s originalcommunity. Although these results clearly showC. maculosa produces toxins capable of inhib-iting growth in other species, the same two ques-tions remain as they have with all previous al-lelopathic investigations: 1) do the plant’s chem-ical products actually have an inhibiting effectin the field, and 2) if they do, is the effect sig-nificant enough to play an important role in theplant’s success over other species?

Ironically, one of the most prescient reflec-tions concerning the problems facing the inves-tigation of allelopathy came from C.H. Mullerhimself when he rejected Gray and Bonner’sanalysis in 1953. It is worth repeating.

The natural habitat even in a relatively sim-ple community of the desert, is far too in-tricate a system of influences and factors,physical and biological, to hope that theremay be found a single factor controlling thecomplicated life of a perennial species. Anexplanation, when it is arrived at, will be

at least as intricate as the situation it seeksto describe.

Perspective. Muller was a talented botanistas well as an independent thinker who clearlyunderstood how science worked. He was wellversed in Chamberlin’s method of multipleworking hypotheses and keenly aware of the pit-falls of becoming overly attached to a theory.Throughout his career, he constantly impressedupon his students the value of designing appro-priate controls and maintaining objectivity.

‘‘The question of the day in Muller’s lab wasalways, ‘Give me ten other reasons for gettingthe data you’re collecting’’’, former graduatestudent Nancy Vivrette said (pers. com. July 03).‘‘Just obtaining a positive result wasn’tenough.’’

‘‘Muller was as fair a scientist and human be-ing as I’ve ever met,’’ Roger del Moral remem-bered (pers. com. June 03). ‘‘Every Tuesdaynight while I was at Santa Barbara, he wouldrun a lively ecology discussion group. Peoplefrom every biological discipline you can imag-ine would come and present their papers. Mullerreally enjoyed arguing. He would take one po-sition and argue for that, then take the exact op-posite perspective later on. The amazing thingwas, he’d win both sides!’’

Muller’s ‘‘bull sessions’’ were legendary. Heviewed science as a sort of intellectual coliseumwhere ideas could be attacked and defendedwith ferocious intensity. Once he decided a par-ticular position was wrongheaded, Muller wouldcharge into the fray with self-righteous deter-mination and slay its supporters with debatingskills few could match. He was equally forcefulin defense of his own positions. For him, therewere very few shades of gray.

‘‘He got so mad at me for suggesting moisturewas an important variable in bare zone forma-tion,’’ Haines remembered. ‘‘He thought I hadbeen brainwashed by the drought specialists atDuke University. I didn’t understand it, becausehe always stressed the value of maintaining mul-tiple working hypotheses. I’d only done whathe’d taught me to do.’’

Pat Halligan (pers. com. July 03) experienceda similar reaction when re-examining Haines’work in the early 1970‘s. ‘‘C.H. became reallyirritated because he felt I kept getting the wrongresults, so I started all over again from the bot-tom with a year of fieldwork behind me. Theatmosphere was almost unbearable. It was easier


to use Dale Smith’s lab on campus during theday, and Muller’s lab at night when no one elsewas around.’’

Muller’s last graduate student, V. ThomasParker (pers. com. Apr. 04), remembered, ‘‘Al-though Muller rejected my results the first fewtimes I presented them, it wasn’t because he wasmad, he just wanted my controls to be uniformand extensive. He always said ‘they had to bebeautiful.’’’

Parker was tasked with investigating possibleallelopathic inhibition by Quercus agrifolia(coast live oak) upon Avena fatua (wild oat), acommon grass in surrounding grasslands butrare under the canopy of isolated oaks. While hefound Quercus had no effect on Avena, his datadid suggest the grass was being inhibited by adifferent source, the dominant understory herbPholistoma auritum (fiesta flower) (Parker andMuller 1979, 1982).

The contradiction between Muller’s scientificphilosophy emphasizing open-mindedness andhis frequent dismissal of evidence contrary tothe allelopathic model seems inexplicable untilone appreciates the determination required tochampion an unpopular idea. Muller saw someof his detractors as the usual crowd of doubterswho were overly attached to outdated theories,unable to properly evaluate new ideas. In part,his reaction to them was shaped by the desire tocounter the remaining followers of Frederic Cle-ments (1905) who was a major influence in plantecology for over fifty years and who dismissedallelopathy as a viable theory (Robert Mullerpers. com. July 03).

In private moments, Muller would readilyagree allelopathy was just one of many variablesaffecting the ecology of plants. But in an effortto promote the idea in papers and during scien-tific conferences he gave the impression the pro-cess was a dominating ‘‘single factor.’’ In striv-ing to disprove every challenge, Muller did nottreat competing hypotheses with equal intensity.The observation confirmed by Christensen’s re-search that post-fire species are deeply dormantwithout chemical inhibition playing a role wasnever fully acknowledged. Despite evidence tothe contrary, Muller continued to support his‘‘secondarily induced dormancy’’ hypothesis inchaparral whereby seeds remain dormant due toexternal, environmental inhibitors.

Muller was, however, very successful in de-veloping an elegant series of experiments to testhis coastal sage scrub ‘‘bare zone’’ model byfocusing on the inhibition of seedling growth.

He uncovered and was able to describe a poten-tially important variable in the community struc-ture of coastal sage scrub vegetation. His errorwas utilizing the same techniques in chaparralas he did in bare zone studies, namely exposingseedlings to vegetation leachate. Demonstratingchamise or manzanita leachate was inhibitory orlethal to seedlings was not relevant to the‘‘chamise-fire cycle’’ model. Chaparral allelop-athy calls for inhibition of seed germination, notseedling growth after germination. If chemicalswere indeed toxic to seeds and seedlings, thechaparral seed bank would eventually becomedecimated, as seeds germinated each spring onlyto be killed by inhibiting chemicals. Few seeds,if any, would remain to account for the explo-sive post-fire germination response.

Judging Muller by his mistakes, however, oras an investigator blinded by passion to prove afavored theory belies the man’s intentions andhis success as a scientist. Emotional attachmentto a particular position is not necessarily con-trary to objectivity. The desire to discover some-thing new and the competitive drive it engen-ders, are critical components to the scientificprocess. Little advancement in knowledge wouldbe gained without them. Propelled by the emo-tional energy that moves knowledge forward,the scientist strives to maintain a delicate bal-ance between desire and truth, knowing full wellone is capable of influencing the other in uncon-scious, yet dramatic ways. It is a balance westruggle with in every aspect of our lives.

The Gnarly. As Muller’s days of active re-search came to a close and he assessed nearlytwenty years of data, he modified his perspectiveon allelopathy to account for the new data hisstudents collected. Although he continued tomaintain chemical inhibition was an importantecological process in southern California’sshrublands, he accepted some changes to hisoriginal hypotheses that he felt were warranted.His co-authorship with Norm Christensen in1975 reflects his willingness to accept conclu-sions contrary to his own. Muller was meticu-lous about where he allowed his name to appear.

‘‘My work did not take me where he hadhoped it would go,’’ Christensen said later (pers.com. Aug 03), ‘‘but in the end he was pleasedthat we had a pretty coherent story to tell. I thinkhe felt that allelopathy was still a factor, butcould see that the patterns we observed weremore complex and that animals were very im-portant.’’


Bruce Haines visited his old mentor in themid-1970‘s and was surprised to hear Muller de-scribe the impact of two wet years on the barezones they first studied together in the early1960‘s. ‘‘He told me they were completely filledin with grass,’’ Haines recalled. ‘‘I was surprisedby his comment because it was the same issue Iraised in my thesis that caused me so much trou-ble. He said that he now saw drought as playingan important role in how effective plant toxinscould be. We talked a bit more and then helooked me right in the eyes and said, ‘You wereright!’ I’ll never forget it.’’

A little later, Muller wrote a letter to Pat Hal-ligan (pers. com. July 03). It was Halligan’s re-search in 1976 that documented the effect of ex-cessive moisture on the inhibitory effectivenessof volatile compounds. ‘‘My project was toprove the allelopathic mechanisms of Artemisiabecause C.H. didn’t like the results Haines cameup with,’’ Halligan said. ‘‘But he didn’t agreewith mine either, so I had a difficult time there.But several years after I left Santa Barbara, C.H.wrote me a note saying he felt I had done a lotof good work and agreed with my conclusions.He acknowledged to me that allelopathy wasjust part of the mix and not the dominating fac-tor.’’

According to those who knew him best, C.H.Muller was an ‘‘old-school’’ Texan willing tofight an honorable battle for what he believed.His passion led his science and sometimes influ-enced his conclusions, but his love for botanyand the natural world led many to follow hisvision and become outstanding scientists them-selves.

‘‘He was certainly an inspiration for youngstudents because he made them feel part of the‘grand battles’ in which he always seemed to beengaged,’’ Harold Mooney (1999) one of Mull-er’s earliest students, wrote.

As a sophomore, Mooney listened to Mullerreject allelopathy as he discussed Gray and Bon-ner’s work on Encelia. Then, after a two-yearstint in the US Army, Mooney returned to findhis teacher ‘‘engaged in research that purportedto demonstrate that allelopathy did indeed exist’’in the foothills of Santa Barbara. ‘‘This was pret-ty exciting for a budding young ecologist, to seethe stuff of science so close up: the proposal andcounterproposal in trying to work out the com-plexities of the operation of natural systems.’’

‘‘It was such an interesting time,’’ NormChristensen said when reflecting upon his workwith Muller. ‘‘I look back on it all now and it

was by far the best research I’ve ever done. Itwas so much fun. Behind his back, we affec-tionately knew C.H. as ‘the gnarly’. We all lovedhis crustiness and knew well that he wouldmarch into the jaws of hell on our behalf. I amgrateful to have had the opportunity to workwith him. He is an exemplar of the fact thatscientists are also very human. That’s not a badthing.’’

By the mid-1970’s, Muller’s deteriorating vi-sion and brush with a near fatal illness madefieldwork impossible, but he continued writingresearch papers into the 1990’s. In 1975, he wasselected as the Ecological Society of America’sEminent Ecologist. The photo accompanying anarticle about the award shows the famous oaktaxonomist with a wry smile holding a sprig ofToxicodendron diversilobum (poison oak) (Fig.3). V. Thomas Parker remembered, ‘‘He wantedto see if anyone would notice.’’ In 1982, CurrentContents, a source for bibliographic research,declared Muller’s 1966 paper, ‘‘The Role ofChemical Inhibition in Vegetational Composi-tion’’, a Citation Classic having been referencedmore than 125 times.

As for others involved in the story, their pathsdiverged in a multitude of ways. Reed Gray,who co-authored the desert allelopathy paperwith James Bonner in 1948, entered the privatesector as a chemist after he was awarded a Ph.D.in biochemistry for his research on Encelia.

‘‘That paper helped me all through my life ingetting jobs and recognition,’’ Gray said in2003. ‘‘I remember the local Pasadena newspa-per even did an article on it. It was titled some-thing like ‘the biochemical warfare amongplants’.’’

The potential of using plant allelochemicals asherbicides prompted Gray to isolate and synthe-size a toxic compound from the genus Leptos-permum, commonly known as tea trees. He re-corded two patents for the compound whileworking for the Stauffer Chemical Company in1980. He is retired now, living with his familyin Northern California.

Phil Wells went on to do pioneering work onthe dramatic vegetation displacements of GreatBasin forests since the last glacial period by us-ing a unique source of information, fossilizedremains of plants preserved in Neotoma (woodrat) nests occupied over the past 12,000 years(Wells 1983). ‘‘The idea first came to me whenI spotted one of their nests at Indian Springs,near Las Vegas in the early 1960’s. The materialwood rats accumulate can be preserved for tens


FIG. 3. C.H. Muller, in the field, demonstrating his well-know sense of humor. Being a recognized experton the genus Quercus, Muller is holding a sprig of poison oak. Photo accompanied the announcement of hisaward as Eminent Ecologist in 1975 in the Bulletin of the Ecological Society 56 (4): 23, 1975.


of thousands of years and contain samplings ofall the plant communities existing aroundthem,’’ (Wells pers. com. June 03). Well’s tech-niques are now the standard for studying Holo-cene and late Pleistocene paleoecology in aridparts of the world.

Wells became Professor Emeritus at Univer-sity of Kansas. He died October 29, 2004.

Helped by Muller’s training, Bruce Haines de-signed a successful dissertation research projectat Duke University involving work at the Smith-sonian Tropical Research Institute in Panama. Itwas there he developed a life-long interest in thebiological and biophysical processes controllingthe abundance of leaf-cutting ants. He remainsa professor of botany at the University of Geor-gia.

Hal Mooney became a professor of biologicalsciences at Stanford University and has built asignificant portfolio of excellent scientific workin plant ecology, chaparral plant physiology,convergent evolution and global climate change.He was also Bruce Bartholomew’s doctorate ad-visor. Mooney continues to teach and researchat Stanford and is a member of the NationalAcademy of Science.

James McPherson became professor of botanyat Oklahoma State University and distinguishedhimself as an outstanding teacher. He workedtirelessly as a conservationist, managing the Na-ture Conservancy’s Springer Prairie Preserve,contributing his expertise to the development ofthe Tallgrass Prairie Preserve, and actively par-ticipated in the Sierra Club. He died unexpect-edly of a heart attack in 1994.

Bruce Bartholomew remained in northernCalifornia and was hired to care for the botanicalcollection at the University of California inBerkeley. He eventually left to become curatorof the herbarium at the California Academy inSan Francisco and has become a renowned eth-nobotanist.

Pat Halligan taught at the University of Ne-braska for a short time, but ultimately went backto school to become a dentist and opened a prac-tice in the state of Washington. ‘‘I was an abys-mally poor teacher,’’ Halligan remembered witha smile in his voice, ‘‘so it became clear to methat I needed to find another profession.’’ De-spite leaving academia, he has continued his in-terest in botany by becoming a respected experton rhododendrons.

Norm Christensen was hired by Duke Uni-versity and began working on the effects of firein southeastern coastal plain ecosystems and re-

sponses of southeastern forests to human distur-bance. His career has evolved considerably overthe past thirty years; first focusing on the basicscience of ecology then shifting towards appli-cations to ecosystem management, especially inregards to fire. He was selected to chair two con-gressional committees to study fire, one in 1986after public complaints about how prescriptionburning charred giant sequoias in California andin 1988 after the great Yellowstone blaze.

V. Thomas Parker completed his work atUCSB and is now professor of biology at SanFrancisco State University. He has done exten-sive work involving changes in plant popula-tions, dispersal, seed bank dynamics, seedlingestablishment, and mycorrhizal ecology. One ofhis specialties include the genus Arctostaphylos(manzanita), leading to his selection as one ofthe authors to the group’s new treatment in theupcoming second edition of California’s JepsonManual.

Jon Keeley left Occidental College and is cur-rently a research scientist with the U.S. Geolog-ical Survey, Western Ecological Research Cen-ter in Sequoia National Park as well as an ad-junct biology professor at the University of Cal-ifornia, Los Angeles. His work in botany andfire management has earned him the reputationas being both a rigorous scientist and one of theforemost fire ecologists in the world.

Neil Muller inspired 12 Ph.D and two mas-ter’s students from 1966 to 1977 and publishedover 100 research papers from the 1930’s intothe 1990’s. He died January 26, 1997. His asheswere scattered over a field of bull thistles in Tex-as.

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