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Biological Control in : An Overview J. C. Yan Lenteren Laboratory of EntomologlF, Wageningen Agricultural University, P.O.Box 8031, 6700 EH WageningenrThe Netherlands

Abstract Van Lenter€n. J.C. 1992. Biological in Greenhouses: An Overview. Arab. J. Pl. Prot., 10 (l): 43-35.

Biological pest control has been applied with commercial crops. In ornamentals a zero-tolerance for pestorganisms or success for circa20 years now in greenhouses. Although it is a their injury creates a great barrier for use of natural enemies. relativelv ne\r' pest control method in this cropping system, Biological pest control further made it possible that bumble the growers did readily accept and rely on it. During the past and bees were used as pollinators for some impor- 20 years 14 species of natural enemies have been introduced tant vegetable crops, particularly tomatoes. Biological pest against 18 pest species. Natural enemies in use are control is an economically profitable endeavour, especially parasites, predators and . Some 10 new for growers of crops. The rather fast evaluation species of natural enemies are in the process of being evalu- and introduction of a number of natural enemies in situations ated for future use. The greenhouse area on which biological where chemical control was either insufficient or impossible; control is applied has increased from 400 ha in 1970 to almost has learned crop protection specialists that biological control, 14,000 in 1991. Most biological control occurs in vegetable within IPM programmes, is a powerful option in pest control.

Introduction of resistance against of several key pests in green- houses. A close relationship among researchers, development The total world area covered by greenhouses is small and extension workers, and the growers has resulted in a rapid (approximately 1.50,000 ha), yet developments in biological transfer and use of information on biological and integrated and integrated pest management (IPM') in this cropping sys- control. To date, most of the successes in greenhouse inter- tem have been significant. Greenhouses offer an excellent gated control have first been accomplished inthe Netherlands opportunity to grow high quality, products in large quantities and the United Kingdom, simply because 20 years ago these on a small surface area. In the Netherlands only0.5 Vo of the two countries together had more than 50 Vo of the greenhouse area in use for is covered with greenhouses (9300 area. ha out of 2 million ha). On this small acreage L7 Vo of the total Presently, biological control of the two key pests in green- value of agricultural production is realized, i.e. 3.2 billion houses, (Trialeurodes vaporariorum,) and spider US $ in 1988 (12). Few specialists in biological control antici- () is applied in more than 20 countries out pated being able to employ natural enemies in greenhouses of in total 35 countries having a greenhouse industry. Recent because growing vegetables in this protected situation is surveys of work on biological control in greenhouses can be rather expensive and pest damage is not tolerated. For found in (7 and 16). Details of the developments in this field ornamentals the situation is even more serious, because pre- can best be traced in the Proceedings of the Working Group sence of extremely low numbers of pest organisms prevents on Integrated Control in Glasshouses of the International export, and therefore a zero-tolerance is literally in force. Organization for Biological Control of Noxious Animals and Successful greenhouse production requires well-trained, Plants (Bulletins of the IOBCAMPRS from 1970 to 1991) intelligent growers who cannot afford to risk any damage from for ideological reasons, e.g. that integrated control The Greenhouse Environment may cause fewer negative side effects than chemical control. If Differences between the greenhouse and field environment chemical control works better they will certainly use it. In may partly explain the success of biological pest control in tomatoes. for example, pest control represents less than 2 Vo greenhouses. Greenhouses are isolated units, particularly of the total overall cost of production, thus the cost of pest during the cold part of the season. At the start of a cropping chemical control is not a limiting factor. period, usually during the winter, the greenhouse can be

Yet despite the se rious constraint that chemical control is so ..cleansed, of pest organisms and subsequently kept pest free easy and inexpensive. the development and application of for quite a while. Later in the season, isolation prevents integrated control has been remarkablv fast. The main reason massive immigration of pest organisms. Furthermore, only a for developing biological control methods \r'as the occurrence limited number of pest species occurs in greenhouses, partly rIPM is definedas:A durablc, environmcntalll'and economirlly justifiable system in which damage caused by pests, diseases and is prevented through the use of natural factors shriri limit the population growth of these organisms, if needed supplemented with aPpropriate control measures. In thisarticlethe term pest often iDctud€s di-es6 and *'eeds.

43:10 Jre (1992) i,i.y'l .rLJl iUJ il+. because of isolation, partly due to the fact that not all pests Small scale application of biological control in greenhouses specific to a certain crop have been imported into countries started in 1968 with the use of the predatory mite P. persimilis. with greenhouses. This makes biological pest control easier formosa is used again since L970. Later , other natu- because the natural enemies of only a few pest species have to ral enemies were selected, tested and introduced in program- be introduced. Another point is that cultivars resistant to mes for commercial integrated pest control (table 1). The diseases ( and fungi) have been developed for the most column ..in use since, in table 1 refers to use on a commercial important vegetable crops, and as a result relatively few dis- scale in West Europe. At the moment various natural enemies eases occur in greenhouses (16). are being tested for use in the greenhouse (table 2). The number of companies that produce Culural measures and pest management programmes can natural enemies for use in greenhouses has increased be organized for each greenhouse unit. Interference with pest from 1 in 1968 to 30 presently. management in neighbouring greenhouses is very limited anci The proceedings of the latest IoBCnvpRS meeting on so all measures can be applied pergreenhouse. The frequentlv integrated pest control in greenhouses in 1990 (8) show that occurring problem of drift which negativelf influ- use of almost all natural enemies is increasing. The growth in ences natural enemies in field crops does not exist here. use of E . formosa and P. persimilis, and the fast increase in the employment On the other hand, pest conrtol in greenhouses in compli- of leafminer parasites, thuringiensis and Amblyseius spp. prove cated by the virtually year round culture of a crop and the that developments in greenhous: biological control have certainly continous heating. These conditions provide excellent oppor- not come to an end. Table 3 provides data on the developments in tunities for pest survival and development once it has invaded world use of biological pest control in greenhouses the greenhouse. Some field pests have adapted to the green- since L970. house climate by no longer reacting to diapause-inducing factors (6). But these complications do not create specitic Table 1. Commerciallv produced natural enemies for control problems for biological control. On the contran'. thev might of greenhouse pests (after van Lenteren & Woets 1988 and even make it more attractive because lou' numberes of natural Ravensberg 1991 ) enemies may survive and be present for most of the time, making reintroduction unnecessary. The greenhouse climate Natural enemy Target pest In use since is managed within certain ranges which makes prediction of pest population development of and natural enemy easier and P hy tos e iu lus pe rs imi lis Tetranychus urticae r 968 more reliable than for field situatron. Trialeurodes vaporario rum te70 (1e26) Histroy of Biological Control in Greenhouses Bembia tabaci 1988 Opius pallipes Biological control of pests in greenhouses started around Liriomyza bryoniae 1980- 1983 ' Amblyseius barkeri 1930. Speyer (24) developed a method for whitefly control tabaci lggl-lgg0' Frankliniella occidentalis I 9g6- I 990' with the parasite Encarsia formosa, which was successfuly applied in several European countries and elsewhere until Dacnusa sibirica Liriomyza bry,oniae l98l Liriomyza rrifolii l98 t 1945. After the Second World War use of E. was formosa Diglyphus isaea Liriomyza bryoniae 1984 discontinued because the newly introduced pro- I 984 vided convenient and efficient control on most greenhouse Liriomy za huidob rens is l 990 crops. A few years later, however, the first signs of resistance B acillus thuringiens is 1983 to pesticides were observed in spider (L urticae). Re- Heterorhabditis spp. O tiorrhy nchus s ulcatus 1984 search by Bravenboer(1) revealed that a predator of spider Steinernema spp. Sciaridae 1984 mites, Phytoseiulus persimilis, was able to efficiently reduce Amblyseius cucumeris Thrips tabaci 1985 the numbers of spider mites. It took several years before the Franklinie lla occide ntalis 1986 predatory mite was used on a large scale. An important stimu- carnea t987 lus for its use came, unexpectedly, from the pesticide indus- Ap hidoletes ap hidimy z a aphids 1989 try: a selective (Milcurb) became available and Aphidius matricariae My zus persicae 1990 integration of the predator and Milcurb for control of and mildew, respectively, became popular. Oirus spp. Franklinie lla occide ntalis t99t Successful application of the predatory mite increased the interest for whitefly parasites because, at the start of the * use terminated, other natural enemy available. seventies, enormous outbreaks of whitefly populations took place. The knowledge of the availability of an efficient para- site paved the way for the development of a control program- Biological Control Today me and, after some trials, mass-rearing and introduction Most of the natural enemies mentioned above are em- methods were developed for E. formosa. Since this revival, ployed in integrated pest management programmes, with dif- biological pest control in greenhouses has become firmly ference in use of insecticides and natural enemies per crop and established. per country. The activities of the IOBC|MPRS Working

42 - Lll s+ll iLt_r il,.., this sort have been obtained with partial resistance in tomato and respectiveh' Table 2. Natural enemies in testing phase (after van Lenteren cucumber against whitefly and spider mite (20). An unexpected development from plant breeding re- Woets 1988, and Ravensberg I99I) search was to change morphological features of the host plant in order to facilitate the searching for hosts by natural ene- Natural enemy Target pest mies. In cucumber, the number of hairs per unit of leaf area Pathogens, predators, parasites thrips spp. has been reduced through a breeding programme, leading to parasites Aphis gossypii improved parasitization of whitefly by E. formosa (15). pathogens,predators, parasites spp. Sill another opportunity to broaden the application of parasites leafminer spp. biological control lies in the use of -resistant natural Aschersonia aleyrodis & whitefly spp enemy strains. In greenhouse IPM an organophosphorus Verticillium lecanii compound resistant strain of P. persimilis is used. In addition, nuclear polyhhydr. Spodoptera exigua climate management to improve the performance of natural soil pests enemies and/or to decrease development of pests and diseases anosipliae Otiorrhynchus sulcatus may become a part of greenhouse IPM programmes. B acillus thuringie ru is var. is rae le ns is Sciaridae Until a few years ago IPM was mainly limited to control of insects. During thc . st decade several initiatives have led to Table 3. World use of biological control in greenhouses since research in non-chemical control of nematodes and fungi. t970. During the latest meeting of the Mediterranean branch of the IOBCflMPRS working group control in Protected Total area "Integrated Area under the Year Pest Natural enemy . , ,t ,. under control Crops" aspects of this work were reported, like: effect of control (na, (ha) on nematodes and fungi, the role suppressive t970 spider mite P.persimilis 295 soils ma)' play in reduction of fungi and the potential use of Whitefly E.formosa l ls 410( 1e70) antagonistic leaf fungi (9). 1980 spider mite P. persimilis 3340 One specific example of an IPM programme is given below. whitefly E. formosa I 180 Chemicals used in IPM programmes vary among countries, leafminers D. sibirica 40 depending on availability and registration. Therefore, names aphids A.aphidimyza 10 4s70(1980) of chemicals are not given; they can be found in the previously r990 spider mite P. persimilis 7000 mentioned IOBC proceedings. whitefly E. formoso 4200 thrips Amblyseius spp. 1200 IPM in Tomato leafminers D. iseae 1000 The success of biological control in tomato crops is related aphids A. aphidimyza 350 to the rather simple pest and disease spectrum of this crop. soil pests nemathodes 50 13,800( 1990) Soil sterilization by steaming shortly before planting is used to eliminate soilborne diseases such as tomato mosaic virus Group on the effects of pesticides on natural enemies, <

-*ll 4l - .2Lrlll iLi-r il+, greenhouses in temperature zones. Table 4 illustrates the mies have been found through trial-and-error. \Ianv res€ar- tomate IPM programme. chers have thought about ways of optimizing the preintroduc- tory studies so as to increase the predictabilitl' of success before introductions are made. We should keep rn mind- Table 4. Commercially applied IPM programme for tomato however, that the success ratio (1:100, i.e. 1 species oi-rt of it-r-r crop. introduced natural enemies is a good control agent ) and the economic evaluations are strongly in favour of biological con- Pest and diseases Control method trol when compared with chemical control (1:10.000;. Pre- sently, we use a set of selection criteria to evaluate natural Trial e uro de s v ap o ra io rum Encarsia formosa enemies ( I 1 These selection criteria are particularly help- Tetranychus urticae P hy toseiulus pe rsimilis ,16). and chemical control ful in making a first selection between potentially promising and apparently useless natural enemies. Liriomyza bryoniae Dacnusa sibirica and natural control Why is Development of Biological Control NeGes- Liriomyzo trifolii Diglyphus isaea sary? and natural control The reasoning behind searching for pest control methods Liriomy zq huidobrenis is Diglyphus isaea other than chemical control, consisted until recently mainly of aphids chemical control the risks of chemicals for the environment and human heath and natural control (e.g. Metcalf 1980). With increasing , in- Lacanobia olerocea B acillus thuringiens is crasing costs of pesticides and the present difficulties in de- Chry sode ixis chalcites B acillus thuring ie ns is veloping new effective pesticides (19,4), there are nowadays also strong signals from the field of agriculture itself that the fungi and viruses resistant and plant material time has come to change from opportunism in pest control - soil nematodes tolerant plant material whereby problems are awaited, solutions in the field trf che- mical control are hoped for and danger signals are neglected - IPM in Other Crops to biologically based pest control (11). For a number of other important greenhouse vegetables Factors Limiting Implementation of Biological (e.g. cucumber, eggplant,sweetpepper) reliable IPM prog- Control developed as well (16). There are. howev- rammes have been Most of factors limiting biological control in greenhouses problem inscets threatening continuation of tPM in er, some are general and relate to all types of biological control. I will The most important species are some crops. e.g. cucumber. try to make clear why biological control is applied on only gossypii occurs frequently in cucum- aphids and thrips . Aphis circa 14,000 of the 150,000 ha with greenhouses. ber and cannot be controlled with the selective pesticide Firstly, there ere situations where the application of biolo- pirimicarb. Biological control of thrips with Amblyseius spp. gical is unneccessarlr or impossibledue a variety of reasons. was almost completely discontinued after several years of to For example, some crops are grown during too short a period application, because of poor results, and new natrual enemies to make biological control an economic investment, e.g. let- are being evaluated presently. tuce needs only 6 weeks from planting to harvest. Further, invader to West Europe, the western ihrips, A recent when a zero-tolerance exists, like in ornamental crops which occidentalis, has led to a critical situation for Frankliniella are grown on about 50 % of the greenhouse area, biological growers: both chemical and biological control of cucumber control is difficult to apply, unless the production is not ex- are very unsatisfactorily. An intensive search for new this pest ported. In addition, climatological conditions may make enemies has been initiated, but it will take several natural biological control in some areas impossible, e.g. in the years before this results in a commercial control programme. Mediterranean area it is frequently too hot and dry for P. recent invader in Europe,but Seems Bemisiatabaci is another persimrlis to control spider mites,and frequently applied non- problems only and can be kept at low to be creating limited selective fungicides will harm the natural enemies. Finally. regular releases of E. (8). densities by formosa pests may occur which cannot (yet) be controlled by natural Although IPM programmes are available for a few flower enemies or selective insecticides, therefore requiring the ap- crops (chrysanthemum, gerbera). they are applied on a very plication of broad spectrum insecticides. If there is a large limited scale and usually for non-export because of probability that such a pest will occur, the control of which will extremely low tolerance levels for pest infestation. upset biological control,growers are not interested in applying biological control for other pests. In field crops this is the most Enemies Selecting Natural important limiting factor. For the main vegetable crops in The selection of natural enemies for biological control greenhouses it is less important. Considering these limitations programmes has been an empirical procedure until now, like it is estimated that presently about 30.000 ha of the total the selection of new chemical pesticides. Most natural ene- greenhouse area have potential for use of biological control.

ilr., With the development of new, more selective chemical con- mite and greenhouse whitefly, did not result in the occurr- trol methods, a much larger area will be available. ence of new pests. The new pests which have occurred since 1975 were Secondly, factorc may hamper use of natural enemies in unintentional imports (e .g. Spodoptera exigua, L. crops where biological control seems feasible.These factors trifolii, L. huidobrensis, F. occidentalis, B. tabaci). These newly imported are related to the quantity and quality of natural enemies at pests have created serious problems in glass- house arrival in the greenhouse, and the service that growers obtain both under biological and chemical control. They threatened from the producer of natural enemies andfor from advisorv the biological control of other pests because natu- ral enemies personnel. If a grower begins to use Biological control. the for them could not always be identified quickly enough. Chemical quality and intensity of the initial guidance determines the control of these pests was also very diffi- cult because pests success of the programme. For beginning producers of natural the were already resistant against most pesticides before they enemies the problems can be manyfold (14) and production of were imported in Europe. Several of these pests a qualitatively good is often underrated. are so hard to control chemically that biological control appears to be These drawbacks will not necessarily' alu'avs cause failure. but the only viable option! amateurism in production and guidance has had more than once a negative influence on application of biological control. Biological control is unreliable. The idea that biological Governmental insitutions demanding certain standards of control is less reliable than chemical control has emerged performance for insecticides should apply the same standards mainly as a result of a strong pressure to market natural for natural enemies. enemies which were not fully tested for efficacy. This critic- ism also arose because some amateuristic producers of natu- Thirdly, biological control may be impeded by a group of ral enemies did not check whether the agents they sold were verious facton One of these is new chemical compounds that effective for control of the target pest. In the Netherlands it appear on the pesticide market before possible negative has always been our philosophy only to market natural ene- effects on natural enemies have been evaluated. Such pesti- mies which have proven to be effective under practical condi- cides may totally disrupt a well balanced IPM programme. tions and within the total pest and disease programme. Natu- This situation is expected to change in Europe, where some ral enemies for which such efticiency studies were per- governments may soon require inclusion of data concerning formed , a.E. P. persimilis, E. formosa, and leafminer para- the effects on natural enemies as part of applications for sites, have shown to be as reliable or even better than che- registration of new pesticides Another important factor is the mical control agents. The present difficulties in controlling F. accidental importation of new pest organisms. Many of the occidentalis, have resulted in a too early large scale usage of greenhouse pests in countries with a temperate climate have predatory mites which have not been tested sufficiently been introduced through the importation of infested plant under practical condtions. As in chemical control, a period material. In the Netherlands, for example, more than thirty of ten years between the start of research and marketing of out of fourty species of greenhouse pests are introduced ones, an agent is often needed for correct evaluation of a natural seven of these are among the 10 most important pests (17). enemy. It is unrealistic to expect that researchers in biologic- Almost every year a new greenhouse pest invades Europe. al control can solve pest control much faster than those New imports require initially extensive chemical control prog- working with chemical control. Biocontrol workers often rammes until proper natural enemies have been found. have to deal with much more complex ecological variables The above factors do limit the implementation of biological than researchers in chemical control. Biological control control and IPM currently. But new developments may stimu- workers should be careful - even if the pressure is very late increase of the use of IPM. Soil solarization is one of the strong - not to release natural enemies too early due to the positive developments, the application of antagonistic fungi, resultant negative advertisement for our profession. or the exploitation of suppressive soils may further enhance IPM in greenhouses. Biological control research is expensive. All cost-benefit Incorrect Criticism Hampering Introduction of analyses show that biological control research is more cost Biological Control effictive than chemical control (cost-benefit ratio's of 30:1 for biological control and 5:1 for chemical control ,(3,25)). In the follou'ing section I will discuss a number of often The fact that despite this, biological control is not used on a heard. but incorrect statements about and unfair criticism of larger scale is mainly due to the relatively cumbersome pro- biologlcal control. duction and distribution of parasites and predators. The Biolryicd control creetes new pests. Use of biological whole methocology of natural enemy production is very control against one specific pest is said to lead to new pests different from that of pesticides. It is often thought that due to a termination of spralang nith broad spectrum pesti- tinding a natural enemy is more expensive and takes more cides. For the glasshouse sirnation this criticism is not cor- time than identifying a new chemical agent. The opposite is rect. Research on biologlcal control sas started to control usually true: costs for developing a natural enemy are on pests which were resistant to pestiodes. During the first average 2 milion US $ and those for developing a pesticide years (1965-1975) control of the key glr*st ous€ pests. spider on average 50 million US $ .

39 - Lll .,+Jl qLi_r il+, Application of commerical biological control is expensive directed at a change of the policy at high levels. A change in for the grower. An important incentive for the use of biolo- policy should not only be expressed on paper, but has to be gical control in glasshouses has been that the costs of natural materialized in research, education and extension. enemies have been lower than that of chemical pest control. Without long-term planning of reseerch end appliation, Ramakers (21) estimated costs (agent and labour) for che- biological control programmes are doomd to fail. mical and biological pest control in 1.980. At that time che- It is an essential prerequisite that all participants -including mical control of whitefly was twice as expensive as biological extension workers and - in an IPM project are re- control with the parasite E. Currently, chemical formosa. ceptive for new developments and are willing to implement control of. T. urticae is almost twice as expensive as biological them. A goal-oriented, long-term planning of crop protec- control with predatory mites (13). A comparison for costs of tion is necessary to base IPM development work on. With a biological control and chemical control of other pests in good planning, existing alternative methods can be used to given by (L2,13). Wardlow (26) states that biological control realize a gradual improvement of crop protection. The appli- of pests in tomato and cucumber is one fifth to one third that cability of new methods should be tested within the econo- of chemical control in the U.K. Ramakers (22) concludes mic constraints of the , to demonstrate and verify that that even the biological control programmes where quite a these methods will not impair financial returns and will prob- number of different natural enemies are used (e.g. cucum- ably be beneficial, in the long-terffi, to society as a whole. ber) , are not more expensive than chemical control program- mes. Ramakers gives the following figures for the costs of Introduction of biological confrol demands a good advis- biological control biological control in the Netherlands: 0.25 US fmzfyear for ory seryice. At the introduction of the first be paid to extension: tomato (4 natural enemies), 0.55 US fm2fyear for sweet agent in a crop, special attention should pepper (6 natural enemies) and 0.75 US fm2fyear for the growers have to rediscover the way biological control cucumber (9 natural enemies). The trade in beneficial works and learn to rely on it. For extension workers the amounts to 20 million US in the Netherlands in problem is that proper guidance of biological control de- t990. mands considerable entomological knowledge and under- standing. The phase of the initial implementation of biologic- Biological control is now so common in the main crops al control is often neglected. Experience in the Netherlands (tomato, cucumber and sweet pepper) that it is sometimes has shown that the amount of application of IPM is strongly hard to make an estimate for pure chemical control costs. related to the activity and attitude of extension personnel. If Pratical use of biological control develops vety slowly governmental extension services are weak, biological control This criticism has already been disputed above. The de- will have no chance, unless the producer of natural enemies velopments in use of natural enemies over the period 1970- has well trained extension personnel and is willing to invest 1988 are given in table 3. The total area now under biological in guidance. For glasshouse growers a period of one or two control amounts to L4,000 hectares, and represents circa years suffices to obtain additional knowledge of, and insight 45 Vo of. the present potential area for biological control. The in biological control. method is applied mainly in vegetables, although recently Acceptance of biological control as a serious control tech- many activities have been additionaly directed in developing nologr necessitates good public relations and education. biological control for ornamental crops. Table L and 3 show Although researchers often do not like to invest time in writ- that after the initial phase when only P. persimilis and E. ing articles that are not for scientific publications, it is essen- formosa were used, the natural enemy market has consider- tial to do so. Publications in the public press, radio and ably diversified. Today, biological control of whitefly and television programmes are usually more helpful in gaining spider mite is applied in more than 20 countries out of the acceptance for biological control than pure scientific articles. total 35 countries that have glasshouses. The teachnig of crop protection should drastically change at Vital Considerations Before Starting with Biolo- all levels (from vocational schools to university). Presently gical Control essentially purelv technical information is taught on how to Good research alone does not guarantee application spray and with what chemicals. This should partly be re- of non-chemical control methods. Based on my experience placed with information on other forms of pest control, espe- of the past 20 years, I have formulated some points to consid- cially biologrcal control. er before starting research in biological pest control; they In the Netherlands such changes have occurred already might help to prevent ivory tower work and frustration. and discussions with young growers have undergone a posi- Acceptance of biological confrol and integnted pest rfloo- tive change over the past decade: it is no longer a matter of agement as the official confrol sfrategt of the county should trying to convince them to use biological control, it is more a be the firlrit goal of biological contol workers. The most matter of being able to appropriately satisfy them with natu- important stimulus for an increase in use of biological control ral enemies for new pests. Integration of natural enemies and is the acceptance by governments of IPM as the main control (selective) chemical control is a normal procedure nowadays. strategy. If governmental bodies do not support implementa- The role of the consumer should be etrploited to the be, tion of IPM, activities of researchers should first and only be nefit of biological confroL The consumer is generally very

38 - +.;"JI .)Lr:ll qLir ilr., receptive to information on and use of pest control not in- fungi, or viruses. The chemical industries are in- volving chemical pesticides. He is even willing to pay more terested primarily in production of microbials and it is ex- for non-sprayed produce. Problems with residues on food, pected that all activities in this area will soon be exclusively accidents with pesticides at production sites and environmen- the domain of the pesticide industry. tal pollution have resulted in a strong awareness of side- The large natural enemy producers can now be considered effects involved in the use of chemical pesticides. Those as professionals, with research facilities, application of quali- working in the field of IPM should now positively interfere ty control, an international distribution network, P-R activi- with the present attitude of the consumer which is that any ties and an advisory service. They are well respected for their reduction in chemical treatments is considered an improve- work and their market will certainly increase with the in- ment. A serious problem is that the consumer has no direct creasing demand for unsprayed food and the growing pesti- influence on the production and sale of pesticide free crops. cide resistance problem. It is the middle man who determines crop quality. Their Quarantine and inspection services should be improved to standards are by no means influenced by the consumer, and prevent unintentional imports of pest insects. During the their selection criteria result in an overuse of pesticides. It past decade numerous pest insects have been imported into would be to the benefit of farmers and the general public if Europe (see elsewhere in this paper for examples). The ini- the last group could have more influence on pesticide-poor tial chemical control programmes developed to eradicate or-free production, e.g. by introducing a protected sales- these pests usually failed, but the spray frequencies advised mark for food produced under IPM. were so high that each time a new pest was imported, the Information on biological and integrated control should be biological control of other pests was put at risk. The creation provided in the same books and pamphlets of the state aduis- of a database with information on potential invaders and ory seruice which contain information on chemical control. methods to control these organisms might help to prevent The first Dutch guide for pest control (The Crop Protection panic reactions aimed at eradiction. Guide issuded by the Advisory Service and Plant Protection Adaptetion of export requirements to m*e biological Service (both from the Ministry of Agriculture) published in control po*sible. Current export requirements are often un- 1968 provided no information on biological control. In the realistic. They result in overuse of pesticides, with the addi- 1981 volume (eight's edition) the first information on biolo- tional risks of a fast development of resistance, high residue gical control was included, more than ten years after the use levels and health risks. More realistic requirements should of P. persimilis. The 1989 volume, consisting of 589 pages, be designed. The first priority should be to change the crite- has 7 pages with information on biological control, including rion that products should be without signs of damz5a, to that lists of which pesticides can safely be used in combination of products having no living pest insects. with specific natural enemies. (This is all in sharp contrast Specific Advantages of Biological Control in with the contents of the first book written by a'Dutch author- Ritzema Bos - on pest control , in 1891: of the 876 pages only 3 had inforamtion on After having heard all these obstactes for biological chemical control). control one might start to wonder why there are still growers using this method. Reliable production of good quality natural enemies There are, of course, the general advantages of biological shoultl be guaranteed. Ihe past 30 years have been characte- control such as reduced exposure of producer and applier to ized by the appearance and disappearance of natural enemy toxic pesticides, the lack of residues on the marketed product producers. Only a few producers active in the L970's are still and the extremely low risk of environmental pollution. in the market. The market has somewhat stablized and be- These are, however, not of particular concern for the grow- sides many small, rather amateuristic producers, less than 5 er. More impotant is that specific reasons exist that make large facilities are available providing qualitatively reliable growers working in greenhouses to prefer biological control: material. The number of beneficials produced at these large (a) with biological control there are no phytotoxic effects production sites is often more than 5-10 million per agent per on young plants, and premature abortion of flowers and week ( 16). The rise and fall of so many producers resulted in fruit does not occur. a negative marketability for biological control. (b) Release of natural enemies takes less time and is more The background of producers is rather diverse. Rearing of pleasant than applying chemicals in humid and wann natural enemies can be a full-time or part-time activity of greenhouses. glasshouse grolvers. The),' can be reared by companies re- (c) Release of natural enemies usually occurs shortly after lated to the glasshouse industn like seed companies and the planting period when the grower has plenty of time producers of fertilizers. In some cases production was started to check for successful development of natural enemies, by a research group with governmenral support and later thereafter the system is reliable for months with only continued as a private endeavour. The narural enem\- pro- occasional checks; chemical control requires continuous ducers mainly rear predators and parasites. onll' a fes' deal attentlon. with microbial agents like nematdes. entomoparhogenic (d) Chemical control of some of the key pests is difficult or

37 - Lll .lLJl qtir il+, impossible because of pesticide resistance. Biological control in greenhouses. Fewer new insecticides (e) With biological control there is rio safety period be- are becoming available because of skyrocketing costs for de- tween application and harvesting fruit; with chemical velopment and registration (18). The few new insecticides control one has to wait several days before harvesting is that are being developed are not likely to be targeted for allowed again. greenhouse use because the greenhouse area is small aird (0 Biological control is cheaper than chemical control. represents a poor opportunity for chemical companies to recover developmental costs. Biological Control in Greenhouses: A Success? Second, the sudden use of bumble bees and honey bees for Due to earlier mentioned resistance problems we were pollination on a large greenhouse acreage, strongly reduces forced to look for other pest control methods than chemical chemical control and intensifies demands for biological con- control. Intensive cooperation between researchers. exten- trol. Ramakers (22) illustrates that during the first period of sion workers, producers of natural enemies and growers has biological control in greenhouses the area under biological led to considerable success both in research and application control increased fast, and that presently, besides a further of biological control. This cooperative effort has led in the increase in area, the trade volume per surface unit is strongly past 20 years to introduction of 14 natural enemies against 18 increasing. Over the past 5 years an 8-fold increase in pests (table In solne countries integrated pest manage- l). turnover/ha was measured in the Netherlands. ment is practiced on a large part of the main vegetables crops in greenhouses (.rp to 90 Vo of the total area for certain Third, pests continue to develop resistance to insecticides, crops, (16). In the Netherlands, for example. gro'*'ers have a particularly prevalent problem in greenhouses where inten- learned to rely on biological control and no\+' ask for neu' sive management and repeated insecticide applications exert natural enemies before we can provide them with the neces- strong selective pressure on insects (10,2). Therefore we ex- sary information. This enthusiasm might, however, create a pect a greater demand for non-conventional pest control new problem: a too early release of a natural enemy can methods. result in a bad control effect and thus in negative advertise- ment for biological control! To date, we can safely conclude We should not see biological control as a control method that biological control in greenhouses has been very success- that will completely replace chemical control. It is a powerful tuI. option and can be applied on a much larger area than is presently done. It should be used in combination with other A number of conditions have to be met before the technic- pest control methods, among which chemical control, in IPM al implernentation of biological control will become a suc- programmes. In this way mutual benefit will be harvested. cess, however. Biological control agents should be as cheap, For chemical control it may result in extended use of pro- as easily available, as reliable, as constant in quality, and as ducts because of slower development of resistance and a well guided as chemical control. They should fit well in the more positive perception of the role of the pesticide industry total crop protection prclgramme and not be seen as an en- by laymen. In order to serve agriculture as well as the en- deavour separate from other crop protection measures. vironment and human health, we should harvest the best Conclusions: The Future of Biologrcal Control in from both methods to develop effective IPM methods. De- Greenhouses signing such environmentally safer IPM programmes is a Several current trends will stimulate the application of challenge for our profession.

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