tdr/bcv-sch/sih/84. 3 :/ english only -...

WORLD HEALTH ORGANIZATION ' TDR/BCV-SCH/SIH/84 . 3 :/ ENGLISH ONLY .,

UNDP/WORLO BANK/WHO SPECIAL PROGRAMME FOR RESEARCH AND TRAINING IN TROPICAL DISEASES

Geneva , 25-27 January 1984 r' ( l{

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REPORT OF AN INFORMAL CONSULTATION ON RESEARCH ON THE BIOLOGICAL--CONTROL OF SNAIL INTERMEDIATE HOSTS

CONTENTS

SUMMARY

INTRODUCTION AND OBJECTIVES

BACKGROUND •

2.1 Current Schistosomiasis Contr ol Strategy 2.2 Present Role of Snail Host Contr ol 2.3 Present Status of Research and Use of

Snail Host Antagonists • • . •

THEORETICAL BASIS FOR BIOLOGICAL CONTROL STRATEGIES

3.1 Major Attributes Affecting Choice of Biocontrol Agent

SAFETY FACTORS • •

Table I Possible Safety Factors for Consideration Before Introduction of Exotic Biological Control Agents

Table II Schematic Repr esentation of Development Testing of a Biological Control Agent

AVAILABLE ANTAGONISTS: CURRENT KNOWLEDGE AND FUTURE PROSPECTS

5.1 Microbial Pathogens 5. 2 Parasites . . . . 5.3 Predator s 5. 4 Competitors . . . . COSTS . . . . TRAINING, RESEARCH COORDINATION AND INFORMATION TRANSFER

7.1 Training • ....• 7. 2 Research Coordination 7.3 Information Transfer

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This report contains the collective views of an International group of experts convened by the UNOP/WOR LD BANK/ WHO SPECIAL PROGRAMME FOR RESEARCH AND TRAINING IN TROPICA l DISEASES (TO RI. It does not ntcessarily reflett the views of TOR/WHO. In the interests of rapid communication it has been submitted to only minimal editorial revision. Moreover, any geo· graphical designatiorts used in the report do not Imply the expression of any opinion whatsoever on the part of TOR or WHO concerning the legal status of any country . territory, city or area or ol its authorities concern ing the delimitation of its frontier$ or boundaries.

Ce rapport exprime les vues collectives d'un groupe international d'experts riuni par le PROGRAMME SPECIAl PNUO/ BANQU E MONOIALE/OMS DE RECHERCHE ET DE FORMATION CONCERNANT lES MAlADIES TROPICAlES (TO R). II ne repr6sente pas necessairement les vues du TOR/OMS et, en vue d'une diffusion aCCiil6r6e, it n'a pas et' !'objet d'une mise en forme particulierement soignie. En outre, las noms g4ographiques utili~s dans le pr~sent rapport n'impliquent, de Ia part du TOR ou de !'OMS, aucune prise de position quant au statut juridique de tel ou tel pays, territoire, ville ou zone, ou de ses autorit~s. ni quant au trad de ses fronti~res.

TDR/BCV-SCH/SIH/84.3 page 2

8. GENERAL RESEARCH PRIORITIES AND RECOMMENDATIONS FOR FOLLOW-UP ACTION

9. ACKNOWLEDGEMENT

10. LIST OF PARTICIPANTS

ANNEX I

ANNEX II

RECOMMENDED SAFETY PRECAUTIONS TO BE TAKEN WHEN TESTING A BIOLOGICAL AGENT IN AN END&~IC AREA BEFORE ITS RELEASE IS APPROVED

GUIDELINES FOR RESEARCH TO DETERMINE THE USE OF EXOTIC BIOCONTROL AGENTS OF SNAIL HOSTS . .

ANNEX III TRAINING OF PERSONNEL IN BIOLOGICAL CONTROL OF SNAIL INTERMEDIATE HOSTS . . . . • . • .

ANNEX IV

SUMMARY

SOME USEFUL REFERENCES ON BIOLOGICAL CONTROL WITH PARTICULAR RELEVANCE TO SNAIL INTERMEDIATE HOSTS

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The biological control of snail hosts remains a relatively unexplored research area. In view of the need for effective snail control methods, rigorous laboratory and field research and training, often lacking in the past, are now required. The present Informal Consultation reviewed the present status of laboratory research and field experience in this area. A theoretical background for biological control based on current knowledge of available snail host antagonists (microbial pathogens, parasites, predators and competitors) was discussed.

Among major constraints on the use of biocontrol agents in endemic areas has been the lack of a balanced appraisal of safety factors and costs. Guidelines were developed for research to determine the effectiveness, acceptability and operational use of exotic antagonists of snail hosts. This report lists not only general research priorities and recommendations, but also specific research recommendations relevant to the four broad groups (microbial pathogens, parasites, predators and competitors) of snail host antagonists.

It is hoped that the report will stimulate and guide scientists in selecting, planning and evaluating their studies on biological control and assist them and the Special Programme for Research and Training in Tropical Diseases (TDR) in the development and assessment of research proposals on promising antagonists. To this end, readers are invited to provide constructive comment and criticism in order to ensure, as far as possible, that research on biological control of snail hosts will in future be pursued with greater relevance to the control of schistosomiasis and, sine qua ~· with markedly improved scientific merit.

1. INTRODUCTION AND OBJECTIVES

An Informal Consultation Research on the Biological Control of Snail Hosts was held in 2

of the


Groups (SWGs) on Biological Control of Vee tors (BCV) and on Schistosomiasis (SCH). The meeting, opened and closed by Dr A.O. Lucas, Director, TDR, was the first of its kind.

The objectives of the Consultation were:

to review the present status of research and field experience of biological control of snail intermediate hosts in general and, in particular, that by intermolluscan competition;

to develop a scheme for field testing control agents, including an account safety regulations and training needs;

snail competitors as bioof research requirements,

to assess critically the major factors, both theoretical and practical, which influence the cost-effective use of biological control in snail host control programmes;

to draw up realistic recommendations for follow-up action.

For the purposes of the present Consultation, a working definition of the term "biological control" was adopted to signify the use of living organisms as snail host antagonists, with the ultimate aim of significantly interrupting the cycle of intense human schistosome transmission.

Of the three conventional approaches chemical, environmental and biological -- to snail host control, the greatest emphasis has so far been given to the use of molluscicides and the least to biological control. In the foreseeable future, no major advances can be expected in the use of chemical and environmental procedures. While research on biological control has been neglected, recent appraisals indicate considerable promise for the costeffective use of biological control of snail hosts in certain kinds of transmission sites. Similarly, encouragement has been drawn from the fact that in the last few decades the biological control of agricultural pests has enjoyed significant successes. For these reasons the present preliminary meeting on biological control of snail intermediate hosts, held to appraise weaknesses, gaps and promises, especially in terms of research and training needs, can be considered timely.

2 . BACKGROUND

In the last five years the overall strategy of schistosomiasis control, including the role of snail host interventions, has undergone significant change. The main features of the new approach are briefly mentioned below as a background to current concepts on research and training on the biological control of snail intermediate hosts.

2.1 Current Schistosomiasis Control Strategy

Never before in the history of schistosomiasis have prospects for its control, in most endemic situations, been more promising. During recent years, schistosomiasis control operations have profited from a better understanding of the epidemiology of the disease, the development and field use of new antischistosomal drugs and simplified quantitative diagnostic techniques. These and other significant advances herald a new era for effective integrated schistosomiasis morbidity control within available resources at the national level.


However, the recent advent of effective, safe and relatively cheap schistosomicidal drugs has permitted a change in strategy, formerly spearheaded by snail host destruction, to the control of schistosomiasis morbidity primarily by the use of population-based chemotherapy, usually in association with snail host control, health education, improved sanitation, etc. The adoption of this strategy now allows for the definition of feasible and attainable objectives, i.e. the reduction of morbidity to a level at which the more serious pathological changes associated with advanced schistosomiasis are unlikely to occur (WHO, 1983a)*. Complete interruption of transmission, unattainable in most endemic countries, no longer needs to be seriously considered in morbidity control programmes.

2.2 Present Role of Snail Host Control

Until about 1970, snail host control (mainly by mollusciciding) was the primary procedure for schistosomiasis control. In consequence, it was, not surprisingly, given major support at both research and operational levels (Ansari, 1973).

The present emphasis on chemotherapy, however, must not be misinterpreted to mean that there is now no place for snail host control in the new strategy. At the present time, snail host control in most areas where schistosomiasis is highly endemic can best be viewed as an important supportive element (in contrast to its former pre-eminent role) in integrated schistosomiasis control activities. It is evident, for example, that where reservoir hosts or marked migration of people are important, population-based chemotherapy alone is unlikely to be satisfactory.

There is now a greater appreciation than ever before that snail host control activities usually form part of a broad range of transmission site control operations. Identification of the most important potential transmission sites and of the main seasons of transmission is a crucial initial task. Next, if snail control activities are to be initiated, careful consideration must be given to the basic options of desirability/feasibility. Should snail control (whether environmental, chemical and/or biological) not be excluded by these options, then plans for its implementation must incorporate satisfactory solutions to the problems of where, when, how and by whom it is implemented. In addition, the aims, costs and evaluation of results must be included in the provisional plans of action and later in the national schistosomiasis control manuals which are now being prepared for planning and training purposes in an increasing number of endemic countries.

As part of the current strategies for schistosomiasis control, potential snail host control operations must be intimately associated with public health considerations (e.g. priority rating, based on quantitative criteria, for undertaking control operations) and subsequently with the implementation of population-based chemotherapy schedules. In general, snail control operations are unwarranted in areas where there is no evidence that schistosome infection is giving rise to detectable morbidity. On the other hand, in areas of intense transmission, where chemotherapy is being applied it is usually desirable that snail control activities be closely coordinated with the treatment regimen. In particular, snail host control activities, like other elements of control operations, must make a discernible contribution to the r~auction of schistosomal transmission to levels which no longer give rise to significant disease in the affected populations; they must also be shown to be cost-effective and without adverse environmental impact.

IV references in this


Significantly, within each of the three areas (environmental, chemical and biological) of snail host control, no radically new, promising approach has been devised in recent years and, in fact, none can readily be anticipated, with the possible exception of biological control. In addition, among major constraints on snail host control are high costs, relatively poor performance and lack of specificity of available methods. Research to identify effective biological control agents in certain transmission sites will be required to aid the overall efficacy of the new strategy.

2.3 Present Status of Research and Use of Snail Host Antagonists

In spite of much interest in biological control, based partly on the successes of this approach in eliminating many agricultural pests (Greathead & Waage, 1983) and also, for example, on the possibility of considerable financial savings, its potential role in the control of snail hosts has seldom been either rigorously or vigorously investigated. This omission, certainly as far as research on the subject is concerned, should now be rectified, especially as the WHO Expert Committee on the Epidemiology and Control of Schistosomiasis (1980) "fully commended support for carefully designed research programmes, especially those concerned with field testing and impact on nontarget species, as well as the search for effective pathogens." This Committee also pointed out that of "all biological control mechanisms intermolluscan competition ... is perhaps the most attractive at present." Bearing in mind these recommendations, the Organization has, therefore, been supporting, within its limited regular budget and also through the resources of TDR, a few laboratory-based research projects aimed at clarifying certain key issues prior to undertaking small-scale field testing of biocontrol agents. Also to this end, it may be noted that the Sixth SWG on Biological Control of Vectors focused on the formulation of protocols for field testing of biological agents, including those of snail hosts (see Annex VII in WHO, 1982d,) as a prerequisite for determining their role in integrated vector control.

Some brief comments are given below on laboratory research and field experiences of biocontrol of snail hosts, especially by intermolluscan competition. It must first be stressed, however, that sound information on the ecology of snail intermediate host populations and the patterns of schistosome transmission will continue to be required as a baseline for research, in order to define the most cost-effective strategies for control that can be applied in diverse biotopes in differing climatic zones or geographical areas. Such strategies imply the need not only for immediate, but also long-term, sustained effects.

2.3.1 Laboratory observations

Laboratory studies on biological control agents have ranged from relatively casual observations that snail colonies can be adversely affected by certain biological agents (e.g. microbial pathogens, ostracods, Helisoma, Bulinus tropic us, etc.), to rigorous investigations on the main biotic and abiotic factors governing the relationships between antagonists and their targets. It must be stressed, however, that even when excellent results are obtained in the laboratory, it is essential to perform carefully controlled field studies (see Annex II) to confirm the true value of any potential control agent. It has been a common finding that some agents which have performed well in laboratory aquaria may not maintain their promise when tested in field situations.

2.3.2


Marisa cornuarietis was first observed in Puerto Rico in 1952 (Oliver-Gonzalez and co-workers, 1956). The snail was introduced in 1956 into 30 lakes and reservoirs containing populations of Biomphalaria glabrata. M. cornuarietis was re-seeded several times and, after 20 years, only five of the original reservoirs contained planorbid snails (Jobin et al., 1977). However, cornuarietis was less successful in flowing water habitats in the Dominican Republic, Puerto Rico and St Kitts.

So far as is .known, under tropical African conditions, there has been only one field investigation of M. cornuarietis. Following its release into a man-made pond in the north-west of the United Republic of Tanzania, three species of indigenous snails (Biomphalaria pfeifferi, Bulinus tropicus and Lymnaea natalensis) were apparently eliminated (Nguma ~ al., 1982).

The thiariid snail Thiara (=Tarebia) granifera has also been reported to be an effective antagonist of Biomphalaria glabrata. It has been observed to replace a previously thriving population of B. glabrata in an extensive habitat on the island of Dominica (West Indies) and may have been responsible for severely restricting the range of the previously widespread !· straminea on the island of Grenada (Prentice, 1983). It has also been reported to be an antagonist of !· glabrata on the island of Puerto Rico (Ferguson, 1978) and, more recently, in a large area of the Dominican Republic. In contrast to these chance observations, T. gran if era was released in limited areas of the island of St Lucia in early 1978 (Prentice, 1983). In four separate field trials, B. glabrata was apparently eliminated from marshes and streams six to 22 months after the introduction of T. granifera. The time at which the target population reached zero was dependent on the number of .:!:_. granifera introduced. When seeded in numbers approximating those of the target snail, dominance was quickly established. Observations made in 1983 showed that .:!:_. granifera had retained its dominance; support for further follow-up studies is being sought.

With regard to Helisoma duryi, although some successes have been reported from lentic environments, this competitor is unlikely to prove useful in streams because it loses its foothold at velocities lower than those which can be withstood by Biomphalaria spp.

H. duryi was first tried in the field, with some success, in Puerto Rico in 195S and it was also successfully introduced into waterbodies at St Croix (Ferguson et al., 1958). In St Lucia, H. duryi was shown to compete successfully withB.glabrata in simulated field conditions, but when released into the environment it failed to become established (Christie et al., 1981). On the African continent, where it is now widely recorded, preliminary studies were carried out in small ponds in Egypt. At Moshi, United Republic of Tanzania, a field experiment in an irrigation system was started in 1973. The experiment failed because of flooding and H. duryi was found in all the furrows. However, after one year, H. duryi ~eded B. pfeifferi and constituted more than 95% of the snails collected. In 1975, H. duryi was seeded in the drains of the irrigation sys tern. A snail survey ~dertaken in 1981 showed that H. duryi was still present in a few drains in which no B. pfeifferi snails were found (Madsen, 1983).

In 1982-83, small-scale field trials were conducted in isolated areas of Saudi Arabia to test H. duryi against B. truncatus, B. arabica and B. beccarii. The preliminary res~lt~dicate that H. duryi supersedes B. beccarii (F. Frandsen, personal communication). -----

The brief account of snail host in ield situations suggests that some may play an role in the control


Medical surveys recently carried out in the island of Martinique have all shown that the transmission of intestinal schistosomiasis is largely or even totally interrupted. It has been impossible to find any child under 12 years of age positive for Schistosoma mansoni infection. This situation appears to be correlated with the replacement of B. glabrata by B. straminea, over a period of probably not more than 10-15 years. Whereas-before 1967 ~· alabrata was widespread, in 1983 it was restricted to only a few habitats; the converse is true of B. straminea, which has become widely distributed during the same period. Although other factors should probably be taken into consideration, for example, an improvement in hygiene, as in Puerto Rico, the replacement of !· glabrata by refractory !· straminea seems to be responsible for the almost complete disappearance of schistosomiasis transmission on the island (Guyard et al., 1983). The Martinican strain of B. straminea could not be infected~by Caribbean strains of S. mansoni, either by-exposure to miracidia or by microsurgical transplantation of sporocysts (A. Theron, personal communication).

In Guadeloupe, a similar situation of biological dominance has been observed. In the site of Grand Etang, fortuitous colonization by Ampullaria ( =Pomacea) glauca resulted in the decrease of !· glabrata densities, while S. mansoni prevalence in rats dropped from 80% to about 5% in five years (Pointier ~ al., 1983). However, in ponds in the low rainfall area of Guadeloupe, !· £labrata and A. glauca often coexist without any marked dominance by the prosobranch.

At the present time, studies on intermolluscan competition are being carried out, or are anticipated, in Brazil, Venezuela and certain Caribbean islands. The research programmes in the neotropics need to be reviewed, coordinated and perhaps expanded. In Africa, investigations on Marisa cornuarietis and H. duryi are being undertaken either together or separately, in Egypt, the Niger.~ Sudan and the United Republic of Tanzania. It is regrettable that, apart from the Niger, no serious research projects are at present being undertaken in West African countries where the risk of schistosomiasis becoming more widespread and intense cannot be refuted.

There is no doubt that snail host population densities in certain kinds of habitat can be drastically reduced, even eliminated, by intermolluscan competition. However, if snail competitors are to be truly successful, they must also contribute significantly to control of the parasite populations which cause disease at levels of socioeconomic significance. With this objective in mind and in relation to the new strategies for schistosomiasis control, which distinguish between schistosomal infection and disease, absolute prevention of transfer of the parasite from snail to definitive host may not be strictly necessary. Unfortunately, snail host population density thresholds, permitting diverse (low, moderate, intense) levels of schistosome transmission, are still unknown. They are likely to be variable, depending on the complex interactions of physical, chemical and biological parameters, but, despite their complexity, a good understanding of them would ensure a valid interpretation of the efficacy of biological or any other snail control procedures.

Apart from field studies on intermolluscan competition, investigations of other snail host antagonists under natural conditions have been relatively few; some are mentioned elsewhere in this report.

3. THEORETICAL BASIS FOR BIOLOGICAL CONTROL STRATEGIES

stages measures

al

of hosts must be


major density-dependent factors act. For most aquatic snails, the dominant density-dependent process is thought to be mortality (often as a result of predation) at the egg stage or of very young snails. A biocontrol agent will therefore have most effect if its major influence is on the late juvenile or adult snails.

3.1 Major Attributes Affecting Choice of Biocontrol Agent

The ideal biological agent would be able to persist stably in the habitat of the target snail and induce substantive long-term depression or eradication of the target snail population. A prime requirement is satisfactory persistence following introduction so that repeated introductions are not required. A competitive interaction has many advantages over predation and parasitism, competition being the only one capable, in theory, of complete displacement of the snail host by competitive exclusion. Predators and parasites require prey and hosts for stable persistence; they do not normally eliminate their food resources (prey) or habitats (hosts). This principle operates with respect to selection at the individual level (natural selection) and in terms of the population dynamics of the two-species association. A further advantage of competitors over pathogens and predators is the general tendency for competitive interactions, in the case of stable coexistence, to be non-oscillatory in nature. Recurrent epidemic behaviour and oscillations in predator and prey densities are familiar phenomena. On ecological grounds, with respect to the biological control of molluscan species, there is good reason to suggest that competition is more desirable than predation and parasitism.

Ideally, microbial pathogens to be used as biological control agents should:

be able to be cultured in sufficient quantities at reasonable cost;

be infective to the snail host by aquatic dispersal and contact;

be capable of rapid dissemination from snail to snail and of residual activity (long-lived infective stages);

cause rapid mortality and/or severely depress fecundity;

be safe for man and domestic animals and be specific for target organisms;

be capable of being stored under tropical conditions for at least a year, preferably longer;

have a stable genetic constitution with respect to shifts in pathogenicity.

In addition, it is desirable that pathogens should be recoverable from an infected specimen so that the cause of its mortality can be properly assessed. Finally, those agents that may require an extra-host stage should ideally not be adversely affected by environmental conditions.

Parasites used as snail control agents should ideally:

have a simple life-cycle capable of being maintained in the laboratory;

have a high reproductive rate with large numbers of long-lived infective stages

be to the snail host and the trematode·


have limited host spe cif i city f or snai l hosts, with broader specifici ty for definitive hosts;

not be infec tive to man and domestic animals .

The most effective predators would:

have a generation time similar to, or not much longer than, the target species;

have a mor e rapid reproductive rate than the target ;

pr ey on the target in preference to other potent ial species of prey;

sear ch actively and successfully f or individuals of species, aggrega ting in areas of high prey density behaviour ) .

the target (aggregative

Ide ally , a candidate for use as a predator should have all of the listed qualities. Unfortuna tely, none of the known pr edator s of schistosome-bea ring snails has more than one of them.

In the case of competitors , those species which compete wi th one another do so through t wo br oad mechanisms : (i) they have closely similar requirements and a better ability than the t a r get species to fill them , r esul ting in successful competit i on for resources; (ii) they cause di rec t damage to each ot her by a variety of measures, such as aggressive behaviour, predation on some life-history stages and production of chemicals that adverse ly affect each other . Such mechanisms are eKamples of interference compe tition , a common evolutionary r esult of in terspecies competition. Frequently, one competi t or has a greater effect on t he other than is possible with competition fo r resources. Such competitors of target snail species are t o be preferred to resource competi tors , but it is frequently difficult and time-consuming to elucida te t he me chanism. The most important property is to have a dep ressing effect on the target population , regardless of how many specimens are i nt roduc ed.

An effective competitor should not be sensitive to environmental fluctuations to which the t a rge t i s well adapted, since this would require repeated introductions after each environmental stress.

Finally, the competi tor that is successful against schistosome-bearing snails should not have inadvertent undesirable effec ts . For example, s i nce t he mos t l ikely competi tor s a re other molluscs, they should not contribute significantly to the t ransmission of other trematodes of socioeconomic significance to man or dome s tic animals . Wi t h the recent advent of safe , ef fective drugs f or the treatment of trema tode infections, this constraint is now less important.

4. SAFETY FACTORS

The risks involved in using biological control agents wil l depend largel y on the ir particular properties. The re are theoretical grounds for supposing that the most effective control agents f or snails will eventually prove t o be microbial pa thogens. At present, t hough, the most promising agents available are eKotic compet itor snails. Such snails should be released in a new country with caution. While t he risks involved can mostly be assessed in advance, some unforeseen consequences may ar ise .

Responsibility for the introduction of a part i cular exotic agent lies with the national regulatory agencies concerned. In order to assist in


decision making, a general safety check list is given in Table I. The first part of the table lists the main targets at risk together with the types of control agents most likely to threaten them. Part II gives the type of danger involved, again specifying the type of agents most likely to be involved. Not all countries will have the same targets or the same risks, although man, already exposed to schistosomiasis, will be universally present. Thus, agricultural crops (mainly rice) (I.d) can be excluded in areas where they are not grown. Equally, game animals (I.e) will be of little importance on a small Caribbean island but, as a tourist attraction and a source of foreign revenue, could be of considerable importance in parts of Africa.

The third part of the table suggests the types of information to be collected in relation to each of the targets listed in part I. The lists are not exhaustive, but form a starting point in gathering the required information. It may seem superfluous to include identification, but there has been some confusion in the literature. For example, the species of Pomacea used by Paulinyi and Paulini (1972) is subsequently named P. haustrum (Andrade, 1974; Hairston et al., 1975) and later referred to as P.- australis by Jordan et al. (1980); Tt is probably a different species from P. glauca, which occurs nat~ally on St Lucia.

Much of the information can be obtained by consulting such publications as Index Medicus, Tropical Diseases Bulletin and Helminthological Abstracts. Monographs, such as that on the helminths of certain African orders of mammals (Rounds, 1968), and textbooks, such as those by Malek (1980), Malek and Cheng (1974), Brown (1980) and others, provide much useful information, as do review articles (e.g. Ferguson, 1978; Frandsen & Madsen, 1979; Hairston ~ al., 1975; McCullough, 198la). The preparation of special data sheets for each potential control agent (e.g. WHO, 1981, 1982b) is especially useful. However, all sources should be examined at first hand and then reviewed critically. There are obvious disagreements between various sources; facts should be carefully separated from unsubstantiated opinions and assertions.

Despite this wealth of information, many questions will remain unanswered. Local sources, such as medical, veterinary, fisheries and wildlife records, may have to be consul ted. Where these fail to provide the required information, consideration will have to be given to field surveys, e.g. Mefit-Babtie (1981). Laboratory investigations may also be necessary to answer specific questions.

Ideally, laboratory investigations should be undertaken away from the area in question to avoid any chance of the accidental introduction of the exotic control agents. In practice, this may not be possible, in which case adequate safety precautions, as described below, will be necessary. It is a good general principle that exotic agents should not be imported until sufficient evidence is available that there will be no unacceptable hazard. It is debatable whether governments, to prevent premature introduction, could or should legislate specific regulations, such as those widely in use for controlling the movement of plants and domestic animals between or even within countries. The range of potential biological control agents is sufficiently broad to make the drafting of specific regulations extremely difficult. In the future it must be expected that an exotic agent will not be introduced until some responsible body, probably a national committee, including representatives of interested government departments (health, agriculture, fisheries, wildlife, water-resources, land-use and conservation, etc.) plus competent representatives of international agencies, authorizes such an introduction (McCullough, 198la) for limited testing in the laboratory and the field.

safety

TDR/BCV-SCH/SIH/84. 3 page 11

Table I Possible Safety Facton f or Consideration Before Introduction of Exotic Biological Contr ol Agents

I. Possible targets a t rislt (agents invol ved)

a) Man (pathogens, paras i tes ) b) Domestic animals (pathogens, parasites) c) Game and other wi l d animals (pathogens, parasites, predators) d) Agricultural crops ( competitors) e) Physical environment (competitors)

II. Informati on required to assess poten t ial dangers

1) ~

2)

3)

a) Pathogens i) Identify i i ) Consult records of related organisms (bacter ia,

vir uses, fung i, proto%oa, e tc .) to determine if any infec tions of I .a, b, c , d or e have been reported

iii) Handle with normal precautions for such agents iv) Conduct laboratory scree ning if there a re any adverse

re ports i n (il), using appropriate animals or planta

b) Parasites i) Identify

c) Predators

ii) List known hosts i n natural area of origin iii) List any r elated parasites i nfecting biota anywhere iv) Tes t susceptibility of this or related parasites v) If pa rasite does infect man elsewhere, assess risk of

this happening in target area

i ) 11 )

Hi) iv)

List known prey in country of origin List similar prey i n target country Evaluate effect i f predator attacks (ii) If ( iii) indicates potential seri ous r isk, conduct l aboratory tests t o obtain more information on likelihood of predator affecting organism at risk

d) C001pe t !tors 1) Identify and lis t known trematode or other parasites in country o! or igin

H)

111)

iv)

v)

vi)

vii)

Asricul t ure i)

ii)

i ii)

iv)

v)

Envi r onmen t i)

11)

List related speci es and their known trematode parasites List par asites t ransmit t ed by existing snai ls in target area, naturally and experimentally, judged by examination of snails Li st parasites of I.a, b and c known t o occur in target ares from medical , veterinary or wildlife recor da Assess risk of competitor s being l i kely to tra nsmit (i v) Conduct laboratory tests to investiga te (v) , if necessary Assess risk of introduction of e.xotic parasites with competitors

Investigate if competitors are crop pests in own coun try Li st related species known to act aa cr op pests elsewhere List important ' aquatic ' crops in target ar ea and note current traditional methods of husbandry Ascertain whether any l i kely agricul t ural development pr ogramme is imminent vhlch will int r oduce new crops or methods of husbandry Conduct laboratory and/or f ield tests of compet i tor agai nst relevant aquatic crops

Investigate poss ible hazards t o game or other wild ani11als Study other environmental eff ects , such as:

e limination of other lower animals , especially snails possible physical effects, such as eliminat ion of Aqua t ic vegetation result i ng in increased water flows, soil erosion , etc .


Table II. Schematic Representation of Development Testing of a Biological Control Agent

Stage of Testing

1. Primary activity screen

~ 2. Systematic lab-

oratory tests

3. Controlled or simulated field trials

4. Effectiveness in field against snails

5. Ability to control transmission of schistosomiasis

Specific Details

a) Laboratory tests to show killing of snails

+ a) Define precise activity

(numerical responses) b) Effect of relevant factors

(pH, temperature, sunlight, dissolved salts, etc.)

c) Safety for man d) Effect on other biota e) Mode of action (parasite,

pathogen, predator, competitor)

f) Pesticide testing (or other control methods)

l a) Performance against local

snails b) Effectiveness in local

conditions

Observations in: Endemic Area

Native Exotic a) a) 1

b)

c) d) e)

f)

l a)

b)

b)

c) d) e)

f)

a)

b)

c) Observations on other biota c) c) including crops. (N.B. Not necessary at this stage to know mode of action or for agent to be completely cleared for human safety)

~ a) Precontrol snail studies in a)

test and untreated areas b) Development of application b)

techniques c) Monitoring effect of target c)

snails d) Observations of effects on

other biota

! a) Pre- and post-treatment

human studies in test and untreated areas

b) Monitoring snail populations c) Observations of any

environmental effects

d)

a)

b) c)

1

l

a)

b)

c)

1 d)

I a) I , I

b)

' c)

2/

1 Sections enclosed in solid lines indicate where special precautions are needed to prevent premature escape of exotic control agents.

Sections enclosed has been released

broken lines agent control


agent will follow the same pattern as that required for any other control measure. The requirements have been discussed in detail elsewhere: e.g. Ansari (1973); Jordan (1977); Jordan et al. (1982); Duncan and Sturrock (in press); Sturrock and Duncan (in press):""" Table II outlines the stages to be followed in the logical development of a biological agent to control snails.

The most important risk with an exotic biological control agent, as compared to chemical control, is that if the antagonist escapes and becomes established, it may reproduce and remain in the environment indefinitely. If it becomes a serious threat, its removal may be as difficult as, or possibly more difficult than, that of the original target snail.

As indicated in Table II, Stage 1 may be and Stage 2 is confined to the laboratory, where suitable precautions can be taken to prevent the escape of the exotic agent (see Annex I). This is not an entirely hypothetical possibility, as is illustrated by the spontaneous spread of Thiara in the Caribbean, Helisoma in East Africa and of the exotic Biomphalaria spp. (!. glabrata) in an area of the Nile Delta, Egypt (Pfluger, 1982). Such a risk is best avoided by performing Stage 1 and 2 testing outside the endemic area as far as possible. In the long term, however, laboratory testing has, by definition, to be done in the endemic area under as realistic conditions as possible, and with a greatly increased chance of the agent escaping unless great care is taken. Specific measures will depend on the nature of the agent, its target, the character of the endemic area and many other factors, making it difficult to indicate precise safety measures for Stages 1 - 3. Annex I describes safety precautions which may be applied.

Stage 4 and 5 testing should not be started without a positive decision to release the control agent. However, precautions should be taken to investigate control measures against the exotic agent so that, if necessary, they could be rapidly implemented. For example, the inclusion of molluscicide trials for potential competitor snails would be a sensible addition to Stage 2f. During Stage 4 and 5 testing, provision should be made to monitor relevant alternative targets which may be affected by the control agent. If M. cornuarietis is used in rice-growing areas, rice fields should be visited regularly to detect any crop damage due to this snail. All competitor snail populations should be examined regularly for trematode larvae and those found should be identified in order to assess their importance.

Such a monitoring programme with competent staff capable of extended period. If the control tested, as suggested in the (McCullough, 198la), provision of programme's manpower requirements, them to fulfil their role.

presupposes the existence of an organization performing the appropriate checks over an

agent is being systematically developed and beginning of this section and elsewhere such trained staff should be included in the along with such resources as are needed for

5. AVAILABLE ANTAGONISTS: CURRENT KNOWLEDGE AND FUTURE PROSPECTS

Our knowledge of snail host antagonists -- microbial pathogens, para-sites • predators and competitors -- is still rudimentary. Recommendations relevant to each of these groups are given below.

5.1 Microbial Pathogens

is reasonable to snails, like other


Snail hosts respond to injury by means of a variety of defence mechanisms, such as phagocytosis by haemocytes, encapsulation and pearl formation. Invading pathogens may cause atrophy of certain organs, aplasia, necrosis and tissue liquification, alterations in tissue enzymes and haemolymph components, metaplasia, hyperplasia and possibly neoplasia. Physiological changes in fecundity, growth, locomotion and feeding behaviour may also occur in snails infected with particular pathogens.

To date, there has been very limited interest in snail host microbial pathogens. Only two laboratories, one in the Far East and the other in West Africa, have prepared research proposals. Not surprisingly, therefore, the number of microbial pathogens described from freshwater snails is relatively small and includes: mycobacteria and other bacterial agents, most of which have not been well defined; protozoa such as Hartmanella, Trypanoplasma, Dimoriopsis, Nosema, Plistophora, Unikaryon; and fungal organisms of unknown aetiology. Viral and rickettsial agents have not, as yet, been described from freshwater snails. Several laboratories in Europe and North America of fer services for the identification of microbial pathogens of invertebrates. No potentially useful pathogens have yet been identified.

5.1.1 Recommendations

The SWG recommends that further search for safe and cost-effective microbial pathogens of snail hosts should be encouraged. The document "Guide to field determination of major groups of pathogens affecting arthropod vectors of human disease" (WHO, 1982c) may provide useful general interim guidelines. It is proposed that a special guide for pathogens of snails of medical importance should be produced.

It is important that close collaboration be established between the small number of laboratories and scientists undertaking work on, or having a particular interest in, microbial pathogens and that these workers should liaise closely with scientists having special knowledge of snail host pathology and/or physiology.

5.2 Parasites

Parasites, including schistosomes, reduce the fecundity of snails. One field trial to prevent transmission of Schistosoma spindale failed to raise the infection rate with Echinostomum malayanum above 50%, despite the application of nearly 600 million eggs to a small pond containing an estimated 13 000 Indoplanorbis exustus over a seven-month period (Lie ~ ~-, 1974b); there was no noticeable reduction of the snail population. Another trial gave more satisfactory results, but the method was still very inefficient. More recently, Ribeiroia marini, a cathaemasid trematode, eliminated Biomphalaria glabrata from a pond in Guadeloupe (Nassi ~ al., 1979). Snail infection rates reached 85% after the addition of seven to nine million parasite eggs over a four-month period. As R. marini is a natural parasite of the little blue heron, Florida caerula, on the nearby island of St Lucia (Basch & Sturrock, 1969; Huizinga, 1973), its use might represent a threat to this and perhaps other water birds.

Along with competitor molluscs, studies on nonhuman trematodes have given rise to the largest number of field trials, mainly in Guadeloupe, Malaysia and, more recently, in the Niger. The results of these investigations, summarized by Combes (1982), indicate that while the approach may be effective, it will be rendered impractical by the need for repeated release of eggs. The cost of such operations and their evaluation is to be

is not simple and their operations.

ions


mechanisms of host populations involved in host/parasite systems undergoing increased parasite pressure should be noted. Moreover, because of the wellknown phenomenon of overdispersion of the parasites, the great difficulty of reaching the whole of the target mollusc population, even when miracidia are very numerous, must not be overlooked. However, Combes (1982) argued convincingly that the castration effect of parasitic trematodes deserves further study.

5.2.1 Recommendations

In general, high priority should not be accorded to support of research on parasites. However, nonhuman trematodes which castrate snails have had some effect, but more efficient parasites are needed and, if found, should be tested in properly conducted field trials.

In the control of S. manson!, it would be of interest to carry out well-designed trials in large transmission sites and determine the efficacy of a single massive egg release, with the ultimate aim of retaining or rejecting this approach.

Angiostrongylus cantonensis, a rat nematode, has been proposed as a biological control agent, but it is known to cause serious human disease in the Pacific region and its use is, therefore, not recommended.

5.3 Predators

Little research has been carried out in recent years on the efficacy of vertebrate predators of freshwater snails. McMahon and co-workers (1977) noted that the fish Astatoreochromis alluadi had a significant long-term effect on snail populations in artificial dams in Kenya, and, in Zimbabwe, Khaki Campbell ducks have been reported to suppress effectively snail populations in fish ponds. The use of such predators is probably of value only in certain specialized habitats.

Sciomyzid flies are obligate predators of mulluscs. The larvae of the 200 reared species of sciomyzid flies (of 600 described species) kill and feed only on aquatic and terrestial snails, eggs of snails, slugs, and fingernail clams. Prey and microhabitat selection ranges from broadly distributed to highly specialized, with the greatest number of agencies preying on several genera of freshwater, nonoperculate snails. A Central American sciomyzid that attacks Lymnaea which transmit fascioliasis has been introduced and established in Hawaii, but the impact of the fly on snail populations has not been determined (Berg, 1973). The larvae of most of the reared, aquatic sciomyzids attack various genera of pulmonate snails in the top few millimeters of the water, or on exposed vegetation or shorelines (Eckblad, 1973; Hairston et al., 1975). Although their effects will not be confined, therefore, to the sole target snail species, the larvae of aquatic sciomyzids are restricted to a specific range of aquatic microhabitats and could not pose a threat to terrestrial snails. Some sciomyzid larvae occupy intermediate microhabitats (shoreline situations) and introduction programmes involving such species would need to determine their microhabitat range and potential impact on terrestrial molluscs. At the present time, there is little direct evidence for the success or failure of sciomyzids as introduced biological control agents under field conditions, primarily because there have been insufficient field studies or biological control attempts.

Some vertebrate predators, especially contribute to the snail host .g.

evidence of The

see

TDR/'BCv-SCH/5 IH/ 84. 3 page 16

McCullough, 1981 b) . Search for sciomyzids with sui table predator properties (see p. 9), with narrow prey ranges and with the ability to search for prey in deeper water , needs to be pursued among the two-thirds of the species of sciomyzids that r emain biologically unknown. The many species of semi-aquatic s c iomyzids that have larvae living in marginal aquatic situations, and those that inhibit small, dispersed bodies of water and headwater situations , need to be examined fo r their potential as biological control agents.

5 .4 Competitor s

In recent years, many authors have published the r esults of their findings on intermolluscan competition involving either prosobranch or pulmonate species (see reviews, among others, by Hairston et a l., 1975; Ferguson, 1978; Frandsen & Madsen, 1979; Jordan et al., 19807"" McCullough, 198la; Pointier , 1983). The more promising competitors--are discussed briefly below.

Helisoma duryi, a New World pulmonate snail, was many years ago observed to displace Biomphalaria spp. in aquaria and has been transpor ted, probably accidentally and mainly via the aquaria trade, to many parts of the tropics . Limited field t rials in Egypt and the United Republic of Tanzania have not given particularly encouraging results (Hairston et al. , 1975; Madsen , 1983) and suggest that it may survive in certain r estricted--microhabitats whi ch only partly overlap those of the target snails . The superficial appearance, especially of certain ecophenotypes, may cause even experienced field workers to mistake it for Biomphalaria (Prenti ce !:!. !.!_., 1977). In a careful review, Frandsen and Madsen (1979) f ound that no trematodes of medical or veterinary importance have to date been r eported to infect any species of this genus. !!· duryi, in particular, was remarkably free of t r ematode parasites. Recent examination of a small sample f r om a population established for at least seven years in a Tanzan ian irrigation s cheme fa iled to reveal any trematodes (Madsen, 1983).

Marisa cornuarietis , a South American ampul l a rid snail with a voracious appetite for higher plants , eliminates Biomphalaria and Bulinus spp. from laboratory tanks as well as from experimental and certain natural field sites . It acts primarily by competition for food , modifying the nature of the habitat and destroying the niches occupied by the target snails; a secondary effect is the predat ion, which may be accidental , of egg masses and hatchlings of the target snail (WHO, 1982b). It is refractory to infection wi th Paragonimus westermani, Cl onorchis sinensis and Fasciola hepatica and does not appear to transmit Puerto Rican avian schistosomes in the field (Ferguson, 1978), but it has been found to be naturally i nfected with strigeid cercariae in Venezuela (Nasir et al. , 1969). Some r eports have incriminated Marisa of feeding on rice seedlings in the field (Ortiz-Torres, 1962; Yeo & Fisher, 1970), and snails of related genera, Pomacea lineata in Surinam (Dinther, 1956; Grist, 1968) and Lanistes spp. in Swaziland (Crossland, 1965), have been reported as pests of commercial (swamp) rice. Species of the latter genus are both common and widely distributed in Africa and , apart from Crossland's findings, which need to be confirmed, have never been incriminated as pests of r ice . I n addition, laboratory studies in Egypt ( Demian & Ibrahim, 1969) and the United Republic of Tanzania (Msangi & Kihaule, 1972) showed that Marisa does not eat either young or old rice leaves, even if no other food is available.

In Brazil, the general absence of Biomphalaria spp. in habitats containing Pomaces australis stimulated labor atory t ests of its compet itive ability (Paulinyi & Paulin!, 1?72) . The related s pecies, !· glauca, was widely distributed in certain habitats on St Lucia, sharing sites with .!!_. glabrata (Sturrock, 1974) in areas where S. manson! t ransmission was prevalent. Trials in simulated field habitats showed that a starting ratio of 3:1 of P. glauca: B. glabrata was necessary t o eliminate the latter within a six-month period.


With progressively lower ratios, !· glabrata populations either declined (but were not eliminated) or remained steady or even increased over the eight-month period, though less rapidly than a population of !· glabrata alone (Upatham & Sturrock, unpublished da ta). A field trial revealed no significant effect when P. glauca were added to !· glabrata populations (Prentice, quoted in Jordan et al., 1980). Pomacea has been implicated in damage to swamp rice (Dinthe;:-1956).

Thiara granifera has been introduced from South-East Asia to the Caribbean region, probably on aquatic plants through the aquaria trade (WHO, 1981). Its rapid natural sprea d in certain areas apparently coincided with the disappearance of Biomphalaria spp. This observation was confirmed when it was deliberately introduced into parts of the island of St Lucia (Prentice, 1983). It feeds on detri tus, di atoms and algae, and, being ovoviviparous, it is a prolific breeder. It is not ye t known precisely how it competes with Biomphalaria spp. (WHO, 1981). .!.· granifera can transmit a variety of other trematode parasites of relatively mi nor socioeconomic importance (TuckerAbbot t , 1952; Malek & Cheng, 1974). As Paragonimus and Metagonimus spp. may infect man, the use of Thiara in the biological control of schistosomiasis has been viewed with some reserve. However, McCullough and Malek (1984) and Prentice (1983) have recently questioned this view and have called for a more balanced approach.

5 .4.1 Recommendations

The competitors are considered to be the mos t promising group of snail host antagonists so far i denti fi ed and a search for additional species should be encouraged. Apart froM their direct effect on target snail numbers, there is some evidence t hat t heir presence may influence the success rate of miracidia! penetration by acti ng as a Miracidia! sponge or through a 'decoy effect 1 • The known competitors may be classed int o t wo groups by descending order of effectiveness.

In the first group are those in which schistosome miracidia fail t o penetrate and thus lose their infective capacity when they encounter an appropriate snail host. This group includes:

Thiara granifera: This is probably the best candidate so far available, but its role in the transMission of Paragonimus spp. needs to be further clarified. With regard to thiariid competitors, the Consultation, in addition, recommended suppor t for research t o:

undertake further well-designed field studies, especially i n the neotropics;

clarify thiariid t axonomy;

establish an inventory of strains of Thiara and related genera having competitor potential;

study the bionomics (life-table patterns, fecundi t y, su rvival characteristics, etc. ) of different species and strains;

investigate their habitat requireMent s and range;

study compatibility of Caribbean and Oriental thiariids , together with closely re l ated African species , for common Paragonimus spp.;

identify definitively the mollusc s pecies responsible for the t ransmiss i on of the zoonotic Paragonimus spp . in Centra l and West Africa;


determine, with as much prec1s1on as possible, the mechanism of the competitive effect of thiariids.

Marisa cornuarietis: These snails can be good antagonists in lentic waterbodies. They may eat rice seedlings, but their capacity to harm rice production, together with their ability to survive in temporary waterbodies, including rice fields, in different climatic zones in the tropics, needs further research. In addition, the Consultation recommended support to:

investigate the role of cornuarietis as a rice pest in areas (e.g. Trinidad) where the species is known to exist and where rice growing is already a major resource;

undertake rigorous studies of its performance in a range of habitats in the neotropics;

study optimum mass-rearing and seeding characteristics with reference to different biotic and abiotic factors in different climatic zones;

determine effects of temperature (degrees and exposure periods) on population dynamics with a view to using these snails in northern and southern extreme ranges as well as in areas of higher altitude where schistosomiasis is endemic;

monitor the biology and competitive effects of Marisa in the manmade, isolated habitat at Kisangara, in the north-west of the United Republic of Tanzania.

Helisoma duryi: meagre evidence permanent field support to:

This is apparently a safe competitor but there is only that it is an effective antagonist even in lentic, habitats. The Consultation therefore recommended

undertake more rigorous field trials to demonstrate its success, particularly over prolonged periods, or failure in habitats typical of transmission sites;

study optimum mass-rearing and seeding requirements.

In the second group are those competitors in which schistosome miracidia penetrate but thereafter become encapsulated and fail to produce an infection. This group comprises:

Biomphalaria straminea: This is a relatively poorly susceptible or insusceptible Biomphalaria which has been remarkably successful as a biocontrol agent in Martinique. However, in Brazil some strains of this species are effective intermediate hosts, making up for their very low infectivity by their very high population density. Although refractory populations of otherwise susceptible Biomphalaria have been proposed as competitors, there is no evidence that such populations will remain refractory. The Consultation, therefore, does not at present recommend that research on this approach be supported, for both practical and theoretical reasons, except perhaps in very special situations.

which it

become established


Dam. The Consultation considered that much sound laboratory and field research on the ecology of ~· tropic us, host species and its possible role in S. to be undertaken before its release in contemplated without serious reserve.

6. COSTS

its relaUonships with snail transmission would have

exotic situations could be

The broad idea behind classical biological control is that an antagonist (including a competitor) will fit so well into its new environment that it will effectively control the target organism and that this effect will be maintained unless the environment is profoundly modified. Careful cost estimates for introductions of biological control agents are rare. Valid available estimates concern mainly biocontrol operations carried out in the United States and refer exclusively to antagonists of agricultural pests. These estimates vary considerably according to the items which have been included in the calculation. Less conservative estimates range from US$ 127 150 to US$ 200 000 depending on the agent introduced. Data from the United States show that the rate of successful introduction has been 1 to 6, and that in these circumstances the cost of a biological control operation may range between us$ 800 000 and us$ 1.25 million. The cost may be considerably reduced if the same antagonist is used for several introduction operations and rearing confined to the first introduction. In developing countries, the cost of research on promising antagonists may vary from a relatively modest sum to over US$ 3 million. In some developing areas, costs might be higher than in North America, as the necessary equipment for introduction and post-introduction requirements are often not locally available.

With regard to biological control of snail hosts, there is only one operational study from Puerto Rico which showed that the use of Marisa is 60 times cheaper than the application of molluscicides. However, the cost of harvesting individual Marisa from holding ponds and transporting them to other habitats was us$ o. 031 per planted snail or us$ 7. 00 per week, excluding supervision and overhead costs (Jobin & Berrios-Duran, 1970).

On the basis of these considerations, it can be anticipated that for certain competitors operational costs will be very low. However, should a microbial pathogen be utilized, costs may be similar to those for the development of Bacillus thuringiensis. It seems reasonable at this time to anticipate that in transmission sites where its use is thought promising, biological control will be cost-competitive with conventional chemical control procedures.

7. TRAINING, RESEARCH COORDINATION AND INFORMATION TRANSFER

7.1 Training

An important and essential consideration of any research or control programme, and perhaps the one in most urgent need of implementation, is the training of an adequate cadre of scientific and technical staff. Since biological control is a sophisticated discipline requ1r1ng highly skilled individuals for the identification, cultivation and evaluation of potential control agents, it is strongly suggested that the recruitment and training of such personnel be a serious consideration in determining the feasibility of this approach.


of trainees should receive as broad a training and experience Ideally, such individuals should have a sound knowledge of the snail/parasite biology, population ecology and statistics, subjects, so that they may interact with specialists in these disciplines.

as possible. principles of

among other and ancillary

The training of personnel to be involved in biological control of snail hosts is considered further in Annex III.

7.2 Research Coordination

It is anticipated that TDR's Scientific Working Groups on Schistosomiasis and on Biological Control of Vectors could: i) identify research needs and priorities; ii) gather and disseminate pertinent literature; iii) provide a network for the exchange of information among workers in the field and encourage possible collaborative arrangements; iv) stimulate the submission of research proposals and provide modest funding for approved projects; and v) undertake site visits to selected projects with the aim of improving coordination, experience and continuity.

7.3 Information Transfer

It is strongly recommended that the data sheets on potential control agents presently issued by the Division of Vector Biology and Control (VBC), WHO, Geneva, be continued, updated periodically and expanded as the need arises. In addition, there is a need for a bibliography covering previously published studies with provisions for annual supplements. The literature on biological control of snail hosts is scattered through a variety of journals published in several languages. A bibliographic review will therefore be of particular value to individuals with limited library facilities. The transfer of information from ancillary disciplines (e.g. pest management, population ecology) will foster an expanded view of the problems at hand and could contribute to their resolution. Although it may be premature at this time, it is hoped that a computerized retrieval service will be set up under VBC auspices. VBC should provide information on sources of biological control agents and a list of collaborating snail identification centres. Some useful references on biological control of snail hosts are given in Annex IV.

8. GENERAL RESEARCH PRIORITIES AND RECOMMENDATIONS FOR FOLLOW-UP ACTION

Apart from more specific recommendations made in earlier sections of this report, the Consultation 1 s overall recommendations, in view of the need for concrete follow-up action, are to support:

properly conducted, scientifically acceptable, controlled field trials of potential control agents, particularly competitors;

ecological and taxonomic studies of target and other aquatic snails in order to improve the application of biocontrol agents;

long-term monitoring of existing biocontrol projects (e.g. in Martinique, St Lucia, the Sudan, the United Republic of Tanzania, etc.);

exchange of materials between interested centres;

relevant studies indicated agents

the check-list for spec

TDR/BCV-SCH/SIH/84,3 page 21

investigations on any agents which might be used against lanids, either separately or in combination with other procedures;

oncomecontrol

studies on the relationships between antagonists and chemical and environmental control methods;

the preparation of inventories of important transmission sites in endemic areas where biological control could be regarded as desirable and/or feasible, and basic ecological studies of representative sites prior to release of antagonists;

the compilation of an updated reference list which should be circulated to interested parties and which would include recent work on the biological control of snail species;

the compilation of a document providing names and addresses of research workers and institutes throughout the world who are either actively engaged in work on biological control agents of snails or who intend to do research in this area;

the release of research funds for i) carefully designed field trials involving the introduction of competitors, and ii) the continued monitoring of snail abundance in habitats in which competitors are already present or have been introduced.

Finally, both national and international institutions should be aware of the danger of a predicted future decline in research expertise in the field of malacology and freshwater biology/ecology. Training programmes for research workers and technicians from developing countries should therefore be encouraged and training fellowships made available.

9. ACKNOWLEDGEMENT

All who took part in the Consultation acknowledge with sincere gratitude the conscientious and prompt help and administrative assistance given by Miss Helen McLaughlan, ECV/VBC, during all stages of the meeting.

10. LIST OF PARTICIPANTS

ANDERSON, Prof. R.M., Department of Zoology, Imperial College, London University, Prince Consort Road, London SW7, UK

COMBES, Prof. C., Departement de Biologie Animale, Universite de Perpignan, Avenue de Villeneuve, Perpignan Cedex 66025, France

DELUCCHI, Prof. V., Institut fUr Phytomedizin, E.T.H. Zentrum- CLS, 88092 Zurich, Switzerland

FRANDSEN, Dr F., Director, Danish Bilharziasis Laboratory, Jaegersborg Aile lD, 2920 Charlottenlund, Denmark

HAIRSTON, Prof. N., Department of Biology, University of North Carolina at Chapel Hill, Wilson Hall 046 A, Chapel Hill, NC 27514, USA (CHAIRMAN)

Prof. of Preventive Medicine Uniformed Services University of Health Sciences


ODEI, Dr M.A., Director, Institute of Aquatic Biology, P.O. Box 38, Achimota, Ghana (VICE-CHAIRM~~)

PRENTICE, Mr M., Wellcome Trust Research Laboratories, P.O. Box 43640, Kenya (RAPPORTEUR)

STURROCK, Dr R., London School of Hygiene Field Station, 395 Hatfield Road,

WHO Secretariat

vlinc he s Farm

DIXON, Mr H., Epidemiological and Statistical Methodology, Division of Epidemiological Surveillance and Health Situation and Trend Assessment

DUBITSKIJ, Dr A., Pesticides Development and Safe Use, Division of Vector Biology and Control (Secretary, Steering Committee on Biological Control of Vectors)

McCULLOUGH, Dr F.S., Ecology and Control of Vectors, Division of Vector Biology and Control (SECRETARY OF THE CONSULTATION)

MOTT, Dr K.E., Chief, Schistosomiasis and Other Snail-Borne Trematode Infections, Parasitic Diseases Programme (Secretary, Steering Committee on Schistosomiasis)

PANT, Dr C., Chief, Ecology and Control of Vectors, Division of Vector Biology and Control

RISHIKESH, Dr N., Ecology and Control of Vectors, Division of Vector Biology and Control

VANDEKAR, Dr M., Pesticide Development and Safe Use, Division of Vector Biology and Control (Secretary, Scientific Working Group on Biological Control of Vectors)

ANNEX I

TDR/BCV-SCH/SIH/84.3 ANNEX I page 23

RECOM}fENDED SAFETY PRECAUTIONS TO BE TAKEN WHEN TESTING A BIOLOGICAL AGENT IN AN ENDEMIC AREA BEFORE ITS RELEASE IS APPROVED

The following suggestions are made primarily with competitor snails in mind, as they seem at present to offer the most hopeful biological control agents against schistosomiasis. Similar, and possibly more stringent, precautions woufd be necessary for some pathogens, parasites, predators and other types of competitors, especially those with greater powers of dispersal than aquatic snails.

Laboratory precautions for Stage 1 and 2 testing*

The exotic snails should be kept in a locked room within the laboratory to minimize the risk of accidental removal by unauthorized people. Any 'equipment' taken into this room should be treated as 'contaminated' and should not be removed from the area until it has been 'decontaminated'. This applies to aquaria, beakers, sieves, forceps, water containers and any other item taken into the area. On no account should such items be taken directly into other rooms containing colonies of indigenous snails kept without full safety precautions. Similarly, waste water and debris from aquaria should not leave the rooms until they have been suitably treated. The main risk is that eggs or minute young snails will accidentally be carried out of the rooms. The water drainage system of such rooms will need to be made safe.

Decontamination may be achieved by various methods. Immersion in a bath of a suitable, cheap chemical solution (e.g. formalin, acetic acid, iodine solutions, alcohol, chromic acid) will be effective. The use of toxic chemicals in a snail room may pose problems and threaten the survival of the snail under test and, for this reason, molluscicides are not recommended.

Small items may be placed in a suitable bath of such a solution but larger items, such as aquaria, will probably have to be rinsed in it, washed and dried. Bulky liquid waste may also be treated with a concentrated solution of formalin. On no account should untreated waste water be poured down a sink connected to a general sewerage system. Even if a mosquito gauze screen is placed across the exit hole, there is a high risk that hatchling snails will pass through.

Heat provides a suitable alternative. Small items placed in boiling water for a few minutes will be satisfactorily decontaminated, and drying in an oven at 100°C would be equally effective. Full-scale autoclaving is unnecessary for snails, but might be required if pathogenic bacteria and viruses were being tested.

All windows to the restricted rooms should be screened against insects. Although the risk is remote, it is possible that some large insect species, especially water beetles, might carry out egg masses or hatchling snails. In particular, screening against insects should always be used to prevent breeding of vector mosquitoes. Similarly, the room should be made rodent-proof, as rats and mice might carry larger snails out of the room,

See IL

TDR/BCV-SCH/SIH/84.3 ANNEX I page 24

Stage 3 testing has to be done outdoors and hence carries a much greater risk of the exotic snail escaping than laboratory testing. The test area should be access! ble, fenced and locked to keep out unauthorized people. In addition to fencing, the area should be screened with a suitable wire or synthetic mesh on a sturdy frame to keep out rodents, birds (especially water birds) and aquatic flying insects.

As with laboratory testing, all equipment brought into the test area must be decontaminated before it is removed. The much greater volumes of water used in the simulated habitats pose a special problem. With regard to water entering the site, suitable precautions must be taken to ensure that no unwanted organisms (including snails) will be able to enter through the water supply. It is also essential to decontaminate this water before it is returned to the natural environment. One method would be to construct a subsurface drainage soak-away system where it is certain that the water will slowly pass underground for a sufficient distance before reaching the surface. Even better would be to pass the water into a covered, low-lying sump within or adjacent to the test site, where it could be treated chemically to kill any snails, held for an appropriate period and then pumped into a subsoil soakage pit rather than into open drains. Molluscicides could be used in this case if there is no risk of their contaminating the test sites.

Another problem is flooding during torrential tropical storms. Test sites may be filled rapidly by rain and overflow. Surface flood water may wash through the sites within the protected area. Roofing will be impracticable for extensive sites and may be undesirable, preventing the simulation of natural conditions. A system of protective walls and ditches could be used to run any spillage from the test sites into a sump to await chemical treatment or into a suitable soakage pit. In the same way, a system of drains could be constructed a) to carry away surface water falling within the area but not coming into contact with the test sites, and b) to divert external flood water away from the area.

Costs

The precautions recommended in the two previous sections will cost money. In any case, those for indoor, laboratory snail rooms would be good practice when maintaining indigenous (or exotic) snail colonies in laboratories within an endemic area. Whether the extra costs involved in the precautions recommended for Stage 3 (outdoor) testing are justifiable depends to some extent on the potential dangers of any specific agent. Savings may be made where these can reasonably be shown to be very low. However, to cut costs with regard to research on agents which carry serious risk, however slight, would be negligent.

ANNEX II

TDR/BCV-SCH/SIH/84.3 &"JNEX II page 25

GUIDELINES FOR RESEARCH TO DETER}IINE THE USE OF EXOTIC BIOCONTROL AGENTS OF SNAIL HOSTS

A provisional protocol for field testing of biological control agents of snail hosts was given in Annex VII of the report of the Sixth Scientific l._!orking Group on Vector Biology and Control (WHO, l982d). lmile this protocol may be consulted, the present guidelines, which also mainly apply to snail host competitors, provide a more rigorous approach, especially in regard to experimental design and sampling procedures.

In broad terms, the introduction of any biological control agent should proceed in two stages (see also the schema given in Table II of this report):

an experimental stage in which both the effectiveness and the acceptability of the agents are rigorously assessed;

an operational stage in which the agent is put to practical use.

Needless to say, the outcome of the experimental activities will determine whether the operational tasks should be undertaken and under what conditions.

In order to reduce to a minimum the risk of accidental escape of the proposed control agent (see Annex I), the experimental stage should be carried out under conditions of strict security.

Experimental procedures to determine the effectiveness of the agent

The effectiveness of the agent against local snail hosts should be tested under an experimental design which will give definitive answers to the expected reduction in density of snail host populations and the duration of such effects. Such answers depend upon the observation of elementary scientific and statistical principles.

In all field situations, each location will be different to some extent, and these differences must be assessed in the design of the experiment. A sufficient number of replicates of each treatment should be provided. The larger the nu.rnber of replicates, the greater the amount of variability that can be taken into consideration. No estimate of variation can be made with fewer than two replicates of each experimental condition, and variability in the field is frequently so great that more replicates are needed. If the conditions are not obviously different on casual inspection, three replicates may suffice. This means that to answer the question whether the introduced species has had an effect, the minimum requirement is for six experimental ponds or selected habitats which can be kept in isolation; i.e. three for introduction and three for comparison in which no manipulation will be carried out.

A satisfactory method of estimating the mean density in each habitat or artificial pond may have to be decided in advance of the experiment itself. Experience with both Bulinus and has indicated in the past that

TDR/ BC\r-SCH/SIH/84. 3 ANNEX II page 26

the marked snails mix randomly with the total population between collecting;

no losses or recruitments have taken place (or, if so, can be measured);

marks do not change death rate or fecundity.

The mean density per habitats in a statistical in degrees of freedom. independent values.

unit area can then be estimated and used to compare analysis. Notice that the 30 samples do not count They provide accuracy only for means, which are

More complex questions require a more complex design and will surely require more total replicates. Thus, if it is important to assess the number of antagonists that must be released in order to achieve the required results, each planned density must also have three replicate habitats or artificial ponds. It is probable that the principal investigator will have some prior information about the annual changes in snail abundance, and this knowledge should be used in deciding the frequency of sampling to be employed.

Experimental procedures to determine acceptability of the agent

The method of assessing damage by the introduced species will depend on its specific characteristics. Since Marisa is of concern mainly as a potential pest in certain kinds of rice field (it has been reported to eat submerged seedlings), small replicate paddies will be required (numerical requirements given above), and some means of measuring damage must be found.

Thiara, on the other hand, is of concern as a potential intermediate host of harmful trematodes. Its susceptibility should be tested in the laboratory, using sufficient numbers to provide reasonable assurance of safety. Other factors affecting real or hypothetical risks of introducing Thiara should also be carefully considered (e.g. would Paragonimus infection really increase if Thiara were introduced).

Helisoma appears to be innocuous, hence carries the least risk from introduction and thus requires no special experiments under this heading.

Operational procedures

A candidate antagonist which meets the prior requirements on experimental testing should be introduced into a number of natural habitats. These should be chosen so as to enable the effects on the snail host population, and subsequently those on the transmission of schistosomiasis, to be assessed as rapidly as possible.

Assessment of the effect on humans should focus on children who were originally negative without prior treatment. This will, of course, require the identification of individuals and observations should be made before and after any season of transmission for as long as the necessary data are required. A comparison where no antagonist has been introduced is scientifically desirable, if ethical clearance can be obtained.

A general description of the biotope should be prepared, and pre-trial activities should least one year, so that all normal seasonal condi t

TDR/BCV-SCH/SIH/84.3 ANNEX II page 27

abiotic factors, especially temperature, rainfall and turbidity;

biotic factors (e.g. aquatic non-target fauna and/or flora, seasonal density and age-structure of snail hosts).

The methods employed should be carefully described and standardized (i.e. the same sampling r:1ethods must be employed during the pre-trial and subsequent phases). Various sampling methods have been described. They should be quantitative and take into account the physical and other characteristics of the habitats and, as far as possible, their validity should be properly evaluated.

Snail should, be presence or sufficient. the habitat.

sampling for operational activities can, and for practical reasons quite simple. If enough habitats are included, data on the

absence of the antagonist and the intermediate host may be Sampling should, however, cover as far as possible all parts of

With regard to the presentation and treatment of collected data, standard forms should be prepared, if possible, in such a way that the data can be processed by computer. Close and continuous collaboration with a statistician, preferably with a knowledge of biological processes, is desirable.

It is recommended that the identification of the selected competitors, as well as of the local snail hosts, be confirmed by competent malacologists. Moreover, agricultural practices involving, for example, the growing and production of rice, must be taken into consideration. The data sheets on certain prom~s~ng competitors* will be found useful for decision-making purposes.

TDR/BCV-SCH/SIH/84.3 ANNEX III page 28

ANNEX III

TRAINING OF PERSONNEL IN BIOLOGICAL CONTROL OF SNAIL INTERMEDIATE HOSTS

The biological control of vectors, involving the production and application of living organisms, must enlist the local community, in addition to professional personnel, in order to reduce costs and also sustain local interest in the control effort. Thus, three levels of training programmes will be required.

l(a) Training needs of the professional team/project leaders

These needs include:

identification (taxonomy) of the snail hosts;

identification (taxonomy) of the biocontrol agent(s);

search for agents;

development and production of agents;

laboratory and field trial methodologies;

sampling techniques for target and non-target organisms in the various habitats;

evaluation techniques, including safety tests.

(b) Training of technical support staff

Training requirements will consist of a simplified version of the above to enable the staff to assist the principal investigator in the various laboratory and field work involved. These needs would include, for example:

identification and mapping of transmission sites;

collection of data by sampling for evaluation and monitoring of target and non-target organisms;

mass breeding, if necessary, and application (seeding procedures) of control agents.

(c) Training the community

Such training will be given mainly to enable the community to understand the basis of the control measures being applied and, if appropriate, to enable them also to produce the agents, apply them and ensure that they are always present.

2. Mode of training

The may be considered

technical s

and

TDR/BCV-SCH/SIH/84.3 ANNEX III page 29

incorporation into the curriculum of paramedical training in endemic countries (technical staff);

staff

inclusion in health education programmes in endemic countries (community);

courses of varying periods given, for example, at the Danish Bilharziasis Laboratory, Copenhagen (for professional and technical personnel).

Sources of personnel for training

(i) Professional

Appropriate professional staff employed by institutions such as the Ministry of Health would be obvious candidates for training. In addition, perhaps to avoid the problems of having to create new career and professional structures, suitable persons could be taken from universities and research institutes and assigned to projects as team leaders while still serving in their parent institutions.

(ii) Technical

Technical staff may serve in existing disease and/or vector control units or in polyvalent health delivery systems. The present training component would therefore add to their existing knowledge.

TDR/BCV-SCH/SIH/84.3 ANNEX IV page 30

ANNEX IV

SOME USEFUL REFERENCES ON BIOLOGICAL CONTROL WITH PARTICULAR RELEV&~CE TO SNAIL INTERMEDIATE HOSTS

&~DERSON, R.M. The regulation of host population growth by parasitic species. Parasi !!]_: 119-157 (l978a).

ANDERSON, R.M. Population dynamics of snail infection by miracidia. Parasitology, 22: 201-224 (1978b).

ANDERSON, R.M. Parasite pathogenicity and the depression of host population equilibria. Nature, 279: 150-152 (1979).

ANDERSON, R.M. Depression of host population abundance by direct life cycle macroparasites. J. Theor. Biol., ~: 283-311 (1980).

ANDERSON, R.M. Population ecology of infectious disease agents. In: Theoretical Ecology. (R.M. May, ed.) Oxford: Blackwell Scientific, 1981, pp. 318-355.

ANDERSON, R.H. (ed.) Applications.

Population Dynamics of Infectious Diseases: London: Chapman and Hall, l982a.

Theory and

ANDERSON, R.H. Theoretical basis for the use of pathogens as biological control agents of pest species. Parasitology, 84: 3-33 (1982b).

ANDERSON, R.H. & HAY, R.M. Regulation and stability of host-parasite population interactions. I. Regulatory processes. J. Anim. Ecol., 47: 218-247 (1978).

ANDERSON, R.H. & HAY, R.H.. Population biology of infectious diseases. I. Nature, 280: 361-367 (1979).

ANDERSON, R.H. & HAY, R.M. The population dynamics of micro-parasites and their invertebrate hosts. Phil Trans Soc. London B291: 451-524 (1981).

ANDERSON, R.M. & MAY, R.M. Directly transmitted infectious diseases: Control by vaccination. Science, 215: 1053-1060 (l982a).

ANDERSON, R.M. & MAY, R.H. Population dynamics of human helminth infections: Control by chemotherapy. Nature, 297: 245-248 (1982b).

ANDERSON, R.M. & MAY, R.M. models, population (1984).

Helminth infections of humans: Mathematical dynamics and control. Advances in Parasitol

ANDRADE, R.M. Biological control of Schistosoma mansoni intermediate hosts through Pomacea haustrum (Reeve, 1843). Proc. Parasit., Hunich (1974).

ANON.

TDR/BCV-SCH/S I H/84.3 ANNEX IV page 31

ANSARI , N. (ed . ) Epidemiology and Cont ro l of Schistosomiasis ( Bi l harzias is). Basel: S . Karger, 1973, 752 pp .

BAKER , K. F. & COOK, R.J. Biological Control of Pl an t Pathogens . Ox ford: W.H. Freeman, 1974, 433 pp .

BARBOSA, F.S . Possible compe t itive displacement and evidence of hybridization between two Brazilian species of planorbid snai l s . Malacologia, 14: 401- 408 ( 1973).

BARBOSA, F.S. & BARRETO, A.C. Differences in susceptibili ty of Brazilian strains of Australorbis g l abratus to Sch i stosoma mansoni. Exp. Parasitol., ~: 137- 140 (1960).

BASCH, P. F. & STURROCK, R. F. Life history of Ribeiroia ma rini (Faus t and Hof fman, 1934) comb. n. (T rema t oda: Cathaemasiidae ) . J. Paras i tol., 55: 1180-1184 (1 969).

BERG, C. O. Biological control of sna i l-borne d iseases: A r eview. Exp. Parasitol . , 33 : 318-330 (1973).

BERRY , E. G. A recently obse r ved snail disease . Ann. Rep. Amer. Malacol . Uni on News Bull., 10-11 ( 1949).

BLACKBURN, R. D. , SUTTON, D.L. & TAYLOR, T.M . Biological control of aquatic weeds . Proc . Amer. Soc. Civil Eng., 97; 421-432 (1971).

BOTTRELL, D.G. Integ ra t ed Pes t Management. Prpt. Counci l Environmenta l Quali ty, U.S. Gov t. Printing Off. (197 9).

BROWN, D. S. Freshwater Sna i ls of Africa and their Medica l Importance. London: Taylor and Francis , 1980, 487 pp.

BUNDY, D.A.P. & COOPER, E.S. Report on the Caribbean Pa r as itoses Workshop. (D.A.P. Bundy , ed.) Department of Zoology, University of the West Ind ies, Kingston, Jamaica, 1983, 33 pp.

CEDENO-LEON , A. & THOMAS, J . D. Competi t ion between Biomphalaria glabrata (S) and Marisa cornuarietis (L) : Feeding niches. J. Appl. Ecol. , 19: 707-721 (1982).

CHERNIN, E. Interferenc e wi th the capacity of Schistosoma manson! miracidia to infect the molluscan host . J . Parasitol . , ~: 509-516 (1968).

CHRISTIE, J . ET AL. Interactions be tween St . Lucian Biompha1aria glabrata and Helisoma duryi , a possible competitor snail, i n a semi -na t ural hab i tat. Acta Trop ., 38: 395- 417 (1981) .

CLAUSEN, C.P. (ed.) I ntroduced Parasites and Predato rs of Arthropod Pests and We eds: A Wor ld Revi ew. USDA: Agr. Handbook No . 480 , 1978, 551 pp.

COLLIER, B.D., COX, G.W., JOHNSON, A.W. & MILLER , P.C. Dynami c Ecology. Eng lewood Cli ffs , NJ, USA: Prentice-Hall, 1973 , 563 pp.

COMBES, C. Trematodes : Antagonism be tween species and s teril izing effect on s nail s in biologica l control. Parasi t ology, 84 : 151-175 (1982) .

COMBES, C. & McCULLOUGH , F. Le controle des mol l usques vecteurs de schis t osomes: Result a t s rec:en ts e t perspec tives. Rev. I be r. Paras i t., Vol . Ext ra : 5-14 (1982).


COMBES, C. & MONE, H. Resultats preliminaires d'une etude de l'influence des non cibles sur la transmission du mansoni. Bull.

_______ __;:;:.~-·' .!_: 23-26 (1983).

COPPELL, H.C. & MERTINS, (West)-Heidelberg-New

CROSSLAND, N.O. The pest status and control of the tadpole shrimp, and of the snail, in Swaziland

-'----'-'---'------'--· ' ~: 115-12 0 (

Berlin

DAVIS, G.M. & RUFF, M.D. Oncomelania hupensis (Gastropoda: Hydrobiidae): Hybridization, genetics and transmission of Schistosoma Malacol. Rev.,~: 181-197 (1973).

DAZO, B.C., HAIRSTON, N.G. & DAWOOD, I.K. The ecology of Bulinus truncatus and Biomphalaria alexandrina and its implications for the control of bilharziasis in the Egypt-49 project area. Bull Hlth. 35: 339-356 (1966).

DEAN, W.W., MEAD, A.R. & NORTHEY, W.T. Aeromonas liquefaciens in the giant African snail, Achatina fulva. J. Invert. Pathol., 16; 346-351 (1970).

DEBACH, P. (ed.) Biological Control of Insect Pests and Weeds. London: Chapman and Hall, 1964, 844 pp.

DEBACH, P. The competitive displacement and coexistence principles. Ann. Rev. Entomol., !.!_: 183-212 (1966).

DEBAGH, P. Biological Control by Natural Enemies. Cambridge: Cambridge University Press, 1974.

DEBACH, P., ROSEN, D. & KENNETT, C.E. Biological control of coccids by introduced natural enemies. In: Biological Control. (C. B. Huffaker, ed.) New York: Plenum Press, 1971, pp. 165-194.

DEBACH, P. & SUNBY, R.A. Competitive displacement between ecological homologues. Hilgardia, ~: 105-166 (1963).

DE BONT, A.F. & DE BONT HERS, M.J. Mollusc control and fish-farming in Central Africa. Nature, 170: 323-324 (1952).

DEMlAN, E.S. & IBRAHIM, A.M. Feeding activities of the snail Marisa cornuarietis (L) under laboratory conditions. Proc. Sixth Arab. Sci. Congress, 145-165 (1969).

DEMlAN, E.S. & LUFTY, R.G. Prospects of the use of Marisa cornuarietis in the biological control of Lymnaea caillaudi in .A.R. Proc. __ .:__.---'"'"'-'--Acad. Sci., 18: 46-50 (1965a).

DEMIAN, E.S. & LUFTY, R.G. Predatory activity of Marisa cornuarietis against Bulinus (Bulinus) truncatus the transmitter urinary schistosomiasis .

. Hed. Paras . , ~: 331-336 (l965b).

DEMIAN, E.S. & LUFTY, R.G. Predatory activity of under laboratory

l965c).

and


DESCHIENS, R., LAMY, L. & LAMY, H. Sur un ostracode predateur de Bulinus et de Planorbis. Bull. Soc. Pathol. Exot., ~: 956-958 (1953).

DINTHER, J.B.M. van. Control of Pomacea (Ampullaria) snails in rice fields. Bull. landbouwp roefstation (Surinam) 68: 1-20 (1956).

DOBY, J . M., MANDAHL-BARTH, G. , CHABAUD, A. & DEBLOCK, S. Elimination de Bulinus truncatus rivularis (Philippi) de collections d'eau connues pour l'h6berger par Po tamopyrgus jenkins! (Smith, 1889) (Hydrobiid€s), et utilisation 6ventuelle de ce mollusque pour le controle biologique des bilharzioses. C. R. Acad. Sci. (Paris) 261 : 4244-4246 (1965).

DUBITSKIJ, A.M. Justification of early field introduction of promising vector control agents as a method for evaluating their potential. Proc. Third Internat. Col!. I nvert. Pathol., 1982, pp . 437-442.

DUCKLOW, H.W., BOYLE, P.J., MAUGEL, P.W., STRONG, C. & MITCHELL, R. Bacterial flora of the schistosome vee tor snail Biomphalar ia glabrata. Appl . Environ . Microbiol., 38(4): 667-672 (1979).

DUNCAN, J. & STURROCK, R.F. Methodology of potential plant molluscicides. BANK/WHO Special Programme for Diseases (in press).

and design of laboratory evaluation In: Plant Molluscicides. UNDP/ WORLD Research and Training in Tropical

ECKBLAD, J.W. Experimental predation studies of malacophagous larvae of Sepedon fuscipennis (Diptera: Sciomyzidae) and aquatic snails . Exp . Parasitol. , E: 331-342 (1973).

EISENBERG, R.M. The regulation of density in a natural population of the pond snail, Lymnaea elodes. Ecology, 47: 889-906 (1966).

FERGUSON, F.F. The Role of Biological Agents in the Control of SchistosomeBearing Snails. U.S. Dept. of Health, Education and Welfare/Public Health Service (Atlanta, GA, USA : CDC/Bureau of Laboratories), 1978, 107 pp.

FERGUSON, F.F. & BUTLER, J.M., Jr. Ecology of Marisa and its potential as an agent for elimination of aquatic weeds in Puerto Rico. Proc. Southern Weed Conf., ~: 468-476 (1966).

FERGUSON, F.F., OLIVER-GONZALEZ, J . & PALMER, J.R. Potential for biological control of Australorbis glabratus, the intermediate host of Puerto Rican schistosomiasis . Amer. J . Trop. Med. Hyg., I: 491-493 (1958).

FERGUSON, F.F. & RUIZ-TIBEN, E. Review of biol ogical control methods for schistosome-bearing snails. Ethiop. Med. J., ~: 95-104 ( 197 1).

FLETCHER, M. & WOODRUFF, D.S. Towards the bio l ogical control of schistosomiasis: A mathemat ica l model of the effects of genetic manipulation of in termediate host snail populations . Unpublished manuscript for a workshop on mathematical modelling of schistos~miasis. Rockefe l ler Foundation/Edna McConnell Clark Foundation, Bellagio, 1976, 13 pp.

FRANDSEN, F. & MADSEN, H. A review of Helisoma duryi in biological control. Acta Trop., ~: 67- 84 (1979).

GREATHEAD, D.J. Arthropod natural enemies of bilharzia snails and the possibilities for biological control. Biocontrol News I nform. I: 197-202 (1980).


GREATHEAD, D.J. & WAAGE, J.K. Opportunities for biological control of agricultural pests in developing countries. World Technical No. ~. 1983, 44 pp.

GRIST, D.H. 4th ed. London: Longmans, 1968, 321 pp.

GUYARD, A., POINTIER, J.P. & THERON, A. The decline of Schistosoma mansoni in Martinique (French West Indies). Role of the competitive displacement of the snail host Biomphalaria glabrata by!· raminea 8th Int. Congr. Halacol., Budapest, August 1983, p. 39 (abstract .

GUYARD, A., POINTIER, J.P., THERON, A. & GILLIES, A. Mollusques hotes intermediaires de la schistosomose intestinale dans les Petites Antilles: Hypotheses sur le role de Biomphalaria glabrata et !· straminea en Martinique. Malacologia, 22 103-107 (1982).

HAIRSTON, N.G. Population ecology and epidemiology problems. Symp. Bilharziasis. (M. O'Connor and G. Wolstenholm, Churchill, 1962, pp. 36-62.

In: CIBA Found. eds.) London:

HAIRSTON, N.G. On the mathematical analysis of schistosome populations. Bull. Wld. Hlth. Org., ~: 45-62 (1965).

HAIRSTON, N.G. The dynamics of transmission. of Schistosomiasis (Bilharziasis). (N. 1973, pp. 250-336.

In: Epidemiology and Control Ansari, ed.) Basel: S. Karger,

HAIRSTON, N.G., ALLAN, J.D., COLWELL, R.K., FUTUYUHA, D.J., HOWELL, J., LUBIN, M.D., MATHIAS, J. & VANDERMEER, J.H. The relationship between species diversity and stability: An experimental approach with protozoa and bacteria. Ecology, 49: 1091-1101 (1968).

HAIRSTON, N.G. & SANTOS, B.C. Ecological control of the snail host of Schistosoma japonicum in the Philippines. Bull. Wld. Hlth. Org., 25: 603-610 (1961).

HAIRSTON, N.G., TINKLE, D.W. & WILBUR, H.M. Natural selection and the parameters of population growth. J. Wldl. Man., 34: 681-690 (1970).

HAIRSTON, N.G., WURZINGER, K.-H. & BURCH, J.B. Non-chemical methods of snail control. Document WHO/VBC/75.573, Geneva (1975).

HASSELL, M.P. The Dynamics of Arthropod Predator-Prey Systems. Princeton: Princeton University Press, 1978, 237 pp.

HASSELL, M.P. Arthropod predator-prey systems. In: Theoretical Ecology. (R.M. May, ed.) Oxford: Blackwell Scientific, 1981, pp. 105-131.

HUBENDICK, B. A possible method of schistosome vector control between resistant and susceptible strains. BulL Wld. 1113-1116 (1958).

competition Hlth Org., 18:

HUFFAKER, C.B. Fundamentals of biological control of weeds. Hilgardia, 27: 101-157 (1957).

HUFFAKER, C.B. Experimental studies on predation: Dispersion factors and predator-prey oscillations. 27· 343-383 (1958).

FFAKER, Pests

HUFFAKER, .B. & lnsec t Pest

HUFFAKER, C.B. Control.

HUIZINGA, H.W. iu the (1973).

t Proc. Study

. R. 9

In: York:

TDR/RCV-SCH/SIH/84.3 ANNEX IV page 3 5

in natur Dynam .

eds. p.

In:

Insect

is and larval trematode antagonism Parasitol., 33: 350-364

28: 142-154

JOBIN, W.R. & BERRIOS-DURAN, L.A. Cost of harvesting and spreading Harisa cornuarietis for biological control of Biomphalaria gl-:ibr;t;i in Aibonito, Puerto Rico. Bull. Wld Hlth . , 42: 177-179 (1970).

JOBIN, W.R., BROWN, R.A., BELEZ, S.P. & FERGUSON, F.F. Biological control of Biomphalaria glabcata in major reservoirs of Puerto Rico. Amer. J He d. Hyg., ~:iol8-1024 (1977).

JORDAN, P., BARTHOLOHEW, R.K., GRIST, E. & AUGUSTE, E. Evaluation of chemotherapy in the control of Schistosoma mansoni in Valley, Saint Lucia. I. Results in humans. ._Am_e~r_. ___ J_. __ _._ ___ _;__"-"'-., 31: 103-llO (1982).

JORDAN, P., CHRISTIE, J.D. & UNRAU, G.O. Schistosomiasis transmission with particular reference to possible ecological and biological methods of control. A review. Acta Trop., ~: 95-135 (1980).

KM1EL, E.G. Studies on the Biolo_gy and Biological Control of SchistosomeCarrying Snails in Egypt. N.S. Thesis, Ain Shams University, Cairo, 1973' 260 pp.

KNUTSON, L.V. Sciomyzid flies. Another approach to bio ical control of snail-borne diseases. Insect Wld. t : 13-18 (1976).

KNUTSON, L.V. & BERG, C.O. and immature stages of ma Diptera of the genus Knutsonla Verbecke. Bull. lnst.

------·---~---------~------------Nat

43: (1967).

tribution and Abundance.

KUlUS


LIE, K.J.

LIE, K.J., SCHNEIDER, C.R., SORNMANI, S., LANZA, G.R. & IMPAND, P. Biological control by trematode antagonism. I. A successful field trial to

Schis spindale in Northeast Thailand. S.E Asian J. 46-59 (l974a).

LIE, K.J., SCHNEIDER, C.R., SORNMANI, S., LANZA, G.R. & IMPAND, P. Biological control by trematode antagonism. II. Failure to control spindale in a field trial in Northeast Thailand. S.E

~~--~--~----~ Med. Publ. Hlth., z: 60-64 (1974b).

LIM, H.K. & HEYNEMAN, D. Intramolluscan inter-trematode antagonism: A review of factors influencing the host-parasite system and its possible role in biological control. Advances in Parasitology, 10 191-268 (1972).

LOKER, E.S., MOYO, H.G. & GARDNER, S.L. in non-lacustrine habitats in Parasitology, ~: 381-399 (1981).

Trematode-gastropod associations the Mwanza region of Tanzania.

LOTKA, A.J. Elements of Physical Biology (1925). Reprinted as: Elements of Mathematical Biology. New York: Dover, 1956, 465 pp.

LUNDHOLM, B. & STACKERUD, M. (eds.) Environmental protection and biological forms of control of pest organisms. Ecol. Bull., No. ll= 1979, 171 pp.

MADSEN, H. Distribution of Helisoma duryi, an introduced competitor of intermediate hosts of schistosomiasis, in an irrigation scheme in Northern Tanzania. Acta Trap., 40: 297-306 (1983).

MALEK, E.A. Snail Transmitted Diseases. Boca Raton, FL, USA: CRC Press, 1980.

MALEK, E.A. & CHENG, T.C. Medical and Economic Malacology. London: Academic Press, 1974, 398 pp.

MALEK, E.A. & MALEK, R.R. Potential biological control of schistosomiasis intermediate hosts by helisome snails. Nautilus, ~(1): 15-18 1978).

MANDAHL-BARTH, G. A possible biological method of controlling bilharzia snails. Unpublished manuscript of a lecture delivered to Ain Shams University, Cairo, 1965, 9 pp.

MANGUIN, S. Donnees sur l'ecologie et la predation de Tetanocera ferruginea Fallen, 1820 (Diptera: Sciomyzidae). Memoire, D.E.A. Parasitologie, Universite des Sciences et Techniques du Languedoc, Mont lier, 1983, 27 pp.

MAY, R. M. Stability and Complexity in Model Ecosystems. Princeton: Princeton University Press, 1973, 235 pp.

MAY, R.M. & ANDERSON, R.M. Regulation and stability of host-parasite population interactions. I. Destabilizing Processes. J. Anim. EcoL 47 249-267 (1978).

MAY, ANDERSON 269

. II.


McCOY , L. E. & JOY, J.E. Tolerance of Sepedon f uscipennis and Dictya sp . larvae (Dip tera : Sciomyzidae) to the molluscic ides Bayer-70 and sod ium pent ach lorophenate . Environ . Entomol., ~: 198-202 (1977).

McCULLOUGH, F. S. Biological control of the snail intermediate hosts of human Schi stosoma s p. : A r eview of its present status and future pr ospects. Acta Trop., 38: 5-13 (l98la).

Mc CULLOUGH , F. S. Cont rol of snail i ntermediate hos ts of Schistosoma spp. by fish. WHO Document TDR/BCV/IC.81.2 , l 98 l b, 4 pp.

McCULLOUGH, F. S. & MALEK, E.A. Notes on t he molluscan hosts of Paragonimus spp. and their possible r o le in biological control. Ann . Trop. Med . Par asito l . , ~: 339-340 (1984 ) .

McCULLOUGH, F.S. & HOTT, K.E. The rol e of mollusc i cides in schis tosomiasis control. WHO Document WHO/VBC/83 . 87 9, 1983.

McJUNKIN , F.E. Engineering met hods for control of schistosomiasis. A r eport fo r the Office of Health, Agency for International Development, Wash i ngton , DC, USA. Cont ract No. AID/csd.2487 , 1970, 69 pp .

McMAHON , J.P . , HIGHTON, R.B . & MARSHALL, R.F. De C. Studies on cont r ol of intermedia t e hosts of schi stosomiasis in Envi ron . Cons., ~; 285-289 ( 1977 ) .

t he biol ogical Wes t ern Kenya.

McMULLEN , 0.8. Biologica l and envi ronmental control of snails. In: Epidemiology and Control of Schistosomiasis. (N. Ansari, ed. ) Basel: Karger , and Ba l timore: University Park Pr ess , 1973 , pp. 533- 591.

MEAD, A.R. The Giant Af r ican Snai l: A Problem i n Economic Malacology. Ch i cago : University of Chicago Pr ess, 1961, 25 7 pp.

MEFIT-BABTIE, R.L. Range ecology , livestock i nvestigat ions and water suppl y. 2nd Interim Report to t he National Council fo r the Development of the Jonglei Cana l , Sudan, 1981 , pp. 29- 35 .

MEYNADIER, G. Eta t actuel des connaissances sur la patho logie des gas t eropodes . Halioti s , ~: 255-262 (1977 ) .

MEYNADIER, G., BERGOIN, M. & VAGO , C. Bacter iose epizootique chez les Helicides (mollusques) . An toni van Leewenhoek , 30: 76-80 ( 1964).

MICHELSON, E.H. Studies on the biological control of schistosome-bea r ing snails. Predators and par asites of freshwater Mollusca: A review o f the l i tera t ure. Parasitology, ~: 413-426 (1957) .

MICHELSON, E.H. Plistophora husseyi s p .n. , a microsporidian par asite of aquat i c pulmonate s nails. J . Insect Patho1., 1= 28- 38 (1963).

MICHELSON , E.H. An ac id-fast pat hogen of fr eshwater snails. Amer. J . Trop. Med. Hyg., 10: 423-427 (1961).

MICHELSON, E.H. & DUBOIS, l . Lymnaea emargi nat a , a possible agen t f or the control of the schistosome-s na il hos t, Biomphalaria glabrata . Naut i l i s , 88 : 101- 108 (1974) .

MICHELSON, E.H. & DUBOIS, L. Compe t i t ive interaction between two snail hosts of Sch i stosoma rnans oni: Laboratory studies on Biorophalaria glabrata and B. st raminea. Rev . Ins t. Med. Tro p. Sao Paulo , 21: 246- 253 (1979) .


MICHELSON, E.H. & DUBOIS, susceptibility of

possibly associated with populations to Schistosoma

mansoni.

MILWARD-DE-ANDRADE, R. Competi9ao entre Helisoma duryi (Wetherby, 1879) e -;-;:_:_:.;:.<:..:C.::.::.:=-=.=-=.i=-a glabrata (Say, em condi9oes de laboratorio

Planorbidae). Rev. Brasil. Bioi., 38(4): 787-800 (1978).

MINCHELLA, D.J. & LOVERDE, P.T. Laboratory comparison of the relative successes of Biomphalaria glabrata stocks which are susceptible insusceptible to infection with Schistosoma mansonL Parasitology, 335-344 (1983).

MOUGEOT, G., GOLVAN, T.J. & DEPERNET, D. Interaction nematode-trematode

and 86:

chez Biomphalaria glabrata, vecteur de la bilharziose humaine a Schistosoma aux Antilles et en Amerique du Sud. Bull. Soc. Sc. Veter. Med. ~: 152-156 (1977).

MSANGI, S.A. & KIHAULE, P.M. Prospects of biological control of schistosomiasis in East Africa. In: Parasitoses of Man and Animals in Africa. (C. Anderson and W.L. Kilama, eds.) Nairobi: East African Literature Bureau, 1972, pp. 439-447.

MUNARI, L. Lo studio degli Sciomyzidae (Diptera: biologica ai molluschi vettori degli eziologici delle bilharziosi e distomatosi Soc. Ven. Sci. Nat., ~: 9-30 (1983).

Cyclorrapha) per la latta eliminti parassiti, agenti umane e del bestiame. Lav.

NASIR, P. Freshwater larval trematodes. biological control of Schistosoma 255-260 (1981).

XXVIII. Some observations on mansoni. Riv. Parassit., ~(2):

NASIR, P., HAMANA, L.J. & DIAS, M.T. Studies on freshwater larval trematodes, XXIII. Additional five new species of Venezuelan cercariae. J. Helminth. Soc. Wash.,~: 231-239 (1969).

NASSI, H., POINTIER, J.P. & GOLVAN, Y.J. Bilan d'un essai de controle de Biomphalaria glabrata en Guadeloupe a l'aide d'un trematode sterilisant. Ann. Parasitol. Hum. Camp.,~: 185-192 (1979).

NGUMA, J.F.M., McCULLOUGH, F.S. & MASHA, E. Elimination of Biomphalaria pfeifferi, Bulinus tropicus and Lymnaea natalensis by an ampularid snail, Marisa cornuarietis, in a man-made dam in northern Tanzania. Acta Trap.,~: 85-90 (1982).

ODEI, M.A. Prospects for the microbial control of molluscs. Proc. Third Inter. Colloq. Invert. Pathol. Microbial Control. University of Sussex, Brighton, 5-10 Sept. 1982, pp. 400-402.

OLIVER-GONZALEZ, J., BAUMAN, P.M. & BENENSON, A.S. Effect of the snail Marisa cornuarietis on Australorbis glabratus in natural bodies of water in Puerto Rico. Amer. J. Trap. Med. Hyg., ~: 290-296 (1956).

ORTIZ-TORRES, E. Damage caused by the snail Marisa cornuarietis, to young rice seedlings in Puerto Rico. _J_. ___ A~g~r_i_c_. ___ U_n_1_·v __ . ___ P_u_e_r_t_o ___ R_1_·c_o~, ___ R_i_o Piedras, 46: 241 (1962).

PAt~, C. A

Parasitol

TDR/BCV-SCH/SIH/84.3 ANNEX I V page 39

PAPAVIZAS, G.C . {ed.) Biological Control in Crop Production. Totowa, NJ, USA: Allanheld, Osmun and Co., 1981, 461 pp.

PAULINYI, H.M. & PAULIN!, E. Laboratory observations on the biological control of Biomphalaria glabrata by a species of Pomacea (Ampullaridae). Bull. Wld . Hlth. Org . , 46: 243-247 (1972).

PFLUGER, W. Introduction of Biomphalaria glabrata to Egypt and other African countries. Trans. Roy. Soc. Trop. Med. Hyg . , !..!!_: 567 (1982).

PIANKA, E.R. Competition and niche theory. In: Theoretical Ecology . (R.M. May, ed.) Oxford: Blackwell Scientific, 1981, pp. 167-196 .

POINTIER, J.P. La lutte biologique contre les mollusques hotes intermediares des bilharzioses a l'aide de mollusques compthiteur s. Symbioses, .!:2(2): 85-91 (1983).

POINTIER, J.P., THERON , A. & IMBERT- ESTABLET , D. Competitive displacement of Biomphalaria glabrata by Ampullaria glauca in a pool in Guadeloupe (French West Indies) and consequences upon the life cycle of Schistosoma mansoni. 8th lnt. Congr . Halacol., Budapest, August 1983, p. 112 (abstract).

PRENTICE, M.A. Schistosomiasis and its intermediate hosts in the Lesser Antillean Islands of the Ca r ibbean. Bull. PAHO , 14: 258-268 (1980) .

PRENTICE , M.A. Displacement of Biomphalaria glabrata by the snai l Thiara granifera in field habitats in St. Lucia, West Indies. Ann. Trop. Med. Parasitol., Zl: 51-59 (1983) .

PRENTICE , M.A . A field evolved differ ential filtration method for r ecovery of schistosome cercariae. Ann. Trop. Med. Parasitol ., ~: 117-127 (1984).

PRENTICE, M.A., BARNISH, G. & CHRISTIE, J.D. An ecophenotype of Helisoma duryi closely resembling Biomphalaria glabrata. Ann . Trop. Med. Parasitol., Z!: 237-238 (1977) .

PRENTICE , M.A. CHRISTIE, J.D. & BARNISH, G. A miracidium trap for use in flowing water. Ann. Trop. Med . Parasitol., 21: 407-414 (1981).

PRENTICE, M.A. & OUMA, J.H. Field comparison of mouse immersion and cercariometry for assessing the transmission potential of water containing cercariae of Schistosoma mansoni. Ann. Trop. Med. Parasitol., ~: 169-1 72 (1984).

RICHARDS, C.S. Genetics of a molluscan vector of schistosomiasis . Nature 227: 806-810 (1970).

RICHARDS, C.S. Susceptibility of adult Siomphalar ia glabrata to Schistosoma manson! infection. Amer. J. Trop. Hed . Hyg., ~: 748-756 ( 1973).

RICHARDS, C.S. & MERRITT, J.W., Jr . Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection. Amer. J. Trop. Med. Hyg., 21 : 425-434 (1972) .

RIDGWAY, R.L. & VINSON, S.B. Biological Control by Augmentat:i.on of Natural Enemies. New York: Plenum Press, 1977, 480 pp.


RONDELAUD, D. Resultats et zonitidae dans Haute-Vienne.

RONDELAUD, D. Les effets a Etude le de de

par 'introduction de limnees t

53 (197

d'un controle bi des populations de

53; 215-222 (1978).

e

ROUNDS, M.C. Check list of the helminth parasites of African mallli11als of the orders Carnivora, Tubulidentata, Proboscidea, Hyuracoidea, Artiodactyla and Perissodactyla. , Vol. 38, St. Albans: Commonwealth

RUIZ-TIBEN, E., PALMER, J.R. & FERGUSON, F.F. Biological control of Biomphalaria glabrata by cornuarietis in irrigation ponds in Puerto Rico. Bull. Wid. , 41: 329-333 (1969).

SLOBODKIN, L.B. Growth and Regulation of Animal Populations. New York: Holt, Rinehart and Winston, 1961, 184 pp.

SMITH, E.H. & PIMENTAL, D. (eds.) Pest Control St Press, 1978.

es. New York: Academic

SMITH, J.M. Models in Ecology. Cambridge: Cambridge University Press, 1974, 146 pp.

SOHN, I.G. & KORNICKER, L.S. Ostracoda (Crustacea).

Predation of schistosomiasis vector snails by Science, 175: 1258-1259 (1972).

SOUTHWOOD, T.R.E. Bionomic strategies and population parameters. In: Theoretical Ecology. (R.M. May, ed.) Oxford: Blackwell Scientific, 1981, pp. 30-52.

STURROCK, R.F. Ecological notes on habitats of the freshwater snail Biomphalaria glabrata, intermediate host of Schistosoma rnansoni on St. Lucia, West Indies. Caribb. J. Sci., 14: 149-161 (1974).

STURROCK, R.F. & DUNCAN, J. Methodology and design of field evaluation of plant molluscicides. In: Plant Molluscicides. UNDP/WORLD BANK/WHO Special Programme for Research and Training in Tropical Diseases (in press).

THOMAS, J.D. Schistosomiasis and the control of molluscan hosts of human schistosomiasis with particular reference to possible self-regulatory mechanisms. In: Advances in Parasitology. Vol. 11. (B. Dawes, ed.) London-New York: Academic Press, 1973, pp. 307-394.

TRIPP, M.R. Is Bacillus pinottii pathogenic in Australorbis abratus? J. Parasitol., 464 (1961)

TUCKER-ABBOTT, R. A study of an intermediate snail host (Thiara granifera) of the oriental lung fluke (Paragonimus). Proc. U.S. Nat. Hus. Wash., 102: 71-116 (1952).

VAN DEN BOSCH, R., MESSENGER, P.S. & GUTIERREZ, A.P. An Introduction To Bi Control. New York Plenum Press,

resser im Ni


isch-taxonomische untersuchungen uber (Trematoda, Troglotrematidae) sowie

und die verbrei tung der parasi ten iiber

in Liberia. ' 24: 4-20 (1973).

WAAGE, J.K. & HASSELL, I:>!.P. fundamental approach.

Parasitoids as biological control agents - a 84: 241-268 (1982).

WHO. Schistosomiasis control. ' 515

WHO. ogy and control of schistosomiasis. 980).

Geneva (1973).

643:

WHO. Data sheet on the biological control agent Thiara granifera (Lamarck). Document WHO/VBC/81.833, Geneva (1981).

WHO. Biological control of vectors of disease. Tech. Rep. Ser., 679: Geneva (1982a).

WHO. Data sheet on the biological control agent Marisa cornuarietis. (Linn.). Document WHO/VBC/82.837, Geneva (1982b).

WHO. Guide to field determination of major groups of pathogens affecting arthropod vectors of human disease. Document WHO/VBC/82.860, Geneva (1982c).

WHO. The role of biological agents in integrated vector control and the formulation of protocols for field testing of biological agents. Document TDR/VEC-SWG(6)/82.3, Geneva (1982d).

WHO. A strategy of morbidity reduction in schistosomiasis. Document WHO/SCHIST0/83.68, Geneva (1983a).

WHO. Integrated vector control. Tech. Rep. Ser., 688: Geneva (1983b).

WILLOMITZER, J. & ROZNOSNY, K. Further observations on the rearing of sciomyzid larvae (Diptera) for the control of intermediate host snails. Acta. Vet. Brno., ~: 315-322 (1977).

WRIGHT, C.A. Some views on biocontrol of trematode diseases. Trans. Roy. Soc. Trop. Med. Hyg., _§2: 320-329 (1968).

WRIGHT, C.A., ROLLINSON, D. & GOLL, O.H. Parasites of Bulinus senegalensis (Mollusca: Planorbiae) and their detection. Parasitology, 79: 95-105 (1979).

YEO, R.R. & FISHER, .W. Progress and potential for biological weed control with fish, pathogens, competitive plants and snails. Background paper for First FAO International Conference on Weed Control, Davis, California, 1970, 15 pp.

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