Indirect and Non-Target Effects of Biological Control

Recently, the potential for negative, indirect, environmental effects of biological control has received increasing attention in the scientific and popular press. In response to this, the International Organization for Biological Control (IOBC) convened an international symposium on `Evaluating indirect ecological effects of biological control' in Montpellier, France on 17-20 October 1999. The aim of this meeting was first, to summarize what is known about indirect and non-target effects of biological control agents, and second, to identify the key research questions and appropriate methodologies to increase the safety and predictability of biological control. The symposium comprised over 70 presentations (either oral or poster) together with two workshop sessions in which the participants broke up into 12 working groups before reporting back for discussion and recommendations.

In opening the meeting, Jeff Waage (CABI Bioscience and President of IOBC) listed three factors that have led to the recent debate about biological control: increased numbers of stake holders, increased interest in conservation and biodiversity, and increased commercial biological control, particularly in greenhouse production. The effect is that the public is now more aware that biological control programmes can involve effects both on the target pest and on non-target organisms such as closely related plants or prey species. Three cited examples of indirect (non-target) effects of introduced biological control agents were: (i) the attack of rare, native species of cacti in the southeastern USA by one of biocontrol's `citation classics', Cactoblastis, which spread accidentally from the Caribbean (Don Strong, University of California, Davis and Bob Pemberton, US Department of Agriculture - Agricultural Research Service (USDA-ARS), Ft. Lauderdale, Florida); (ii) the impacts of the seed feeding weevil, Rhinocyllus conicus, originally introduced to North America to control nodding thistle, but now reducing seed production of several native thistles and influencing a native picture winged fly that feeds on the thistle seeds (Svata Louda and Amy Arnett, University of Nebraska, USA); and (iii) the decline of Aphidoletes aphidimyza, an important, early season dipteran predator of aphids in apple orchards in the eastern USA following the introduction of the Asian ladybird, Harmonia axyridis, (Mark Brown, USDA, Kearneysville, West Virginia).

Moving on from the fact that important indirect and nontarget effects can and do exist, Mark Lonsdale, David Briese and Jim Cullen (Commonwealth Scientific and Industrial Research Organisation (CSIRO), Canberra, Australia) pointed out that risk assessment must involve both determining the potential hazards or unwanted events, and the probability of the hazards occurring. They stressed that for appropriate evaluation, benefit assessment must accompany risk assessment; while an introduced control agent may attack a native species, the impact of the target pest on other native species such as rare species living in the same environment must also be evaluated. Don Strong, among other speakers, pointed out that for many introduced pests, biological control is the only feasible solution. Peter Neuenschwander (International Institute of Tropical Agriculture (IITA), Cotonou, Benin) and Richard Markham (IITA, Ibadan, Nigeria) reinforced this message and highlighted the serious consequences of imposing too many restrictions on and over regulating biocontrol. But Strong and Pemberton also cited the apparent lack of restraint in recent biological control programmes as demonstrated by the introduction of 31 species of natural enemies between 1986 and 1993 in the Russian wheat aphid control programme in North America. Given that with each biological control agent comes the possibility of non-target impacts, what emerged from this was that a better understanding of the characteristics of successful agents is a necessary prerequisite to reducing the number of unsuccessful species that are introduced.

In terms of other practical considerations, determining host specificity was the most widely mentioned approach to avoiding non-target effects. Various reports showed how host specificity testing has been widely used in the biological control of weeds but much less so for biological control of insects. Phylogenetic, trophic, geographical, habitat, climatic and phenological similarities were suggested as characteristics to be considered in host range testing. What also emerged was that interpreting host range is difficult because the physiological host range demonstrated in the laboratory is not necessarily the same as the ecological host range observed in the field. This is particularly a problem for pathogens (Mark Goettel, Agriculture Canada, Lethbridge, Alberta and Ann Hajek University of Cornell, USA). To test the effectiveness of protocols for predicting the host range of parasitoids, Elizabeth De Nardo (Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA), Jaguariúna, Brazil) and Keith Hopper (USDA-ARS, Newark, Delaware) used a retrospective case study of parasitoids introduced for corn borer control. This work is still in progress but was an innovative approach to a very difficult problem of designing appropriate and safe protocols for biological control.

As an additional dimension to this, the risk of evolutionary host range expansion is always of concern in biological control programmes. However, Rieks Van Klinken (CSIRO, Indooroopilly, Australia) found no evidence of such shifts having occurred thus far, but suggested that increased use of a host that was in the fundamental host range of a species was possible as density of the target host changed. Similarly, Bob Pemberton (USDA-ARS, Ft. Lauderdale, Florida) showed, through an analysis of weed control projects in the USA, the Caribbean and Hawaii, that risks of non-target attacks are not associated with host changes but with the existence of native relatives and target plants in the same locations. Michael Hochberg (Université Paris VI, France) addressed this issue from a theoretical perspective using insect parasitoids as his model system. He concurred that there was no evidence for host range evolution, and proposed that this related to a range of genetic barriers to parasitoid adaptation as well as weak selection pressure on the parasitoids to adapt.

Beyond this, as a general observation, few studies attempted to link empirical investigations with theoretical models. Two notable exceptions were presentations from Bob Holt (University of Kansas, USA) and Liam Lynch and colleagues (the latter working as part of the ERBIC project, which comprises a consortium of European Union partners looking at evaluating risks of biocontrol introductions, led by Heikki Hokkanen from the University of Helsinki, Finland). Both these studies identified the need to investigate transient population dynamic effects, in addition to the traditional equilibrium states of agent-host interactions. This work showed that in the short term, overflow of the control agent is likely if the carrying capacity of the target population is high, possibly resulting in local extinction. Thus absolute, rather than relative, attack rates on different host species are important, underlining the need for no choice in addition to choice experiments in host range studies.

By way of closing, there was clear agreement that biological control is, and can remain, an effective tool for combating agricultural, environmental and green house pests. There was also a consensus across a very international and diverse group of scientists that techniques are available for improving the safety and effectiveness of biological control. Host range testing, pre-release experimentation in the native habitat, and post-release monitoring for direct and indirect impacts were emphasized as being necessary for future programmes. Additionally, in order for the pros and cons to be considered more fully, the public needs to be better educated and more involved in the decision making process; a challenge to which biocontrol practitioners must themselves rise. However, in order for real progress to be made, funding agencies must recognize that biological control is a discipline built on solid ecological principles, and that safe and effective biological control requires more than just collecting agents from one area, releasing them in another and then hoping things will work out for the best.

By: Matt Thomas1, Jenny Cory2, Judy Myers3 and Liam Lynch1

1Leverhulme Unit for Population Biology and Biological Control, NERC Centre for Population Biology and CABI Bioscience, Silwood Park, Ascot, SL5 7TA, UK
Email: m.thomas@cabi.org
Fax: +44 1491 829123
2Ecology and Biocontrol Section,
NERC Institute of Virology and
Environmental Microbiology, Oxford, UK
3Department of Zoology and Faculty of Agricultural Sciences,
University of British Columbia,
Vancouver, Canada

Organic Banana Workshop

Many small-scale banana farmers who are facing increasing difficulty in competing in a free market economy desperately need production and diversification alternatives. One possibility, the organic production of bananas, has attracted considerable interest in both producer and consumer countries. As a result, INIBAP (International Network for the Improvement of Banana and Plantain), CAB International, and CTA (the Technical Centre for Agricultural and Rural Cooperation, Netherlands) jointly organized an international workshop on the production and marketing of organic bananas produced by smallholder farmers, and this was held in the Dominican Republic on 31 October - 4 November 1999 by kind invitation of the Executive Director, Centro Para el Desarrollo Agropecuario y Forestal, Inc. (CEDAF).

The workshop had a specific focus on production and marketing requirements and constraints for organic bananas produced by small-scale farmers in the Caribbean region. Key players in the farmer-to-table chain were participants, and these included representatives of farmers and producers (mainly from the Caribbean and Latin America regions, but also from Africa), European and North American organic certification organizations, importers and retailers. Other participants included representatives of governments, donor agencies and a number of regional and international bodies.

The main aim of the meeting was to provide an impartial forum for discussion and information exchange, with the objective of establishing a nucleus to take organic banana initiatives further. It was recognized at the outset that organic banana production would not provide a solution to all the problems facing the banana industry in the Caribbean, but that it does have the potential to provide a stable source of income for some smallholder producers, and a continuous, guaranteed supply of organic bananas is required for the market.

The meeting consisted largely of working group meetings, with discussions focusing on five major issues, and these are summarized below.

Technical Constraints to Production

Black Sigatoka and lack of soil fertility are the key production constraints. Site selection is crucial in any organic initiative and it was recommended that organic production should be based on an entire watershed with a sufficiently large area. This requires a co-ordinated approach and a critical mass of farmers. A systems-based approach to production was also recommended with participatory research methodologies used to address the key constraints. It is extremely difficult to produce Cavendish varieties organically where there is a heavy presence of black Sigatoka. However, other varieties with potential for organic production are available, either as Cavendish replacements or as speciality bananas for niche markets.

Main research needs were identified as:

• Guidelines for site selection
• Strategies for black Sigatoka management - including biocontrol; methods to reduce impact such as replanting, shade/mixed cropping; organic spray applications
• Integrated pest management
• Banana breeding, focusing on resistance to black Sigatoka and nematodes and dwarfness
• Field selection and evaluation of varieties
• Delivery mechanisms for beneficial micro-organisms such as mycorrhizae
• Post-harvest research on crown rot and latex stain and the post-harvest handling of new varieties
• Improvement of soil fertility

It was recommended that demonstration farms be set up to facilitate the training of farmers in the application of new technology packages. In addition the need for information sharing, creation of linkages and exchange of experiences was highlighted.

Mechanisms to Support Conversion

For individual smallholders, the financial and human time and resources investment necessary for conversion to organic production may be difficult without some external support. There is an urgent need for training and information for farmers who are considering converting to organic production. It was recommended that `leader farmers' should be specifically targeted for training, not only in technical issues, but also in record keeping and skills associated with team building and negotiating. Farmer groups or co-operatives provide the ideal fora for discussion and provide the framework through which support services can be provided.

Some possibilities for financial support during conversion exist within the framework of linkages with `Fair Trade' or `Pesticide-free' labels. An enabling environment, in terms of local institutional support for organic farmers and a favourable policy framework, is also essential in encouraging farmers to convert. In the longer term, public awareness and education at all levels will be a major element in maintaining organic production and reducing the risks of `contamination' from outside sources and abuse of organic systems.

Specific research needs were identified as:

• Socio-economic/technical aspects of conversion in tropical agroecosystems to identify locally appropriate approaches
• Local adaptation of participatory research and training techniques, such as farmer field schools
• Market research for diversification systems to help plan diversification associated with conversion
• Potential impacts of organic farming on the national scale to help support investments.

Certification

The certification of organic production is an extremely important issue for small holder producers. At the present time most certification is carried out by international certifiers using national inspectors. This process is costly, and there is a need to develop the capacity for certification at the national level. The advantages of carrying out certification nationally include the reduced administrative and management costs and the greater understanding that would develop between producers and certifiers. However, national certification has to overcome problems of credibility on the side of the importer, increased possibilities for conflicts of interest, financial limitations, the need for accreditation and the lack of human resources.

The market benefits of linking organic and fair trade certification are clear, even though fair trade does not embrace all the standards of organic products. It would be particularly desirable to have the same certifiers for both fair trade and organic certification.

The appropriateness of standards developed for European agriculture being imposed on tropical production systems was also discussed, and it was recommended that producer representatives from tropical countries should be involved in this process. Issues such as the initial cost and ownership of certification must also be addressed. These issues are common for all organic production, not just bananas.

Marketing

There is currently some confusion regarding the market for organic bananas. From the demand side, it is felt that organic bananas are presently far from meeting the market potential, whereas on the production side there is a conception that organic bananas cannot be sold. Members of this working group agreed to form a task force to collect relevant information and to assess the real demand and supply situation. More solid price information is also needed, and realistic price premiums need to be worked out for organic bananas by country. There is a clear need for transparency in such information and the establishment of a global monitoring system was recommended.

There is a market for different types of bananas, so long as they meet basic criteria with respect to appearance, taste, shelf-life and ripening characteristics. The market for organic bananas is no longer considered to be a niche market but, rather, a mainstream market with similar quality demands. One important aspect is the need to create consumer-producer solidarity, through which consumers can be educated to understand the limitations and constraints of producers. Products with both fair trade and organic labels stand the best chance of market entry. It was recommended that fair trade organizations be engaged to create more general access for smallholders, including organic growers. Consistency of supply is key. Present experience indicates that the minimum block size to produce homogenous container loads is 25-30 ha.

Total Quality Assurance and Exporting

The goal of total quality assurance was defined as the development of a well-flavoured banana, without progressive defects and with attractive appearance to consumers, wherever and whenever they wish to purchase it.

Quality criteria for Cavendish and for other varieties need to be defined according to stakeholders' demands. (Such stakeholders would include consumers, regulatory bodies and distributors/retailers.) It is also necessary to understand how these criteria relate to the quality aspects of the fruit. Research is therefore needed to understand the factors determining quality and to develop guidelines and minimum standards for producers and ripeners.

There is a need to define smallholder production system protocols, which will ensure that a quality product, meeting the identified criteria is achieved. In addition, it was recommended that smallholder audit trails be put in place and an audit trail manual be developed.

Specific areas for research include methods for controlling crown rot in organic systems and for minimizing latex stains on fruit.

Conclusions and Action Needed

The meeting recognized that a growing market for organic bananas does exist, particularly in Europe and North America. In contrast, local markets have a low awareness of organic issues, but have the potential for growth. Organic banana initiatives are in place, particularly in the Dominican Republic, and have been shown to work well with organized groups of small-scale producers. It is clear that organic production methods are more sustainable than traditional methods and could provide an alternative market opportunity for smallholders.

In general the meeting acknowledged the importance of information sharing and dialogue between all the stakeholders, and the desirability of partnerships between the producers and the market. In addition, a co-ordinated approach and collective commitment are essential, particularly in the case of small-scale producers. Other important issues include the need for further research in a number of areas, the need for training of new organic farmers and the need for greater efforts in public awareness, both amongst producers and consumers.

Looking specifically at the Windward Islands, it was noted that there are several factors in favour of organic banana production there. These include the absence of black Sigatoka, the existence of a `banana culture' and farmer associations, the possibility of linking organic production to tourism, especially eco-tourism, the existence of a market demand and the interest of younger farmers. On the down side, adverse factors include the topography of the islands, the large numbers of small-scale farmers, a lack of organic materials for improving soil fertility, the high labour cost, an ageing farming community, problems of land tenure (especially for younger farmers) and lack of technical knowledge.

A number of specific immediate action points were identified during the meeting:

• To carry out, in the short term, feasibility studies with farmers on the socio-economic and agronomic potential for organic banana production in the Windward Islands
• To put in place further variety evaluation trials (these are already planned for FHIA-23 in the Dominican Republic)
• To initiate research on organic banana management systems and particularly the management of black Sigatoka and soil fertility for smallholder organic farms
• Follow-up on standard setting mechanisms (ISO 14000 and 9000, FAO-CODEX, IFOAM)
• The marketing task force established through the meeting to carry out a supply-and-demand study and provide a report by March 2000
• The World Organic Supermarkets Consortium to set up a forum for discussion between producers and retailers
• INIBAP to put in place a website for relevant producer/market information regarding organic banana production
• Interested parties to approach donors/regional organizations for support to move forward on this initiative
• To produce the proceedings of the meeting including a research agenda

Contact: Ulrike Krauss,
CABI-CATIE Project, CATIE,
7170 Turrialba, Costa Rica
Email: ukrauss@catie.ac.cr
Fax +506 556 0606

Cocoa-Coffee Research Meeting

A USDA/CABI/ACRI Collaborative Cocoa-Coffee Research Meeting was held in London in December 1999 under the auspices of ICO/ICCO (the International Coffee Organization/the International Cocoa Organization). The meeting was organized by Julie Flood, Julius Jackson and Iratxe Rodriguez for CABI, Eric Rosenquist (USDA, United States Department of Agriculture) and Carol Knight (ACRI, American Cocoa Research Institute). All three organizations are working together on many common research programme areas pertinent to coffee and cocoa.

During the last two years there have been some considerable developments in the biocontrol of pests and diseases of cocoa and coffee, some of which have attracted significant international donor interest. This conference provided a timely venue for researchers to present scientific papers and hold discussions regarding future research directions and areas of emphasis.

On the first day, Julie Flood chaired a session of six presentations on biocontrol methodology involved in cocoa diseases. The first presentation was by Prakash Hebber (USDA-ARS, Agricultural Research Service) on the biocontrol of cocoa diseases. He described activities to resolve the problems associated with the mass production of biocontrol agents; a major constraint to conducting large scale field trials with biocontrol agents. This was followed by Bob Lumsden (USDA-ARS) who concentrated on the biocontrol of Phytophthora, and described a simple bioassay using cocoa leaf discs or pod discs for screening for biocontrol efficacy. Ulrike Krauss (CABI/CATIE, Centro Agronómico Tropical de Investigación i Educación, Costa Rica) described work on biocontrol of frosty pod disease and concluded that in Costa Rica, Panama and Peru, the most promising approach to disease management appears to be a combination of cultural and biological control; weekly pod removal and applications of mixed mycoparasite inocula. UV tolerant strains that can reduce frosty pod disease in the absence of shade have also been identified. Ulrike's presentation was followed by a paper on research and extension, with particular reference to biocontrol of cocoa in Peru, was given by Enrique Arévalo Gardini (CICAD/ICT, Comisión Interamericana para el Control del Abuso de Drogas/Instituto del Cultivos Tropicales) and Alberto Hart (CICAD/OAS, Organization of American States). This project aims to overcome some phyto-sanitary limitations with an integrated approach to tropical crops which form part of the agricultural production system of the Huallaga Valley in Peru. Harry Evans (CABI) gave an exciting talk on the exploration for potential biocontrol agents of cocoa diseases. He described two distinct strategies in the search for potential biocontrol agents for witches' broom and frosty pod diseases. The classical approach involves exploration of co-evolved mycoparasites in the purported centres of origin of the diseases, namely coastal Ecuador (frosty pod) and Amazonas (witches' broom). An additional strategy involves assessing endophytic fungal isolates from woody tissues of wild Theobroma and Herrania spp. These isolates are being screened in vitro and in vivo (callus system). In the last presentation on cocoa, Smilja Lambert described biocontrol research at the Mars farm at Almirante in Brazil, and in particular described the antagonistic effects of Trichoderma stromatcium. A 99% reduction in basidiocarp production by the witches' broom pathogen and a 31% pod infection were reported in laboratory and small field trials using this antagonist.

After tea, Jeff Waage took over to chair the session, which concentrated on biocontrol methodology associated with insects, and especially with regard to coffee berry borer (CBB) (Hypothenemus hampei). There were four presentations. The first paper was by Don Nordlund (USDA-ARS) on biocontrol of CBB (the major insect pest of coffee) who reported that classical importation has given no satisfactory control to this pest. Thus, there is increasing interest in augmentative biocontrol such as releases of parasitoids or predators as a way of control. However, our inability to rear large number of these agents is impeding our ability to evaluate these agents. Peter Baker (CABI) described the limitations of parasitoids as a control for CBB. Cephalonomia stephanoderis and Prorops nasuta (two bethylid parasitoids) have been introduced to many coffee growing countries in Latin America, but there is considerable evidence that C. stephanoderis is ineffective. The paper argued that research on bethylid wasps should be wound up for the time being and all available resources devoted to Phymastichus coffea. Fernando Vega (USDA-ARS) described the exploration and characterization of natural enemies of CBB. Many fungi are pathogenic to the pest, with Paecilomyces farinosus outperforming all other entomopathogens tested. Phymastichus coffea was again noted as a very useful parasitoid of CBB. In the last presentation, Roy Bateman (CABI) described the application and testing of biopesticides for perennial crops. Experience has shown that consideration of formulation and application together, i.e. the complete `delivery system', is vital. Additionally, testing in the field situation should be done as soon as possible after laboratory screening trials.

If you would like electronic copies of the papers mentioned above, please send an e-mail to coffee-cocoa@cabi.org with `December Conference Paper' as the subject header. We can currently supply versions of the following presentations:

1. Ulrike Krauss: Biological control of moniliasis (Moniliophthora roreri) in cocoa.

2. Alberto Hart & Enrique Arévalo Gardini: Research and extension in tropical crops, with emphasis on biological control of cocoa diseases in Peru.

3. Harry Evans: Exploration for potential biocontrol agents of cocoa diseases.

4. Smilja Lambert: Biocontrol research at Almirante.

5. Don Nordlund: Biological control of coffee berry borer.

6. Peter Baker: Limitations of parasitoids as a control technology in Colombia.

7. Fernando Vega: Exploration and characterization for natural enemies of coffee berry borer.

By: Julie Flood and Julius Jackson,
CABI Bioscience UK Centre (Egham), Bakeham Lane, Egham,
Surrey,
TW20 9TY, UK
Email: coffee-cocoa@cabi.org
Fax: +44 1491 829100