Biological and Environmental Control of Disease Vectors

Biological and Environmental Control of Disease Vectors

Biological and Environmental Control of Disease Vectors

Edited by

M.M. Cameron and L.M. Lorenz

London School of Hygiene & Tropical Medicine, London, UK

CABI is a trading name of CAB International

© CAB International 2013. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners.

A catalogue record for this book is available from the British Library, London, UK.

Library of Congress Cataloging-in-Publication Data

Biological and environmental control of disease vectors / edited by M.M. Cameron & L.M. Lorenz.

p. ; cm.

Includes bibliographical references and index.

ISBN 978-1-84593-986-1 (alk. paper)

I. Cameron, M. M. (Mary M.) II. Lorenz, L. M. (Lena M.)

[DNLM: 1. Insect Vectors. 2. Insect Control--methods. 3. Pest Control, Biological--methods. 4. Tropical Diseases. QX 650]

363.7’8--dc23

2012046420

ISBN: 978 1 84593 986 1

Commissioning editor: Rachel Cutts

Editorial assistant: Alexandra Lainsbury

Production editor: Tracy Head

Typeset by Columns Design XML Ltd, Reading, UK.

Printed and bound in the UK by CPI Group (UK) Ltd, Croydon, CR0 4YY.

Contents

Contributors

Dedication

1 Introduction

Lena M. Lorenz and Mary M. Cameron

2 Control with Arthropods

Annabel F.V. Howard

3 Use of Larvivorous Fish in Biological and Environmental Control of Disease Vectors

Goutam Chandra, Anupam Ghosh, Indranil Bhattacharjee and Susanta K. Ghosh

4 The Use of Plants in Vector Control

Lena M. Lorenz, Marta F. Maia and Sarah J. Moore

5 Control of Disease Vectors using Fungi

Jennifer C. Stevenson, A.F. Harris and B.G.J. Knols

6 Vector Control using Semiochemicals

James G. Logan, John A. Pickett and Mary M. Cameron

7 House Screening

Matthew J. Kirby

8 Sanitation and Vector Control

Jeroen H.J. Ensink, Flemming Konradsen and Sandy Cairncross

9 Water Management for Disease Vector Control

Flemming Konradsen, Wim van der Hoek and Jeroen H.J. Ensink

10 Integrated Vector Management

Mary M. Cameron, Melissa Bell and Annabel F.V. Howard

11 Evidence Required for Adoption of New Vector Control Methods in Public Health

Jo Lines

Index

Contributors

Melissa Bell, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Indranil Bhattacharjee, Department of Zoology, Mosquito and Microbiology Research Units, The University of Burdwan, Golapbag, Burdwan 713104, West Bengal, India

Sandy Cairncross, Environmental Health Group, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Mary M. Cameron, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Goutam Chandra, Department of Zoology, Mosquito and Microbiology Research Units, The University of Burdwan, Golapbag, Burdwan 713104, West Bengal, India

Jeroen H.J. Ensink, Environmental Health Group, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Susanta K. Ghosh, National Institute of Malaria Research (ICMR), Devanahalli, Bangalore, 562110, India

Anupam Gosh, Bankura Christian College, Bankura 722101, West Bengal, India

Angela F. Harris, The Mosquito Research & Control Unit, Cayman Islands Government, 99 Red Gate Road, PO Box 486, Grand Cayman KY1-1106

Annabel F.V. Howard, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Matthew J. Kirby, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK and Vector Control Cluster, Malaria Consortium, Development House, 56–64 Leonard Street, London EC2A 4LT, UK

Bart G.J. Knols, In2Care BV, Costerweg 5, 6702 AA Wageningen, the Netherlands

Flemming Konradsen, Department of International Health, Immunology and Microbiology, University of Copenhagen, Øster Farimagsgade 5, 1014 Copenhagen, Denmark

Jo Lines, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

James G. Logan, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Lena M. Lorenz, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Marta F. Maia, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK and Biomedical and Environmental Group, Ifakara Health Institute, PO Box 74, Bagamoyo, Tanzania

Sarah J. Moore, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK and Biomedical and Environmental Group, Ifakara Health Institute, PO Box 74, Bagamoyo, Tanzania

John A. Pickett, Biological Chemistry and Crop Protection Department, Rothamsted Research, Hertfordshire AL5 2JQ, UK

Jennifer C. Stevenson, Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

Wim van der Hoek, Department of International Health, Immunology and Microbiology, University of Copenhagen, Øster Farimagsgade 5, 1014 Copenhagen, Denmark and Epidemiology and Surveillance Unit, Centre for Infectious Disease Control, National Institute for Public Health and the Environment, PO Box 1, 3720 BA Bilthoven, the Netherlands

Dedication

The authors would like to dedicate this book to three world-leading medical entomologists, formerly employed at The London School of Hygiene & Tropical Medicine, who taught and inspired generations of young scientists to embark on careers in public health and the control of vector-borne diseases. Tragically, all three died prematurely, and within a period of less than 2 years of each other, but their legacy lives on through the network of alumni that have benefited through their teaching.

Professor Chris Curtis started his career in vector control by studying genetic manipulation of tsetse flies, but devoted most of his working life to develop low-cost and appropriate methods of mosquito control to reduce transmission of malaria and lymphatic filariasis. An example of his work, relating specifically to the environmental focus of the current volume, is the use of expanded polystyrene beads to control Culex mosquitoes breeding in pit latrines and soakage pits of Tanzania. Chris will be remembered fondly by all students and colleagues who were fortunate enough to receive his wisdom and kindness.

Professor Clive Davies will be most remembered for his rigorous research aimed to control leishmaniasis by reducing sandfly vectors in South America, the Middle East and the Indian subcontinent. His group achieved significant control of infantile leishmaniasis in Iran by fitting deltamethrin-impregnated collars to canine reservoir hosts. Clive’s other research interests included Chagas disease and dengue fever. Clive earned respect as a teacher and supervisor of students, and was always there to advise colleagues by improving their study designs.

Dr Nigel Hill spent his entire working life at the School. Throughout those 30 years, Nigel was exceptionally generous and was always available to support students and colleagues. Nigel conducted much of his field work in China, Laos and South America on the use of topical and space repellents to provide protection against malaria where mainstay insecticidal tools failed. He was particularly interested in the development of natural repellents for indigenous people who are unable to use any other forms of protection against malaria. With this view in mind, Nigel proposed the present volume focusing on biological and environmental tools for the control of disease vectors and it was he who approached most of the authors herein for their contributions.

1 Introduction

Lena M. Lorenz* and Mary M. Cameron

London School of Hygiene & Tropical Medicine, London, UK

For the majority of people, the most obvious example of using vector control for an infectious disease that immediately springs to mind is that of malaria control. Progress in the fight against malaria has been headline news since Bill Gates called for its eradication at the Gates Malaria Forum in 2007 (Roberts and Enserink, 2007; Tanner and de Savigny, 2008), which initiated increased public and private spending for the cause (RBM, 2011). Therefore, it is fitting to provide a synopsis of the classical example of the history of malaria vector control, and its limitations, prior to presenting an overview of alternative methods based around environmental and biological control. Throughout this book, both malaria control and the control of a diverse array of other tropical vector-borne diseases (Table 1.1) will be described in more detail. A range of control methods other than insecticides have been developed and employed against disease vectors to combat site- and species-specific ecological traits of vectors, changes in disease patterns due to environmental change and urbanization and the evolution of resistance against chemical control methods.

1.1 Malaria Control and its Limitations

Malaria parasites are transmitted between humans by species of the anopheline mosquito complex. The very specific biting and blood feeding behaviour of the main vector in sub-Saharan Africa Anopheles gambiae sensu stricto, namely indoor biting and resting during evenings and at night time, has allowed the use of targeted control tools, particularly indoor residual spraying (IRS) with insecticides and the use of insecticide-treated bed nets (ITNs) (Pates and Curtis, 2005). However, alternative methods of anopheline control now need to be sought following a surge in insecticide resistance in mosquitoes (Ranson et al., 2011), potentially rendering ITNs and IRS less effective in areas with high levels of resistant mosquitoes (e.g. in Benin; N’Guessan et al., 2007; Asidi et al., 2012). In addition, the successful application of tools targeting indoor mosquito activities has led to a change in species composition from the specialist An. gambiae s.s. to the more generalist An. arabiensis females, which bite in- and outdoors (Reddy et al., 2011; Kitau et al., 2012).

Table 1.1. Summary of vectors of tropical infectious diseases and potential control methods.

1.1.1 Malaria control during the pre- and post-DDT era

Before the discovery of DDT (dichlorodiphenyltri-chloroethane) in the 1940s, early disease control programmes included environmental and biological methods, such as house screening and the drainage of swamps and other breeding sites (Rozendaal, 1997; Keiser et al., 2005). For example, on the island of Java in Indonesia, periodic drainage of rice fields and cleaning of fish ponds helped to eliminate malaria; a success that is still evident now 80 years after implementation (Raghavendra et al., 2011). Generally, environmental management strategies focus on changing natural habitats by removing existing or avoiding the creation of new vector breeding sites, and improving human habitation and sanitation to reduce the number of disease vectors in a given area (Walker and Lynch, 2007). Often, these strategies aim to promote community participation and enhance community benefits without polluting the environment. In Malaysia, specific environmental control methods were employed after the local mosquito vectors and their ecological breeding requirements had been identified. Indoor residual spraying, ITNs and personal protection measures were combined with house screening, clearance of vegetation to remove shade required by the anopheline larvae and environmental modification, including the installation of automatic siphons to flush streams, drains packed with coconut husk to create stable underground drainage channels, and construction of tidal gates to control the salinity in coastal swamps (Konradsen et al., 2004; Jobin, 2012). Keiser et al. (2005) conducted a meta-analysis of the impact of environmental management on the prevention of malaria-attributable morbidity and mortality, and concluded from a total of 24 studies, most of which had been conducted pre-1955, that environmental modification, manipulation and changes in human habitation provided a high protective efficacy on clinical malaria parameters (79.5–88% reduction in risk). Although these conclusions are promising, and warrant the renewed interest in alternative methods of disease control, the studies included in the meta-analysis were few and at least 50 years old; in addition, heterogeneity between studies was large and publication bias was detected, i.e. studies with positive results were more likely to be published.

However, despite the promises of environmental management, once DDT and, in the 1980s, synthetic pyrethroids became widely available, the world adopted insecticides for IRS and to impregnate bed nets, leaving the more localized, environmentally sensitive methods to fade. Unarguably, DDT was highly successful in eliminating malaria from North America, Europe, the former Soviet Union and most Caribbean islands (Bruce-Chwatt, 1980) as well as Taiwan (Chen and Chen, 2009). None the less, concerns about the impacts of DDT on the environment and human health, initiated by Rachel Carson’s publication of Silent Spring (Carson, 1962), led to the ban of DDT by the Environmental Protection Agency (EPA) in the USA in 1972. To date, the long-term impacts on human health are disputed and the available epidemiological studies on associations with cancer and other diseases are inconclusive (e.g. van den Berg, 2009, 2010; Tren and Roberts, 2010). What is known is that the replacement of DDT with pyrethroids in South Africa was partly to blame for a sharp increase in malaria incidence by fivefold to around 60,000 cases per year as mosquitoes developed pyrethroid resistance (Hargreaves et al., 2000) and the malaria parasite evolved resistance to sulfadoxine-pyrimethamine (SP) (Blumberg and Frean, 2007). In fact, malaria incidence only decreased again after the reintroduction of DDT in IRS programmes, and after the drug artemetherlumefantrine was made available (Barnes et al., 2005). The World Health Organization (WHO) now recommends the use of DDT against malaria vectors in Africa and other areas where mosquitoes are still susceptible to DDT, as reasoned in a recent WHO position statement: ‘The Convention has given an exemption for the production and public health use of DDT for indoor application to vector-borne diseases, mainly because of the absence of equally effective and efficient alternatives. … It is expected that there will be a continued role for DDT in malaria control until equally cost-effective alternatives are developed’ (WHO, 2011).

1.1.2 Current insecticide-based control methods and their limitations

The insecticides currently recommended by the WHO Pesticide Evaluation Scheme (WHOPES) to be used in IRS belong to four insecticidal compound classes: pyrethroids, organochlorines (DDT), organophosphates and carbamates; only pyrethroids are licensed to be used on long-lasting insecticidal nets (LLINs). Both methods are the mainstay in modern day malaria control, and have led to incredible reductions in malaria incidence: LLINs and IRS are estimated to avert approximately 220,000 deaths of children under the age of 5 every year (WHO, 2012b). Insecticide-based control methods are predicted to remain an essential component of disease control strategies, particularly in high transmission settings and in areas where most vectors are still exhibiting indoor biting and indoor resting behaviours and are still susceptible to insecticides. However, the reliance on the small arsenal of insecticidal compounds that is currently available (Nauen, 2007) and the rapid evolution of insecticide resistance in mosquitoes (Ranson et al., 2011; Asidi et al., 2012) are putting existing global eradication efforts at risk, recently prompting the WHO to publish a document on the management of insecticide resistance for malaria control (WHO, 2012b). In fact, particularly now that more and more attention is being paid to malaria eradication, and reductions in entomological inoculation rates (EIRs) occur even in historically high transmission settings (e.g. an 18-fold reduction in EIR between 1990 and 2008 in the Kilombero Valley, Tanzania; Russell et al., 2010), alternative control methods will increase in relative importance (Shaukat et al., 2010). Whereas chemical control is highly effective at early stage control programmes, more species- and location-specific malaria control (such as environmental and biological control methods) will become a central component in low and moderate transmission settings when disease incidence nears elimination (Beier et al., 2008). Thus, both for malaria control and for control of other vector-borne diseases (Table 1.1), alternative, sustainable and environmentally friendly methods that do not select for resistance and that are locally adaptable, are required.

1.1.3 Specifically tailored control interventions

All disease control programmes need to be specific to disease epidemiology and vector ecology and behaviour to reduce their vectorial capacity in local settings. Often, environmental and biological control methods are not universally applicable, and their efficacy in reducing disease transmission depends on how well the intervention is matched to the vector’s specific ecological characteristics, which may include breeding site preferences, dispersal distance, feeding preferences (e.g. type of host, time of feeding, location of feeding) and the level of insecticide resistance (WHO, 2012a). Misidentification of species can thus lead to the targeting of non-vector species with subsequent failure of control programmes. For example in Vietnam, Anopheles varuna, a zoophagic mosquito species that does not vector malaria was identified as Anopheles minimus. This led to intense efforts to eliminate An. minimus rather than the actual predominant malaria vector present (Anopheles dirus), which exhibits different behaviours and requires different control interventions (Van Bortel et al., 2001). Additionally, environmental conditions, such as temperature, humidity and rainfall may also affect particular interventions, and therefore their effects on disease transmission.

This knowledge is leading to the increasing recognition of the importance of combining a range of different control methods within programmes, sometimes not just to fight one disease but to target several vectors or diseases within one programme (see Cameron et al., Chapter 10, this volume). Integrated vector management (IVM), adapted from the agricultural concept of integrated pest management, is being hailed for the sustainable management of disease vectors (Thomas et al., 2012; WHO, 2012a) and should complement already existing disease control strategies to avoid the dependence on single methods (e.g. Killeen et al., 2000).

1.2 A Role for Environmental and Biological Control

So, what are the alternatives to supplement the use of insecticides in disease control, and to restrain the evolution of insecticide resistance in vectors? Options for vector control include chemical control, environmental management, biological control and personal protection, such as use of repellents, wearing protective clothes and sleeping under bed nets.

As described above, environmental management, which includes environmental modification, environmental manipulation and modification of human habitations (WHO, 1980), is a viable option that has been successfully employed in water management schemes, such as drainage and irrigation (see Konradsen et al., Chapter 9, this volume), in vegetation manipulation schemes (see Lorenz et al., Chapter 4, this volume), in sanitation schemes to develop more hygienic sanitation options and reduce diarrhoeal infections (see Ensink et al., Chapter 8, this volume) and in house improvements, including house screening (see Kirby, Chapter 7, this volume). Biological control utilizes natural enemies, such as arthropods, including copepods and Toxorhynchites (see Howard, Chapter 2, this volume), fish (see Chandra et al., Chapter 3, this volume), fungi (see Stevenson et al., Chapter 5, this volume) and biological toxins, Bacillus thuringiensis israelensis, Bti, and Bacillus sphaericus, Bs (see Cameron et al., Chapter 10, this volume), and plant- and chemically derived semiochemicals (see Lorenz et al., and Logan et al., Chapters 4 and 6, this volume, respectively) to control and suppress disease vector populations. Plant extracts often form the basis of the development of new insecticides, against both vector larvae and adults (Koch et al., 2005).

1.2.1 Control options against vector larvae and adults

Traditionally, biological agents such as larvivorous fish, Bti/Bs and arthropods were employed to target larval breeding sites, thus making them mainly useful against vector species with few and easily identifiable breeding sites. Stegomyia (formerly Aedes) aegypti female mosquitoes, vectors of dengue and other arboviruses, lay their eggs in peri-domestic habitats, which are relatively easy to locate and can thus be controlled effectively with larval control agents. More recently, there has been increased research into biological control agents that can also target adult vectors, for example the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae (see Stevenson, Chapter 5, this volume). Their use as adulticides, particularly against anopheline malaria vectors, is based on the epidemiological principles of malaria (Smith et al., 2007). Late-life acting (LLA) biopesticides or insecticides will kill mosquitoes before they can transmit the malaria parasite but after they have reproduced, thus decreasing the selection pressure to evolve resistance against the control agent (Read et al., 2009). Plant- and chemically derived semiochemicals can be utilized in another sustainable way, which is predicted to select for lower resistance, by manipulating natural olfactory-driven behaviours such as mate- or host-seeking, breeding site selection or avoidance of natural predation (Gibson and Torr, 1999; Logan and Birkett, 2007). The deployment of odour-baited traps and insecticide-treated targets reduced tsetse fly populations by more than 99.9% in two key trials in Zimbabwe (Vale et al., 1986, 1988). Many insect repellents are based on plant-derived compounds, such as PMD (para-menthane-3,8-diol), which reduced the risk of contracting malaria in Bolivia by 80% (Hill et al., 2007).

1.2.2 Genetic manipulation of disease vectors

Other techniques to control populations of disease vectors, which we do not describe in more detail in this book, are genetic approaches to vector control. Here we describe three recent examples that utilize different molecular techniques in the fight against disease vectors.

A transgenic method closely related to Sterile Insect Technique (SIT) is the release of insects carrying a dominant lethal gene (RIDL), where Stegomyia males are modified to carry a lethal gene for female mosquitoes, causing the death of the dengue vectors unless they are reared on specific dietary supplements (Thomas et al., 2000). In the Cayman Islands, it was demonstrated that releasing genetically modified males of St. aegypti for a 4-week period resulted in about 56% mating success with wild females, however with large uncertainties around this estimate (field competitiveness compared to wild-type males: 0.56; 95% CI: 0.032–1.97) (Harris et al., 2011). Additional essential parameters that determine the competitive fitness of mosquitoes, such as longevity and dispersal of the released transgenic males, were not recorded, making the overall applicability of the RIDL technique in realistic settings difficult to judge. Recently, a genetic strain of the maternally inherited bacterium Wolbachia, which naturally infects 60% of insect species, reduces the lifespan of adult Stegomyia mosquitoes (McMeniman et al., 2009) and blocks transmission of dengue (Walker et al., 2011), was shown to successfully invade two natural St. aegypti populations in Australia (Hoffmann et al., 2011). Therefore, this novel approach could reduce the capability of St. aegypti to transmit dengue without the need to eradicate the whole mosquito population. Finally, Anopheles stephensi mosquitoes, the main malaria vectors in south Asia and the Middle East, were modified to over-express Akt, a protein that regulates insulin signalling. Transgenic mosquitoes were 60–99% less likely to be infected with malaria parasites and had an approximately 20% shorter lifespan than unmodified mosquitoes, thus reducing the time that mosquitoes can be infective to humans (Corby-Harris et al., 2010). These approaches are just some examples amongst many currently being developed in laboratory environments around the world. Of course, one major issue with genetic manipulation of disease vectors is their ethical considerations and the acceptance of the public. Recently, there have been vocal protests by anti-GM activists both in the UK against research on genetically modified wheat at Rothamsted Research, Hertfordshire (BBC, 2012), and in Miami, Florida, against the experimental release of Oxitec’s RIDL mosquitoes (Huffington Post, 2012). Thus, whether the release of more vectors, supposedly disease-proof or not, will become generally acceptable is a question that remains to be answered (Bonhannon, 2002; Lavery et al., 2008).

1.2.3 Community and industry engagement

Overall, however, the success of all potential vector control methodologies, whether chemical, environmental, biological or genetic, depends not only on the technical advances and ecology of disease vectors, but also on community, government and industry engagement. Many potential elements of control strategies, such as sanitation, housing and agricultural irrigation systems, lie outside the scope of disease control programmes. Therefore, inter-sectorial collaborations need to become more active to help reduce the burden of disease (WHO, 2012a). Currently, the health sector often lacks the capacity to assist community participation and education, despite the benefits that local organizational structures have shown (e.g. in South America; Bryan et al., 1994). If control programmes generate income for the community members, for example by improving rice yield by stocking rice paddies with edible fish that remove mosquito larvae (Wu et al., 1991; Howard et al., 2007), then the uptake is usually much greater, making programmes more cost-effective (van den Berg et al., 2007). According to Rozendaal (1997), suitable vector control methods for community involvement should be effective, affordable, simple to apply, compatible with local customs and beliefs, safe and use local materials and equipment. In addition, it is also essential to create financial incentives for industries to invest in research and development of new strategies to increase the wealth in new, alternative and sustainable disease control strategies. One successful example is the Innovative Vector Control Consortium (IVCC), which is a product development partnership that helps to innovate new insecticides for public health vector control (http://www.ivcc.com).

1.3 Conclusions

In the final chapter (see Lines, Chapter 11, this volume), Jo Lines outlines the evidence that is required for public health practitioners to justify the adoption and implementation of a new biological and environmental intervention in publicly funded disease control programmes. Two systematic Cochrane Reviews, one on the use of larvivorous fish against malaria (Burkot et al., 2009) and the other on the use of larval source management with Bti and Bs on malaria incidence (Thwing et al., 2011), are currently being finalized. However, Cochrane Reviews, originally designed to summarize the results of randomized-controlled clinical trials of medical interventions, have some limitations when it comes to comparing interventions aimed at different vector populations in field settings (see Lines, Chapter 11, this volume). Nevertheless, the reviews are likely to highlight the lack of good quality studies that evaluate the effectiveness of alternative or supplementary control strategies, which supports the views made by many of the authors in this volume. In conclusion, the need to investigate the progress in biological and environmental control methods for malaria and other vector-borne diseases that have received less attention has never been timelier.

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2 Control with Arthropods

Annabel F.V. Howard*

London School of Hygiene & Tropical Medicine, London, UK

2.1 Introduction

Deploying arthropods to seek and destroy other arthropods – to some it may sound like science fiction, but this is what underpins the whole concept of biological control. Biological control is defined as the deliberate use of natural enemies to reduce the number of pest organisms (Rodriguez-Perez et al., 2012). While this covers the whole range of interactions between predators, parasites and pathogens with their hosts, it is the predation of arthropods on arthropods that has been most widely used for biological control. As early as AD304, the weaver ant, Oecophylla smaragdina, was being intentionally placed into citrus orchards in China to prevent tree