Forest Pest and Disease Management in Latin America: Modern Perspectives in Natural Forests and Exotic Plantations 3030351424, 9783030351427

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Sergio A. Estay  Editor

Forest Pest and Disease Management in Latin America Modern Perspectives in Natural Forests and Exotic Plantations

Forest Pest and Disease Management in Latin America

Sergio A. Estay Editor

Forest Pest and Disease Management in Latin America Modern Perspectives in Natural Forests and Exotic Plantations

Editor Sergio A. Estay  Instituto de Ciencias Ambientales y Evolutivas Universidad Austral de Chile Valdivia, Chile Center of Applied Ecology and Sustainability (CAPES) Pontificia Universidad Católica de Chile

Santiago, Chile

ISBN 978-3-030-35142-7    ISBN 978-3-030-35143-4 (eBook) https://doi.org/10.1007/978-3-030-35143-4 © Springer Nature Switzerland AG 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

To my grandparents, who encouraged my curiosity. To my mom, who taught me the discipline necessary to use my curiosity. To my dad, who taught me to be patient along the way. To Stella, for her company all these years. A mi familia, porque nada sería posible sin ellos.

Acknowledgements

First, thanks to all the colleagues that accepted to participate in this monograph. I hope you are happy with the final result. Thanks a lot to Joao Pilvervasser, Springer editor, who originally had the idea for this book. Many thanks to Carmen Paz Silva for helping me with all the small details that editing a book involves. Thanks to my friends, los maestros, for their support, discussions and all the great moments. Thanks to Naty for making me feel older and older. Many thanks to all the former and current Anubis Lab members. My deepest gratitude to Jaime E.  Araya and Mauricio Lima for guiding my first steps in the world of pest management and ecology. Finally in Spanish, gracias a todos los sobrinos, hijos de amigos y pequeños curiosos que cada vez que ven un insecto se acercan a preguntar al tío Sergio que especie es.

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Contents

1 Introduction����������������������������������������������������������������������������������������������    1 Sergio A. Estay Part I General Perspectives 2 Biological Control of Forest Pests in Uruguay��������������������������������������    7 Gonzalo Martínez 3 Past and Current Strategies for the Control of Leaf-Cutting Ants in Brazil��������������������������������������������������������������������   31 Terezinha Maria Castro Della Lucia and Karina Dias Amaral 4 Remote Sensing for Insect Outbreak Detection and Assessment in Latin America����������������������������������������������������������   45 Roberto O. Chávez and Ronald Rocco Part II Pests of Natural Forests 5 Ormiscodes amphimone Outbreak Frequency Increased Since 2000 in Subantarctic Nothofagus pumilio Forests of Chilean Patagonia��������������������������������������������������������������������������������   61 Álvaro G. Gutiérrez, Roberto O. Chávez, Javier A. Domínguez-Concha, Stephanie Gibson-Carpintero, Ignacia P. Guerrero, Ronald Rocco, Vinci D. Urra, and Sergio A. Estay 6 Ormiscodes Outbreak Dynamics: Impacts and Perspectives in a Warming World��������������������������������������������������������������������������������   77 Juan Paritsis 7 Native Forest Health in Chile: Toward a Strategy of Sustainable Management��������������������������������������������������������������������   89 Cecilia Ruiz, Cristian Montalva, and Milixsa González ix

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Contents

Part III Pests and Diseases of Forest Plantations 8 Invasive Insects in Forest Plantations of Argentina: Ecological Patterns and Implications for Management ����������������������  107 Juan C. Corley, José M. Villacide, and María V. Lanstchner 9 Diseases of Eucalyptus Plantations in Uruguay: Current State and Management Alternatives����������������������������������������  123 Sofía Simeto, Gustavo Balmelli, and Carlos Pérez 10 Pests Management in Colombian Forest Plantations ��������������������������  145 Olga Patricia Pinzón-Florián 11 Disease Management in the Forest Plantations in Chile����������������������  171 Rodrigo Ahumada and Alessandro Rotella 12 Insect Pests Affecting Exotic Trees in Chile and Their Management ��������������������������������������������������������������������������  185 Sergio A. Estay 13 Pest Status and Management in the Forest Plantations of Costa Rica��������������������������������������������������������������������������������������������  197 Marcela Arguedas 14 Forest Diseases in Brazil: Status and Management������������������������������  211 Edson Luiz Furtado, Waldir Cintra de Jesus Junior, and Willian Bucker Moraes Index������������������������������������������������������������������������������������������������������������������  231

Contributors

Rodrigo  Ahumada  Bioforest S.A., Camino a Coronel km 15 s/n, Coronel, Concepción, Chile Karina  Dias  Amaral  Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil Marcela Arguedas  Instituto Tecnológico de Costa Rica, Cartago, Costa Rica Gustavo  Balmelli  Programa Nacional de Investigación en Producción Forestal, Instituto Nacional de Investigación Agropecuaria (INIA), Estación Experimental INIA Tacuarembó, Tacuarembó, Uruguay Roberto  O.  Chávez  Laboratorio de Geo-Información y Percepción Remota, Instituto de Geografía, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile Juan C. Corley  Grupo de Ecología de Poblaciones de Insectos, IFAB—Instituto de Investigaciones Forestales y Agropecuarias Bariloche (INTA-CONICET), Bariloche, Argentina Departamento de Ecología, Universidad Nacional del Comahue, Bariloche, Bariloche, Argentina Waldir  Cintra  de Jesus  Junior  São Carlos Federal University (UFSCar), Buri, SP, Brazil Terezinha  Maria  Castro  Della  Lucia  Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil Javier A. Domínguez-Concha  Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile Sergio  A.  Estay  Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile xi

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Center of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile Edson  Luiz  Furtado  Department of Plant Protection, College of Agronomic Science Research Farm Lageado Botucatu - São Paulo State University, Botucatu, SP, Brazil Stephanie Gibson-Carpintero  Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile Milixsa González  Unidad de Protección Agrícola y Forestal, Servicio Agrícola y Ganadero, Coyhaique, Chile Ignacia  P.  Guerrero  Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile Álvaro  G.  Gutiérrez  Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile María  V.  Lanstchner  Grupo de Ecología de Poblaciones de Insectos, IFAB— Instituto de Investigaciones Forestales y Agropecuarias Bariloche (INTACONICET), Bariloche, Argentina Gonzalo  Martínez  Laboratorio de Entomología, Programa Forestal, Instituto Nacional de Investigación Agropecuaria (INIA), Tacuarembó, Uruguay Cristian Montalva  Instituto de Conservación, Biodiversidad y Territorio, Facultad de Ciencias Forestales y Recursos Naturales, Universidad Austral de Chile, Valdvia, Chile Willian Bucker Moraes  Agronomy Department, Espírito Santo Federal University (UFES), Alegre, ES, Brazil Juan  Paritsis  Laboratorio Ecotono, INIBIOMA-Universidad Nacional del Comahue, CONICET, Bariloche, Argentina Carlos  Pérez  Departamento de Protección Vegetal, EEMAC, Facultad de Agronomía, Universidad de la República, Paysandú, Uruguay Olga Patricia Pinzón-Florián  Facultad del Medio Ambiente y Recursos Naturales, Universidad Distrital “Francisco José de Caldas”, Bogotá, Colombia Ronald Rocco  Laboratorio de Geo-Información y Percepción Remota, Instituto de Geografía, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile Alessandro  Rotella  Bioforest S.A., Camino a Coronel km 15 s/n, Coronel, Concepción, Chile

Contributors

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Cecilia  Ruiz  Instituto de Conservación, Biodiversidad y Territorio, Facultad de Ciencias Forestales y Recursos Naturales, Universidad Austral de Chile, Valdvia, Chile Sofía Simeto  Programa Nacional de Investigación en Producción Forestal, Instituto Nacional de Investigación Agropecuaria (INIA), Estación Experimental INIA Tacuarembó, Tacuarembó, Uruguay Vinci  D.  Urra  Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile José M. Villacide  Grupo de Ecología de Poblaciones de Insectos, IFAB—Instituto de Investigaciones Forestales y Agropecuarias Bariloche (INTA-CONICET), Bariloche, Argentina

Chapter 1

Introduction Sergio A. Estay

Forests cover around 46% of Latin America and the Caribbean (FAO 2018), an area of ~885 million ha (FAO 2015). Ninety-eight percent of this area corresponds to native forests and only 15 million ha to plantations (FAO 2015). These forests produced US$18.7 billion in export value for our countries in 2017 (FAO 2019) and also provide multiple economic goods and ecosystem services. Despite this clear importance for the social, environmental, and economic development of our countries, Latin American forests face several threats. For example, it is expected that the extension of these forests will be reduced by 5% by 2020 (FAO 2006). In the same vein, these forests face a myriad of phytosanitary problems that negatively impact on both conservation efforts and the forest industry. Native and exotic pests and diseases can be found damaging trees from the tropical forests of Central America to the Mediterranean and temperate vegetation of the Southern Cone. The FAO (2009) identified 113 pest organisms in eight countries in the region. Ten years after this evaluation, the number of phytosanitary problems has increased significantly, in some cases due to the introduction of exotic organisms or to the adaptation of native organisms to exotic forest resources like plantations of pines or eucalyptus. Using available data, van Lierop et al. (2015) estimated the area affected by insect pests in South America alone is almost 1.14 million ha. The importance of the impact of pests and diseases on forest resources in our countries has led, at least in part, to the creation of several regional plant protection organizations. Today, regional forest protection is promoted and coordinated through several organizations in Latin America (FAO 2009):

S. A. Estay (*) Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile Center of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile e-mail: [email protected] © Springer Nature Switzerland AG 2020 S. A. Estay (ed.), Forest Pest and Disease Management in Latin America, https://doi.org/10.1007/978-3-030-35143-4_1

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–– Comité de Sanidad Vegetal del Cono Sur (COSAVE): Argentina, Bolivia, Brazil, Chile, Paraguay, Peru, and Uruguay –– Comunidad Andina (CA): Bolivia, Colombia, Ecuador, and Peru –– Caribbean Agricultural Health and Food Safety Agency (CAHFSA): Antigua and Barbuda, Bahamas, Barbados, Belize, Dominica, Grenada, Guyana, Haiti, Jamaica, Montserrat, Saint Lucia, St. Vincent and the Grenadines, Suriname, and Trinidad and Tobago –– Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA): Belize, Costa Rica, Dominican Republic, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, and Panama Unfortunately, the institutional support for phytosanitary protection is sometimes insufficient considering the importance of the resources. The FAO (2009), in its diagnosis of the capacity for forest health protection in Latin America, indicated that in many countries, these activities are still informal processes, so the availability of high-quality data is scarce. The need for quantitative data is central to achieving comparative analyses that will allow Latin American decision makers to continuously improve operational tasks. The availability of high-quality data is a key component to comparing not only the impact of similar pests throughout Latin America but also the effectiveness of control practices or the coordination of common strategies among countries. In this book, we have collected the perspectives of several Latin American researchers on pest and disease management. Each chapter provides modern views of the status and management alternatives to issues as serious as the impact of introduced exotic insects and diseases on Pinus and Eucalyptus plantations across the continent, or the emergence of novel insect outbreaks in tropical and temperate native forests associated with global warming. The book is structured in three parts. In the first, several authors provide their view on several phytosanitary issues common to many countries in the region. An introductory chapter provides context to the importance of the forests for Latin American countries, their current status, and major challenges for forest health nowadays. General preventive and control strategies are also reviewed. Invasion patterns, biocontrol strategies, and technological tools applied to pest surveys are analyzed in detail. The second part focuses on pests in native forests. Several insects have historical importance due to their severe attacks on trees in temperate forests, but climate change also seems to be causing the emergence of new problems. Both topics are extensively reviewed in this part. Finally, the last part addresses the problem of pests and diseases on forest plantations. Despite its small size in relation to natural forests, the economic importance of exotic tree plantations has meant that most of the research efforts have concentrated on these resources. From tropical and subtropical plantations of high-value wood trees to the extensive pine and eucalyptus plantations in South America, these plantations face the threat of several native and exotic pests and diseases, which are reviewed in detail in this part. We hope this volume will be a useful guide for researchers and practitioners working on forest health in our region and around the world and serve as an ­incentive for greater collaboration between researchers and governmental institutions to

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improve the health of our forests on a regional scale by sharing experiences and avoiding duplicate efforts. It has been a privilege to work with this select group of specialists. My deepest gratitude to you all.

References FAO (2006) Tendencias y Perspectivas del Sector Forestal en América Latina y el Caribe. FAO montes estudio N°156. Rome FAO (2009) Global review of forest pests and diseases. A thematic study prepared in the framework of the global forest resources assessment 2005. FAO Forestry Paper 156. Rome FAO (2015) The global forest resources assessment. Rome FAO (2018) The State of the World’s Forests 2018—forest pathways to sustainable development. Rome FAO (2019) FAOSTAT. Food and Agriculture Organization of the United Nations, Rome. Web. http://www.fao.org/faostat/en/#data van Lierop P, Lindquist E, Sathyapala S, Franceschini G (2015) Global forest area disturbance from fire, insect pests, diseases and severe weather events. For Ecol Manag 352:78–88

Part I

General Perspectives

Chapter 2

Biological Control of Forest Pests in Uruguay Gonzalo Martínez

2.1  Introduction Forestry used to be a minor activity in Uruguay, a country historically devoted to cattle breeding and agriculture (Morey and Porcile 2002). This picture changed drastically following the passing of the Forestry Law 15.939 in 1987 (Ley Forestal 1987), which encouraged afforestation with exotic species, leading to an explosive growth of commercial tree plantations in the country. Currently, more than a million hectares are covered by tree plantations, mostly with eucalypt and pine tree species. This growing forest sector benefited initially from a relatively benign sanitary situation, due in part to the relative distance of the plantations to the centre of origin of the tree species, but the expanding area and the elapsed time soon led to the introduction of exotic insect pests, threatening plantation health and productivity (Martínez 2010; Morey and Porcile 2002). In fact, more than half of the pests currently affecting Eucalyptus entered the country after 1995 (Fig. 2.1). This situation was favoured not only by local factors but also by a worldwide acceleration in the rate of insect invasion as a consequence of an increased global trade of seeds, plants and wood packaging material (Humble 2010; Liebhold et  al. 2017; Paine et  al. 2011; Wingfield et  al. 2008), a global homogenisation of tree species planted (Garnas et al. 2012) and climate change (Battisti et al. 2005; Watt et al. 2019). In order to keep tree plantation free of insect pests, foresters have resorted to several management strategies, such as tree breeding, silvicultural management, chemical control or biological control (Ciesla 2011). Selection of resistant materials

G. Martínez (*) Laboratorio de Entomología, Programa Forestal, Instituto Nacional de Investigación Agropecuaria (INIA), Tacuarembó, Uruguay e-mail: [email protected] © Springer Nature Switzerland AG 2020 S. A. Estay (ed.), Forest Pest and Disease Management in Latin America, https://doi.org/10.1007/978-3-030-35143-4_2

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Fig. 2.1  Evolution of the introductions of forests pests (circles) and natural enemies (squares) in Uruguay. Black squares represent adventive introduction of natural enemies, together with the pest

is a common choice for dealing with diseases in the country, with some successful examples (Balmelli et al. 2004, 2014a, b). Tree selection has also been used to manage some insect pests in Uruguay. For instance, the introduction of the pine shoot moth Rhyacionia buoliana Schiff (Lepidoptera: Tortricidae) in 1955 triggered the replacement of the then extensively planted susceptible species Pinus radiata Don by other species, particularly Pinus taeda L. (Morey and Porcile 2002). Tree breeding has also been pointed out as a promising management tool for the blue gum chalcid Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae) (Jorge et al. 2016; Quang Thu et al. 2009). However, the extensive use of tree breeding as a reliable pest management strategy is unlikely, given the costs and the time required to obtain results, which is particularly critical in a scenario of constant introduction of new pests (Garnas et al. 2012). Silvicultural control methods have been extensively used in pest management in forestry (Klapwijk et  al. 2016). For instance, adjusting pruning and thinning calendars to avoid insect infestation is a usual strategy in Uruguay for the control of the wood wasp Sirex noctilio Fabricius (Hymenoptera: Siricidae) (Rebuffo 1990) and for managing bark beetle (Scolytinae) infestation (Gómez 2016). Semiochemicals can be a reliable and environmentally safe alternative for pest management (Nadel et  al. 2012), but few studies have addressed the use of semiochemicals for forestry pests in the country (but see Gómez and Hirigoyen 2016).

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The only insects that are managed by means of synthetic pesticides in Uruguayan tree plantations are the leaf-cutting ants (Formicidae: Attini) that are controlled with toxic baits (Listre 2018). Apart from this pest, the use of synthetic pesticides is greatly restricted, provided around 90% of the plantations are under FSC and/or PEFC certification schemes (http://www.spf.com.uy/uruguay-forestal-aspectosambientales). FSC standards, for instance, discourage the use of pesticides, provided the economic costs and the risk they pose to people and the environment (Willoughby et al. 2009). Moreover, synthetic pesticides are economically costly and rarely effective against cryptic species such as wood borers or gall makers. Hence, in dealing with insect pests, foresters must come up with more environmentally friendly, yet reliable strategies. Eilenberg et al. (2001) define biological control (BC) as ‘The use of living organisms to suppress the population of a specific pest organism, making it less abundant or less damaging than it would otherwise be’. Although the existence of early observations of the use of living organisms for pest management dates as old as 304 CE in China (Huang and Yang 1987), the introduction from Australia to California in 1888 of the vedalia beetle Rodolia cardinalis (Mulsant) to control the cottony cushion scale Icerya purchasi Maskell on citrus trees is considered the start of modern BC (Bentancourt and Scatoni 2001). The great success of this introduction paved the way to the current use of BC as a management tool, either alone or in combination with other techniques within the framework of Integrated Pest Management (Eilenberg et al. 2001). Biological control currently represents the major contribution to pest management in forestry and the most promising strategy to deal with the global problem of invasive insect pests in tree plantations (Garnas et  al. 2012). Indeed, above 50% of the introductions of parasitoids and predators have been made within the framework of classical BC programmes against pests of woody plants (Kenis et al. 2017). Furthermore, success rates on forest ecosystems are higher than in agriculture as it is exemplified by many cases (Cock et al. 2016; Cordero Rivera et al. 1999; Garnas et al. 2012; Hajek 2004; Hanks et al. 1996; Mendel et al. 2017; Protasov et al. 2007). Thus, classical BC seems to work better in forests and other perennial ecosystems than in agricultural systems. Finally, classical BC programmes in forestry seem to exhibit more advantageous cost-benefit ratios than those recorded for chemical control programmes (Kenis et  al. 2017). Benefits of the use of BC strategies as an alternative to synthetic pesticides have been underlined by many authors (see, e.g., Barratt et al. 2018; Brodeur et al. 2018; van Lenteren et al. 2018; Shields et al. 2019). Implementing a BC programme includes several stages and involves the participation of multidisciplinary teams (Kenis et al. 2017; van Lenteren et al. 2018). Such a complex process is not free of difficulties, resulting from the many interacting factors (Hokkanen and Sailer 1985; Hokkanen and Lynch 2003). Prior to the introduction of an organism for BC purposes, research efforts must be invested in taxonomical, physiological and ecological studies for both the pest and the potential BC agent (van Lenteren et  al. 2018) as well as the development of effective rearing systems for both organisms (Etzel and Legner 1999). Furthermore, introduction of BC agents into new areas implies international collaboration and interinstitutional

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agreements (Garnas et  al. 2012). Recent instruments in the international regulations, such as the Nagoya Protocol, impose new restrictions to the transit of organism from different country that can be a major threat to the successful implementation of BC programmes in the future (Smith et al. 2018). Here, I review the state of the art of the BC of forest insect pest in Uruguay. In the first section, I provide some context of the forestry industry in the country, including fact and figures, the institutional landscape and the regulatory framework. In the following section, I summarise the historical context in which BC of forestry pest has been developed in Uruguay, underlying the most important milestones and providing a comprehensive list of pests and natural enemy introductions on eucalypts and pine trees in Uruguay. With this background provided, I move to analyse in the third section the status of BC in the country, and I review the most relevant cases. I conclude with comments on the strengths and hurdles and a wish list for the future of BC in Uruguay.

2.2  The Forestry Sector in Uruguay 2.2.1  Fact and Figures Commercial forestry is one of the most dynamic sectors of the Uruguayan economy. Currently, forests cover 1,914,509 ha in Uruguay, considering natural and planted forests, which correspond to around 10% of land area (Boscana and Boragno 2018). Natural forests cover 835,349  ha (4.7%) while commercial tree plantations have grown since the passing of the last forestry law in 1987 from 95,000 to 1,079,160 ha in 2018 (Boscana and Boragno 2018). Uruguayan gross domestic product (GDP) reached US$56 billion in 2018 (BCU 2018). The forestry sector, which comprises the forest plantations, has increased its share in the agricultural product from 3.8 to around 9% between 1990 and 2017 (OPYPA-MGAP 2018). In 2018, export of forestry goods reached US$2.25 billion, ranking first in the export of agricultural goods (OPYPA-MGAP 2018). Commercial forestry in Uruguay relies mostly on monocultural tree plantations of eucalypt species which reach 80% and of pine tree species, which comprise the extant 20% (Boscana and Boragno 2018). A distinctive feature of the forestry sector in Uruguay, when compared to neighbouring countries, is the large integration of the productive chains, given the existence of big companies that are involved in the whole process, from the production of seeds and clones to the pulp extraction (Instituto Cuesta Duarte 2018). Additionally, as mentioned above, Uruguayan forestry characterises by a large coverage of FSC and PEFC certification which restricts the use of synthetic pesticides, opening an opportunity window for BC.

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2.2.2  Institutional Landscape Three governmental agencies have competencies on forestry pest management and BC. The role of National Plant Protection Organisation (NPPO) is fulfilled in Uruguay by the General Direction of Agricultural Services (DGSA, by its acronym in Spanish), a secretary of the Ministry of Livestock, Agriculture and Fisheries (MGAP). Thus, DGSA is responsible for gathering information on phytosanitary status through surveillance, to confer the pest status to a certain organism or group of casual agents, following national and international regulations (CECOPE 2012). The General Forestry Direction (DGF), also within the MGAP, oversees the National System of Forest Information and the National Forest Inventory, and it is responsible for granting permission to private and public companies to exploit tree resources nationwide. The DGF has also direct competencies in forest protection and surveillance, conferred by the Forestry Law (Ley Forestal 1987), namely, the establishment of a protection service against the different agents of damage in the natural forests and tree plantations, as well as to advice on the prevention and management of pests and abiotic disturbances that can affect the survival of the forest (CECOPE 2012). Technical staff from this agency was responsible up to the first decade of the twenty-first century for the BC programmes developed in the forestry sector. Finally, the National Direction of Environment (DINAMA) seated in the Ministry of Housing, Territorial Ordering and the Environment is the agency responsible for the exclusive coordination of the environmental management within the governmental entities and the focal point of the Convention on Biological Diversity (CBD) and the Nagoya Protocol. The private forestry sector in Uruguay is characterised by the coexistence of large, foreign multinational vertically integrated companies with many small-scale primary producers and foreign investors (Morales Olmos et  al. 2018; Morales Olmos and Siry 2009). Most of the companies are members of the Society of Forest Producers (SPF). The big companies usually include their own programmes of R&D, and they usually hire specialised professionals to design their own pest management programmes. There is also a group of small companies and producers that depend on dissemination and extension by the academia and the government. Apart from the foresters, there is a variable group of professionals with different career background who give advice to plantation owners on pest management strategies. Some of these advisors, which usually work as freelancers, maintain insect rearing or assist in the release of BC agents (Balmelli et al. 2008). The academic sector in Uruguay is characterised by a big concentration of researchers on a single public institute, the University of the Republic (UDELAR), where more than 60% of the national research is conducted (http://georef.d2c2.gub. uy/en/). Additionally, in 2008, the National Agricultural Research Institute (INIA) started a new research line on forest health (Balmelli et al. 2008). In August 2001, a ministerial resolution by the MGAP created the Executive Committee of Pests and Diseases affecting Tree Plantations (CECOPE). The CECOPE has become an integrative space for the discussion and coordination of

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pest management policies. It is made up of representatives from the DGF, DGSA, SPF and INIA. In 2012, the CECOPE redacted the current national strategy for the health of planted forests (CECOPE 2012). This strategy emphasises the use of BC as a preferred sustainable technique for pest management in tree plantations.

2.2.3  Regulatory Framework Uruguay has a long history of adherence to international agreements and standards (Fonalleras 2012). For instance, Uruguay signed the foundational act of the IPPC and ratified it in 2001 (Law 17.314). Uruguay is also part of the CBD (Law No. 16.408, 1993) and the Nagoya Protocol (Law No. 19.227, 2014). Considering the regional landscape, Uruguay is part of the COSAVE, the Regional Plant Protection Organisation for southern South America (http://www.cosave.org) since its foundation in 1989 (Fonalleras 2012). In the last decade, Uruguay has strengthened the regulatory framework concerning the use of BC in agriculture and forestry to encourage its implementation in the country. The Decree 170/2007 declared the use of BC agents ‘of interest for the agricultural production’ and established some conditions for their importation and release, harmonised with the ISPM 3 (FAO 2005: 3). Microbial control agents are regulated by the Resolution of the MGAP no. 688 passed in February 2013, which establishes the conditions for their register and use, including standards for risk analysis and product labelling. Similarly, the registry and use of entomophagous insects as BC agents are regulated by the Resolution no. 220, passed on April 2014, which regulates the requirements needed for the register of predators and parasitoids as BC agents, including risk analysis prior to release and the efficacy assessment and monitoring after the release. Register in both cases is granted for 4 years, so the producers must apply for a new permission after this period.

2.3  Biological Control in Uruguayan Tree Plantations 2.3.1  A Bit of History Biological control started in Uruguay with the importation of Encarsia berlesei (Howard) (=Prospaltella berlesei; Hymenoptera: Aphelinidae) to control the white peach scale Pseudaulacaspis pentagona (Targioni-Tozzetti) (Hemiptera: Diaspididae) in 1912 (Trujillo 1963). The use of microbial agents for BC in Uruguay can be traced back to 1911, when Dr. D’Herelle came to the country to make some experiments with Coccobacillus acridiorum D’Herelle as a controller for Schistocerca cancellata (Serville) (Orthoptera: Acrididae) (Trujillo 1963). The first BC agent used in Uruguayan forestry was the parasitoid wasp Anaphes nitens Girault (Hymenoptera: Mymaridae), imported from South Africa in 1941 to manage the eucalypt snout beetle (Trujillo 1963).

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Most of the insects attacking eucalypt and pine trees in Uruguay are exotic. The arrival of forest insect pest in Uruguay, as well as the introduction of natural enemies, both intended or incidental, is well documented in the country, but not always included in peer-reviewed publications, making some records difficult to locate, as they were originally published on internal communications of the MGAP or even on the local press. We can divide the history of Uruguayan forestry into four periods, from the point of view of pest management and BC. An initial chapter in Uruguayan forestry includes the late nineteenth century and the first half of the twentieth century. During this period, forestry was still an incipient activity, marginal when compared to cattle farming or agriculture. Biological control was a common practice in agriculture then, maybe more than today, and the country used to introduce and export several natural enemies as BC agents for different agricultural pests (Trujillo 1963). In 1911, the first public forestry nursery was opened in the country. In 1921, Pissodes notatus Fabricius (Coleoptera: Curculionidae) became the first forestry insect to achieve official pest status (Morey and Porcile 2002). Apart from P. notatus, two other insects were reported attacking eucalypts in this period, although none of them reached official pest status. Two honorary commissions were created to promote tree planting in 1938 and 1945 (Morey and Porcile 2002). The first natural enemy was introduced for BC of a forest pest during this period, the parasitoid wasp Anaphes nitens. At the end of the period, in the 1940s, radiata pine trees were extensively planted in the country (Morey and Porcile 2002). The second period starts with the report of the pine shoot moth in 1954, which eventually led to the substitution of Pinus radiata with loblolly pine, Pinus taeda, as the most planted commercial pine tree species in the country (Morey and Porcile 2002). During this period, two key institutions were created: the SPF (1959) and the DGF (1964). Three insect pests were reported during this period, all attacking pine trees, from which only the wood wasp Sirex noctilio reached pest status, triggering the development of the second BC programme in the country and the first including the use of a parasitic nematode, Deladenus siricidicola (Bedding) (Nematoda: Neotylenchidae). During most of the second part of the twentieth century, a national strategy for organising the defence of the woods against agents of damage was formulated, including a project for the creation of a national system of protection against forestry pest and diseases (Morey and Porcile 2002). Two laws promoting commercial forestry were passed during this period: the first forestry law (13.723) in 1968 and the law in force up to date (15.939) in 1987, which concludes the period. Between the passing of the Law 15.939 and the year 2000, national tree plantations experienced an explosive growth. Three new forest insect pests were reported, all in eucalyptus. In 1992, the COSAVE created a working group on forest protection which enhanced the coordination between the DGSA as the local NPPO and the DGF, as well as among the forestry agencies and the NPPOs in the region (Fonalleras 2012; Morey and Porcile 2002). Two new introductions of entomophagous insects were recorded in the country during this period, Avetianella longoi Siscaro (Hymenoptera: Encyrtidae) (Tellechea 1999) and Psyllaephagus pilosus Noyes (Hymenoptera: Encyrtidae) (Morey et al. 2002), as well as new strains of D. siricidicola (Bianchi 2008). The introduction of A. longoi in 1998 was made in the context of a parasitoid exchange between South America and South Africa that con-

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stituted the first of such collaborative efforts between these two regions (Tellechea 1999). By the turn of the century, however, most of the team devoted to research on forest pest management at the MGAP was close to the retiring age, and the country was about to face big changes in the R&D policies. The last 20 years have shown an increase in professionalisation of the academia and a displacement of research on tree protection from the governmental agencies to research institutes and universities. The creation of research lines devoted to forest pest in the University of the Republic (UDELAR) and in the National Agricultural Research Institute (INIA), as well as the establishment of new campuses closer to the forestry areas, led to the consolidation of more research teams. Simultaneously, a tree health commission was created within the SPF, which improved the communication between the foresters and the academic sector. Last but not least, the creation of the CECOPE in 2001 catalysed the synergies among the government, the academia and the stakeholders. All these new institutional developments helped in dealing with the characteristic feature of this period: a historical increase in pest records. Between 2000 and 2019, a total of nine new insects were reported in Uruguayan forestry. Unlike the previous periods, all of these insect pests have been reported on peer-reviewed journals (Gómez et  al. 2012, 2013, 2017; Jorge et  al. 2016; Martínez and Bianchi 2010; Martínez et al. 2014a). Additionally, two monitoring schemes have been installed, maintained and improved since 2009 (Bianchi et  al. 2008; Gómez 2016). Biological control programmes developed in the last decade have been the result of a strong coordination in the context of the CECOPE, depending strongly on the academia and the private stakeholders (Martínez et al. 2018a, 2019), unlike BC programmes during the former periods which relied almost exclusively on governmental or private initiative (Morey and Porcile 2002; Trujillo 1963).

2.3.2  The Current Status of Biological Control To date, Uruguay imported five entomophagous insects and one parasitic nematode as BC agents of forest insect pests (Table 2.1). Additionally, two parasitoid wasps are known to have been introduced along with their hosts (Table 2.2). Currently, seven insect species are under BC as a result of intended programmes (Table 2.1). Classical BC has been the chosen strategy in most of the cases, but three of the programmes have resorted to inoculative releases as a regular (D. siricidicola) or additional practice (P. pilosus, A. nitens) (Table 2.1). No explicit strategy has been developed for conservative BC, although the scarce use of insecticides in the plantations may help in the conservation of natural enemy fauna. Indeed, an analysis of the community of Araneae in tree plantation showed that even when the assemblage of spiders in monospecific tree plantation tends to be less biodiverse than in the adjacent grassland (which constitutes the matrix ecosystem in the majority of the country), some species are well adapted to this habitat and remain present for a long time (Jorge 2013; Simó et al. 2011). So far, no predators have been used in BC of

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Table 2.1  List of natural enemies introduced for biological control of forest pests in Uruguay Anaphes nitens (Girault) (Hymenoptera: Mymaridae). Egg parasitoid. Introduced and released in 1941 from South Africa vs. Gonipterus platensis Marelli (Coleoptera: Curculionidae; misidentified as G. scutellatus and G. gibberus). Reintroduced in 1950 from Argentina. Classical BC. Eventually, inoculative releases have been done locally since the late 1990s (González et al. 2010; Morey and Porcile 2002; Trujillo 1963) Avetianella longoi Siscaro (Hymenoptera: Encyrtidae). Egg parasitoid. Introduced and released in 1999 from South Africa vs. Phoracantha semipunctata Fabricius (Coleoptera: Cerambycidae). Classical BC. No further introductions. No further monitoring (Bianchi and Sánchez 1999a; Morey et al. 2001; Porcile 1992; Tellechea 1999) Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae). Egg parasitoid. Introduced and released in 2013 vs. Thaumastocoris peregrinus Carpintero and Dellappe (Heteroptera: Thaumastocoridae). Classical BC. Local populations established. Monitoring ongoing (Martínez et al. 2018a) Deladenus siricidicola Bedding (Nematoda: Neotylenchidae). Pathogen. Introduced for the first time in 1987 from New Zealand vs. Sirex noctilio Fabricius (Hymenoptera: Siricidae). Regularly imported from Brazil or Chile for inoculative BC (González Parodi and Nosei Canavesi 1997; Rebuffo 1990) Psyllaephagus pilosus Noyes (Hymenoptera: Encyrtidae). Nymphal parasitoid. Introduced in 2001 from Spain vs. Ctenarytaina eucalypti (Maskell) (Sternorrhyncha: Aphalaridae). Classical BC, with occasional inundation in nurseries of E. globulus (Bianchi 2008; Morey et al. 2002; Tellechea 2008) Selitrichodes neseri Kelly and LaSalle (Hymenoptera: Eulophidae). Larval parasitoid. Introduced in 2019 from Argentina vs. Leptocybe invasa Fisher and LaSalle (Hymenoptera: Eulophidae). Classical BC ongoing (Martínez et al. 2019) Table 2.2  Exotic natural enemies introduced with their host pest in Uruguay Ibalia leucospoides (Hochenwarth) (Hymenoptera: Ibalidae). Larval parasitoid. First reported in 1984. Host: Sirex noctilio. Not used as BCA in Uruguay. It has not been recovered in the last years (Tellechea 1999) Psyllaephagus blitteus Riek (Hymenoptera: Encyrtidae). Nymphal parasitoid. First reported in 2005. Host: Glycaspis brimblecombei. Established in the whole country (Bianchi 2008)

forestry pests in Uruguay although on a comprehensive review of natural enemies used in BC of insect pests in Uruguay, the author mentioned predator insects being used in other production systems (Bentancourt and Scatoni 2001). Despite the early adoption of entomophagous insect as BC agents of forestry pests, the BC by using microbial agents and other parasitic organisms in forestry (and in agriculture in general) has not been adopted, and it has been restricted to very few cases (Bettucci et  al. 2006). So far, only the aforementioned nematode D. siricidicola has been used systematically as a BC agent for the pine wood wasp S. noctilio (Morey 1993). Specifically, the use of entomopathogenic fungi had only been explored in the laboratory for some forestry insect pest until recently (Bettucci et al. 2006; Corallo et al. 2017; Tiscornia et al. 2014). The development of a biopesticide for the bronze bug constitutes the largest effort made so far (Abreo et  al. 2019). In the following sections, I describe the BC programmes developed in the country up to date.

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2.3.3  The Eucalyptus Snout Beetle The existence of beetles from the genus Gonipterus is known in Uruguay since February 1937, when some insects attacking urban Eucalyptus trees in Montevideo were identified as G. gibberus (Trujillo 1963). It was assumed they entered from Buenos Aires province, where this species had been known long before (Trujillo 1963). From the parks in the capital city, the snout beetle dispersed to Eucalyptus stands in several parts of the country. Although the Eucalyptus snout beetle never reached official pest status in the country, the initial impact of the pest raised great concern among the authorities and the foresters (Morey and Porcile 2002). Hence, in 1939, Uruguayan authorities contacted the Division of Entomology in the Department of Agriculture of South Africa via the Uruguayan embassy to ask for a shipment of the parasitoid Anaphes nitens to be released in the country. In 1941, after a series of communications, a set of parasitised eggs was sent to Montevideo by sea (Trujillo 1963). Once in Montevideo, the parasitoids were multiplied in vitro prior to their release in the most affected area in the city. The introduction was initially successful, and soon foresters in the whole country asked for shipments of parasitoids to be released in their plantations (Porcile 1996). However, after the initial success, the population of A. nitens decreased, and by the end of the decade, it ceased to be recovered from the field (Ruffinelli and Carbonell 1954). Thus, in 1950, a second shipment of parasitised eggs of the snout beetle was imported, this time from Argentina, and released in the department of Canelones (Trujillo 1963). This was the last introduction of A. nitens from abroad; local populations of the parasitoid have remained in the field since. On the first decade of the twenty-first century, foresters reported an increase in the population of the snout beetle, particularly in the east of the country, dominated by stands of E. globulus, due to a local decrease in the populations of A. nitens. To deal with this problem, some forestry companies developed a rearing method for the parasitoid and made inoculative releases in areas with low parasitisation rates (González et al. 2010). Fungal strains with potential entomopathogenicity for the snout beetle have been assessed both in in vitro and field conditions (Bettucci et al. 2006). In vitro test with strains of Beauveria bassiana (Bals.-Criv.) Vuill. and Metarhizium anisopliae (Metschnikoff) Sorokin calculated an LT50 of 9  days at a concentration of 107 spores/mL in both species (Bettucci et al. 2006). Trees exhibiting high infestation by larvae of the snout beetle were treated with a spore suspension in water containing a concentration of 109 conidia/mL of both fungal species at a ratio of 1:1. After 8  days, 40% of the larval mortality recorded on the trees were caused by fungal infection (Bettucci et al. 2006). Although this study was very promising, no commercial biopesticide has been developed with these strains. The taxonomic status of the genus Gonipterus has been subject of a big revision (Mapondera et al. 2012). Recently, specimens of the snout beetle were collected in the country to confirm their taxonomic status by morphological comparisons and molecular tools. Preliminary results suggest that Uruguayan populations of the snout beetle belong to the species Gonipterus platensis Marelli (Martínez, et  al. unpublished data).

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2.3.4  The Pine Tree Wood Wasp The wood wasp Sirex noctilio (Hymenoptera: Siricidae) is one of the major pests affecting pine tree forestry worldwide (Slippers et al. 2015). This insect attacks and kills pine trees in a symbiotic association with the fungus Amylostereum areolatum (Chaillet ex Fr.) Boidin (Talbot 1977). Native from Eurasia, it invaded New Zealand at the beginning of the twentieth century and later spread to other pine-growing regions in the planet (Slippers et al. 2015). The wood wasp was first detected in Uruguay in 1980 (Rebuffo 1990) in the northeast part of the country. In 1984, the first outbreak was recorded in plantations of Pinus taeda in the littoral of the river Uruguay (department of Paysandú), affecting on average 70% of the trees and generating costs above 3000 US dollars per hectare (Morey and Porcile 2002). Given the extensive damage recorded, in 1985, a task force was created to study the importance of the problem and suggest management strategies, and the wood wasp was officially declared pest by the MGAP by Decree 890/985 by the end of that year (Rebuffo 1990). In 1987, a joint mission by the University of the Republic and a private company imported the parasitic nematode Deladenus siricidicola (Nematoda: Neotylenchidae) from New Zealand and started its production and release in the field (Morey 1993). The management strategy for the wood wasp used up to date implies yearly monitoring by sequential sampling (Penteado et al. 2008) and inoculation of nematodes depending on the result of the monitoring. However, Uruguay still lacks a national unit for producing the nematodes, depending mostly on the importation of doses from neighbouring countries, mostly Chile or Brazil. In 1984, Ibalia leucospoides (Hochenwarth) (Hymenoptera: Ibaliidae) was first recorded in Uruguay; it is likely that it was introduced along with the pest (Morey 1993). This wasp is a koinobiont parasitoid that attacks eggs and first instar larvae of S. noctilio (Fernández-Arhex and Corley 2005). When exposed to volatiles from A. areolatum, I. leucospoides exhibited increased activity, suggesting it may exploit such fungal volatiles to locate its host (Martínez et al. 2006). Despite its presence in the country, no study has assessed parasitisation of S. noctilio by I. leucospoides in Uruguay. To our knowledge, the development of a BC programme with this parasitoid has not been considered in Uruguay, although it was exported to South Africa within the context of a bilateral agreement (see below).

2.3.5  Eucalypt Psyllids Four species of Australian psyllids from the family Aphalaridae have been reported on eucalypt plantations in Uruguay. The blue gum psyllid Ctenarytaina eucalypti (Maskell) was first detected in October 1998 on E. globulus in the department of Paysandú (Burckhardt et  al. 1999). A local bioprospection of natural enemies in Uruguay detected native syrphid larvae (Diptera: Syrphidae) and ladybugs (Coleoptera: Coccinellidae) feeding on the psyllids but discarded the presence of parasitoids (Porcile 1998).

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In 2000, representatives from the DGSA and from a private company started a collaboration with the Estaçao Fitopatologica do Areiro in Pontevedra (Spain) to introduce individuals of the parasitoid wasp Psyllaephagus pilosus (Hymenoptera: Encyrtidae) that had been previously introduced from Australia and released in the field with relative biocontrol success (Bianchi 2008; Morey et al. 2002). The first release of P. pilosus in Uruguay was made in April 2001 in commercial stands of E. globulus in the department of Maldonado. A second release was made in November 2001 in Montevideo. In both cases, parasitised nymphs, also known as ‘mummies’, were placed in release devices that were taken to the field and hung to the affected trees. The release in both sites was successful, and from there, the parasitoid started spreading into new areas (Morey et al. 2002). No further introductions of this parasitoid were made in Uruguay, but an inoculative strategy was used to increase the population of the parasitoid on nurseries of E. globulus where C. eucalypti may occur. So, on the following years after the introduction, parasitised mummies were brought frequently from the field to greenhouses (Tellechea 2008). Parasitisation rate measured in young plantations of E. globulus between 2008 and 2009 varied from less than 5% in autumn to almost 40% in spring (Martínez 2010). Although no economical assessment has been made in Uruguay, BC of blue gum psyllid has proven economically beneficial in North America (Dahlsten et al. 1998). The replacement of most of the stands of E. globulus by other less susceptible species such as E. dunnii and, more recently, E. smithii has decreased the interest on this pest. The lerp psyllid Glycaspis brimblecombei Moore was introduced in Uruguay in 2004 (Bianchi and Sánchez 2004). In Uruguay, this insect attacks mostly red gums belonging to the species E. tereticornis and E. camaldulensis, but it is considered a pest of secondary importance for Uruguayan forestry (Martínez et al. 2018b). Three years after this insect was reported, the parasitoid Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) was found in the country (Bianchi 2008). Interestingly, the adventitious introduction of P. bliteus has also been observed in other regions where the lerp psyllid has been introduced (Boavida et al. 2016; Caleca et al. 2011). No assessment of parasitisation rates has been made for this parasitoid in the field, to our knowledge. The extant two Australian species of psyllids recorded in Uruguay, Ctenarytaina spatulata Taylor and Blastopsylla occidentalis Taylor, represent no significant problem for Eucalyptus forestry, and to date, no efforts have been invested in their BC (FAO-MGAP 2006; Martínez et al. 2014a).

2.3.6  The Eucalypt Longhorned Borer Phoracantha semipunctata (F.) (Coleoptera: Cerambycidae) is a pest of several Eucalyptus species native to Australia (Wang 1995). It was first detected in South America in 1917, in Buenos Aires, and it reached Uruguay in 1932 (Morey and Porcile 2002; Porcile 1992). A relative species Phoracantha recurva Newman was first detected in December 1998 (Bianchi and Sánchez 1999b). This congener species also invaded other regions during the 1990s (Luhring et al. 2000).

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Female adults oviposit under the bark of the trunk and branches of susceptible trees, and the larvae make their way to the cambium by penetrating the bark. In heavy infestation, trees are debilitated or killed by ringing (Seaton et  al. 2015). Attacks by the eucalyptus longhorned borer intensify under water stress condition given that bark moisture content plays a critical role in the resistance of eucalyptus trees against colonisation by the larvae (Hanks et  al. 1991; Seaton et  al. 2015). Although it is considered a secondary pest in Uruguay, attacks can intensify in seasons affected by drought, as it was the case observed in the spring of 1999 to summer of 2000 (Morey et al. 2001). In 1992, the wasp Avetianella longoi Siscaro (Hymenoptera: Encyrtidae) was found parasitising eggs of P. semipunctata in Australia, becoming a potential BC agent for the eucalyptus longhorned borer (Luhring et al. 2000). Soon after the discovery, A. longoi was introduced in South Africa. In 1996, Uruguayan authorities explored the possibility of a parasitoid exchange collaboration with the Plant Protection Research Institute of Cape Town, South Africa. Uruguay offered to provide South Africa with    I. leucospoides for the BC of S. noctilio in exchange of getting  A. longoi. The details of this joint mission were reviewed by Tellechea (1999). Between November and December of 1996, pine trunks parasitised by S. noctilio from different parts of the country were taken to the laboratory of the DGF and placed in cages to collect the adults of I. leucospoides. Simultaneously, trunks of Eucalyptus were inspected in the field for eggs of Phoracantha spp. and taken to the laboratory to start a rearing of the longhorned borer. The rearing of Phoracantha was not successful initially, so eggs had to be collected from the field on several occasions or obtained from an experimental rearing set on the University of the Republic. The South African mission was led by Dr. Judy Moore from the Plant Protection Research Institute, who arrived in the country in January 1998 and stayed for 15 days. During this period, she transferred knowledge on rearing A. longoi. A total of 400 adult A. longoi were introduced from South Africa (Moore 1998). At the same time, adult wasps of I. leucospoides recovered from the rearing cages previously set were shipped to South Africa. A second shipment of wasps was sent a month later. The release of I. leucospoides was successful in South Africa. To release A. longoi in the field, the parasitoid was transported in two stadia: as parasitised eggs and adult wasps, on an approximate ratio of 2:3 (Tellechea 1999). To maximise the success of the establishment, sites with low risk of frost were chosen. The first release was made in a set of few points in the departments of Maldonado and Canelones. In January 1999, the first assessment of parasitism was done, detecting parasitisation rates above 50% (Tellechea 1999). Other natural enemies have been employed as BC agents for Phoracantha in other parts of the world. For instance, the Australian parasitoids Syngaster lepidus Brullé and Callibracon limbatus (Brullé) (Hymenoptera: Braconidae) were introduced in California to control P. semipunctata (Hanks et al. 2001). In Uruguay, a nematode was recovered from rearings of P. semipunctata and P. recurva, identified as a new species (Bianchi 2004). Additionally, strains of Beauveria bassiana were recovered from natural populations of the pest and tested in vitro for pathogenicity and virulence; one strain in particular showed an LD50 of 2.8 × 106 spores/mL at an

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LT50 of 8 days on P. recurva (Bettucci et al. 2006). However, no further studies were conducted, possibly given the low concern on this pest. In the last two decades, a more adjusted silvicultural control together with a better election on the species planted according to the site has diminished the incidence of the longhorned borer, given that this is a secondary pest.

2.3.7  T  wo Ongoing Programmes: Biological Control of the Bronze Bug and the Blue Gum Chalcid The bronze bug Thaumastocoris peregrinus Carpintero and Dellappe (Heteroptera: Thaumastocoridae) is an important eucalyptus pest worldwide that was first detected in Uruguay in 2008, attacking trees of several species of Eucalyptus (Martínez and Bianchi 2010). Soon after the report, the CECOPE asked for the development of a monitoring strategy for the bronze bug (Bianchi et al. 2008) by using yellow sticky traps to assess the distribution of the pest in the country. By 2009, the insect had only been introduced to a quarantine facility in South Africa but had not been released outside Australia yet, so Uruguay searched for partners in South America for introducing the pest in the region. A collaborative network of researchers and authorities of Argentina, Brazil, Chile and Uruguay and a minor participation of Paraguay and Bolivia was set with the help of two regional forums: the PROCISUR (http://www.procisur.org.uy) and the COSAVE. A regional project was developed aimed at coordinating research activities and facilitating the rapid exchange of the egg parasitoid Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae) among the parts, while the COSAVE redacted a regional plan for monitoring and management of the bronze bug (Martínez 2017). Uruguayan efforts focused on the setting up of a rearing system to multiply eggs of the bronze bug (Martínez et al. 2014b). In February 2013, a set of 2400 eggs of T. peregrinus potentially parasitised by C. noackae was taken from the Laboratory of Entomology of EMBRAPA in Curitiba, Brazil. Half of the shipment was immediately released, and the extant eggs were taken to the Laboratory of Entomology of INIA in Tacuarembó to start a massive rearing of the parasitoid. After 3 years of release and monitoring, data suggest that populations of C. noackae have been installed in at least four sites in the country, from where it is spreading (Martínez et al. 2018a). Emergence of the parasitoids in the field has reached a maximum of above 50% (Martínez et al. 2018a). On the first years after the detection of T. peregrinus, sets of egg clusters were left in the field to check for potential native parasitoids, and a prospection of other natural enemies was done, none of which was successful in detecting potential beneficial fauna. However, field observation accounted for several epizootic events, particularly in late summer; laboratory analysis of the infested bugs identified several strains of entomopathogenic fungi as causal agents of these epizooties (Corallo et al. 2019; Mascarin et al. 2012). Hence, a project started on 2012 aimed at the development of a biopesticide by using the most common strains attacking the

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bronze bug in the field (Simeto et al. 2012). A first prototype of this biopesticide is currently under evaluation (Abreo et al. 2019). The last BC programme started in the country concerns the management of the blue gum chalcid, Leptocybe invasa, which is perhaps a clear example of BC in the post-CBD era. The blue gum chalcid is one of the most invasive pests recorded in recent years. In less than a decade, this tiny gall former dispersed to four continents, after being detected for the first time in Israel in the year 2000 (Jorge et al. 2016). In Uruguay, it was first detected in 2011 (Jorge et al. 2016). Given that the country was monitoring the invasion of this pest since it was detected in Brazil in 2008 and based on the successful experience of the previous introduction of C. noackae, the members of the CECOPE agreed on starting a new mission to introduce the parasitoid Selitrichodes neseri Kelly and LaSalle (Hymenoptera: Eulophidae) that had been released and recovered in Brazil (Masson et al. 2017). In the context of a PhD, negotiations started with Brazil, to make an introduction of this parasitoid wasp from EMBRAPA, and administrative procedures started in the country. Unfortunately, the fact that Brazil included S. neseri in the list of native fauna after being recovered in the field would demand a new set of administrative procedures to comply with the requirements set by the CBD, and it would stretch the time for the introduction. Having Argentina introduced S. neseri successfully, a task force made by representatives of DGSA, DGF, INIA and UDELAR contacted the Argentinian authorities of the SENASA and the research team of the quarantine facility at INTA Castelar to arrange the preparation of a shipment of the parasitoid, given that the administrative procedures required less steps with this country. In February 2019, the Uruguayan mission travelled to INTA Castelar and assisted in the collection of S. neseri from galls previously brought from sites with occurrence of the parasitoid. Once the shipment was prepared, the Uruguayan researchers were taken to the border by officials of SENASA where they were received by representatives of the CECOPE. Part of the adult wasps contained in the shipment was immediately released in one commercial stand of E. grandis affected by L. invasa, while the extant material was taken to the laboratory in order to start a rearing of the BC agent. A new shipment is coordinated by September 2019 (Martínez et al. 2019).

2.4  Discussion Biological control has been a usual pest management strategy in Uruguayan forestry, and to date, almost all the forest insect pests considered of importance possess natural enemies that have been (or are being) introduced within the context of classical BC programmes. Messing and Brodeur (2018) enumerate three main challenges BC currently faces: a shift in public risk perception towards BC that implies a loss of confidence on the method, a regulatory overload that hampers the introduction of natural enemies and reduction in public resources devoted to BC. I will evaluate these challenges from a Uruguayan perspective in the following lines.

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The perception of BC as environmentally risky is not an issue in Uruguay. Public concern in the recent years deals more with an increasing use of agrochemicals as a result of agricultural intensification in the country, which may lead to environmental deterioration (https://www.elobservador.com.uy/nota/agroquimicos-un-mal-necesario-20161210500). Under this scenario, public opinion welcomes the use of BC (see, for instance, https://www.republica.com.uy/uruguay-apuesta-al-control-deplagas-agricolas-y-uso-de-controladores-biologicos-id714978/). Despite that, more emphasis must be put in increasing visibility and public awareness of BC as a reliable and sustainable strategy. The spread of the use of BC in forestry may serve as an interesting example to increase public awareness on the advantage of this pest management alternative. It is important to note that the national strategy defined for forest pest management considers BC as crucial and promotes the allocation of efforts and resources to increase public knowledge on BC (CECOPE 2012). The deployment of BC takes between 2 and 104 years after the pest report (or the discovery of a biocontroller), with an average (mean ± SE) of 28 ± 8 years (Garnas et al. 2012). In Uruguay, this figure has fluctuated between 4 (Anaphes nitens) and 8  years (Selitrichodes neseri), with an average of 6  ±  1  years. The major factor increasing the gap in the last decades has been undoubtedly the more difficult regulatory landscape the researchers have faced, particularly due to the absence of a local quarantine facility and the compliance to the CBD and the Nagoya Protocol. The Nagoya Protocol is a supplementary agreement to the Convention on Biological Diversity (CBD) that provides a framework for the effective implementation of the fair and equitable sharing of benefits resulting from the utilisation of genetic resources, including invertebrate BC agents (Mason et al. 2018). After the Protocol came into force on 12 October 2014, the collection and use of BC agents must be done in compliance with its specifications in the countries that are signatory to it. This new regulation, although based on good intentions (to grant the sovereign rights claimed by the countries over their genetic resources) has created several complications towards the implementation of BC programmes. For instance, when materials are subject to legislation, an a priori informed consent (PIC) must be obtained, and Mutually Agreed Terms (MAT) including the specific intended use, a Material Transfer Agreement (MTA) and, if possible, an Internationally Recognised Certificate of Compliance (IRCC) may be required (Smith et al. 2018). Given that Uruguay and the extant members of the COSAVE are parties of the Protocol, so as are strategic countries for the BC of forest pest such as Australia, South Africa and New Zealand, the additional burden imposed by the Nagoya Protocol may hamper the introduction (or exchange) of beneficial fauna by extending the administrative times for importation or generating difficulties in obtaining information on the different focal points (Smith et al. 2018). Additionally, the NPPO and the focal point of the Nagoya Protocol are provided by different governmental agencies in Uruguay (the DGSA and the DINAMA, respectively), so we urge the creation of a coordination space that could help in speeding up the communication between these agencies to minimise the administrative burden. The relative weight of forestry sanitary problems within the country’s priorities is still low, when compared with other sectors of the rural production, such as agriculture, fruticulture and cattle breeding (CECOPE 2012; Morey and Porcile

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2002). This lack of attention towards forest pest problems has also been identified as a weak point in other forestry countries, particularly in the Southern Hemisphere (Anderson et  al. 2017; Carnegie et  al. 2018; Yemshanov et  al. 2010) and has affected the capacity building in particular. Biological control agents have been introduced to the country from different origins (South Africa, Spain, Brazil, Argentina, New Zealand), none of which is the area of origin of the species imported. The main reason for not resourcing to native populations of natural enemies has been the lack of an official quarantine facility for entomophagous insects in Uruguay, a decision supported by the high investment in money and human resources that this type of highly specialised laboratories usually requires (Kenis et al. 2017). Given the important development of the forestry sector in the country, the relative importance of BC as a key pest management strategy on tree plantations and the actual scenario of global forest pest invasions, the establishment of a national quarantine facility is a question that is worth being revisited in Uruguay. Such facility would give more autonomy to the country to deal with new pests, and it also would help to speed up the time for the introduction of BC agents. Two important bottlenecks in capacity must be faced. First, correct taxonomical identification of both insect pests and natural enemies is crucial for the success of a BC programme. The situation is even more critical for hymenopteran parasitoids, a key group in BC (Bentancourt and Scatoni 2001). Uruguay faces the challenge of dealing with multiple species identifications in a country where the number of professionals devoted to taxonomy and even entomology is scarce. As a clear example, in a country where commercial tree plantations occupy more than a million hectares, only four professionals hold permanent positions as forest entomologists, considering universities, private companies and research institutes! The lack of specialised taxonomists may be solved in part by the establishment of a national reference biological collection for parasitoids and other natural enemies, but unfortunately, as it is the case in other countries, few efforts have been put on maintaining such collections (Bentancourt and Scatoni 2001). Alternatively, small independent collections already established in different institutions could be connected by means of a web portal. Additionally, new methods of identification by using molecular tools could be an interesting alternative to consider (Bilodeau et  al. 2019; Mapondera et  al. 2012). A second bottleneck also connected to the country’s scale is the rearing capacity. Biological control requires the massive rearing of the BC agents and generally also the targeted pest (Kenis et al. 2017; van Lenteren et  al. 2018). This usually implies important investments in infrastructure building and human resources that require collaborative efforts. An example of this was the installation of a centre (CEBIOF) that provided biological control services within the UDELAR and INIA campus in Tacuarembó that was opened from 2012 to 2017 (Torres et al. 2013). The CEBIOF is being revisited now in the context of a collaborative forestry consortium recently created with the participation of the forestry companies and two research institutes (http://www. inia.uy/estaciones-experimentales/direcciones-regionales/inia-direcci%C3%B3nnacional/Consorcio-para-la-investigacion-y-la-innovacion-forestal-del-Uruguay). Pre-establishment strategies are crucial if the focus will be to prevent the pests from entering the country or establishing in the plantations (Garnas et  al. 2012).

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However, inspection and quarantine capacities have been overwhelmed by the acceleration on global trade and the traffic of goods and wood packages worldwide (Anderson et  al. 2017; Augustin et  al. 2012; Garnas et  al. 2012; Meurisse et  al. 2019). In Uruguay, the development of a coordinated strategy for surveillance is currently under development (CECOPE 2012). The use of informatic tools, such as smartphone apps, and the involvement of citizen science are other ways to obtain valuable phytosanitary data that is being implemented in Uruguay with the use of the app P-FOR INIA. This smartphone app allows foresters and general public to send pest incidence report to a centralised database (Simeto et al. 2017). It has also been proposed to send reports on areas invaded by pests under BC, to facilitate the shipping of natural enemies on demand. Climate change can be a threat to BC by changing the phenology of the pest species or affecting the interspecific interactions between trophic compartments (Shields et al. 2019). Atmospheric changes linked to climate change can affect the emission of volatile organic compounds or VOC by plants (Peñuelas and Staudt 2010) which are used by forest insect pests, as well as their enemies to locate their host plants (Bouwer et al. 2014; Martínez et al. 2006, 2017). So, disruption of the efficacy of the parasitoid due to changes in the climatic regime can be expected. It is important to start assessing the effect of climate change on the efficacy of the BC agents currently active in our tree plantations even if that implies a national effort to develop reliable indicators for each pest-BC agent system. Last but not least, as it has been pointed out by many researchers, the immense demand to implement BC programmes in the current pest scenario exceeds the national capacities and requires the strength of coordinated international focus on monitoring, management and control of exotic insect pest of forestry (Garnas et al. 2012). Uruguay in particular requires such collaboration with other countries to achieve critical mass in resources and knowledge, given the small scale of the country, but in exchange, the country can offer its vast experience in international cooperation, especially at the regional scale. In the last century of BC in Uruguayan forest, such international collaboration relied mainly on personal contacts between academics and governmental agents and a small number of international collaborative efforts (Tellechea 1999; Trujillo 1963). However, this model of collaboration is inviable to date, given the extent of the invasion and the current international regulations (Garnas et al. 2012; Smith et al. 2018).

2.5  A  Wish List for the Future of Biological Control in Uruguay As a way to provoke further discussion, I identify some particular actions that would be desirable towards a further development of BC in Uruguay. 1. Create a centralised national biological collection of forestry pests and natural enemies (or a network of interconnected collections).

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2. Create a tool for documentation of programmes, experts, pests and natural enemies for forestry. 3. Build capacity on taxonomy and insect rearing through educational offer. 4. Consider the creation of national capacity for quarantine of entomophagous organisms. Acknowledgements  The author wants to thank the collaboration of the representatives of the CECOPE, providing public information and private reports.

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Martínez G, González A, Dicke M (2018b) Effect of the eucalypt lerp psyllid Glycaspis brimblecombei on adult feeding, oviposition-site selection, and offspring performance of the bronze bug, Thaumastocoris peregrinus. Entomol Exp Appl 166(5):395–401. https://doi.org/10.1111/ eea.12645 Martínez G, Jorge C, Escudero P, Martínez Haedo J, de los Santos M, Scoz R (2019) Hacia un programa de control biológico de la avispa agalladora del eucalipto. Revista INIA 56: 75–78 Mascarin GM, Duarte V d S, Brandão MM, Delalibera Í Jr (2012) Natural occurrence of Zoophthora radicans (Entomophthorales: Entomophthoraceae) on Thaumastocoris peregrinus (Heteroptera: Thaumastocoridae), an invasive pest recently found in Brazil. J Invertebr Pathol 110(3):401–404. https://doi.org/10.1016/j.jip.2012.03.025 Mason PG, Cock MJW, Barratt BIP, Klapwijk JN, van Lenteren JC, Brodeur J et al (2018) Best practices for the use and exchange of invertebrate biological control genetic resources relevant for food and agriculture. BioControl 63(1):149–154. https://doi.org/10.1007/s10526-017-9810-3 Mendel Z, Protasov A, La Salle J, Blumberg D, Brand D, Branco M (2017) Classical biological control of two Eucalyptus gall wasps; main outcome and conclusions. Biol Control 105:66–78. https://doi.org/10.1016/j.biocontrol.2016.11.010 Messing R, Brodeur J  (2018) Current challenges to the implementation of classical biological control. BioControl 63(1):1–9. https://doi.org/10.1007/s10526-017-9862-4 Meurisse N, Rassati D, Hurley BP, Brockerhoff EG, Haack RA (2019) Common pathways by which non-native forest insects move internationally and domestically. J Pest Sci 92(1):13–27. https://doi.org/10.1007/s10340-018-0990-0 Moore J (1998) Control biológico en Sud África. Uruguay Forestal 17:8–11 Morales Olmos V, Siry JP (2009) Economic impact evaluation of Uruguay forest sector development policy. J For 107(2):63–68 Morales Olmos V, Ansuberro J, Pintos M, Pérez G, Olmos VM, Ansuberro J et al (2018) Panorama empresarial del sector forestal uruguayo productor de Eucalyptus globulus. Agrociencia Uruguay 22(1):133–139. https://doi.org/10.31285/agro.22.1.14 Morey CS (1993) Detección y control de Sirex noctilio en Uruguay. Uruguay Forestal 6:6–9 Morey CS, Porcile JF (2002) Aspectos fitosanitarios del desarrollo forestal en Uruguay: Antecedentes históricos y una década de sucesos [Informe técnico]. MGAP-DGF, Montevideo, pp 1–33 Morey CS, Terra AL, Frioni MI (2001) Identificación de los taladros del eucalipto Phoracantha semipunctata (F.) y P. recurva (N.) (Coleoptera: Cerambycidae). Uruguay Forestal 26:4–7 Morey CS, Terra A, Frioni I (2002) Establecimiento de Psyllaephagus pilosus (Hymenoptera: Encyrtidae) en Uruguay. Forestal. Revista de la Sociedad de Productores Forestales de Uruguay 17:28–30 Nadel RL, Wingfield MJ, Scholes MC, Lawson SA, Slippers B (2012) The potential for monitoring and control of insect pests in Southern Hemisphere forestry plantations using semiochemicals. Ann For Sci 69(7):757–767. https://doi.org/10.1007/s13595-012-0200-9 OPYPA-MGAP (2018) Anuario OPYPA 2018. Montevideo, pp 1–667 Paine TD, Steinbauer MJ, Lawson SA (2011) Native and exotic pests of Eucalyptus: a worldwide perspective. Annu Rev Entomol 56:181–201 Penteado SRC, Oliveira EB, Iede ET (2008) Utilizaçao da amostragem seqüencial para avaliar a eficiência do parasitismo de Deladenus (Beddingia) siricidicola (Nematoda: Neotylenchidae) em adultos de Sirex noctilio (Hymenoptera: Siricidae). Ciência Florestal 18(2):223–231 Peñuelas J, Staudt M (2010) BVOCs and global change. Trends Plant Sci 15(3):133–144. https:// doi.org/10.1016/j.tplants.2009.12.005 Porcile JF (1992) El taladro del eucalipto Phoracantha semipunctata F. Uruguay Forestal 3:16–18 Porcile JF (1996) Manejo integrado de plagas. Uruguay Forestal 12:16–17 Porcile JF (1998) Ctenarytaina eucalypti (Maskell) Homoptera, Psyllidae. Uruguay Forestal 19:26 Protasov A, Blumberg D, Brand D, La Salle J, Mendel Z (2007) Biological control of the eucalyptus gall wasp Ophelimus maskelli (Ashmead): taxonomy and biology of the parasitoid species Closterocerus chamaeleon (Girault), with information on its establishment in Israel. Biol Control 42(2):196–206. https://doi.org/10.1016/j.biocontrol.2007.05.002

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Quang Thu P, Dell B, Burgess TI (2009) Susceptibility of 18 eucalypt species to the gall wasp Leptocybe invasa in the nursery and young plantations in Vietnam. ScienceAsia 35(2):113–117 Rebuffo S (1990) La “Avispa de la Madera” Sirex noctilio F. en el Uruguay. MGAP, Montevideo Ruffinelli A, Carbonell CS (1954) Segunda lista de insectos y otros artrópodos de importancia económica en el Uruguay. Universidad de la República, Facultad de Agronomía, Montevideo Seaton S, Matusick G, Ruthrof KX, Hardy GESJ (2015) Outbreak of Phoracantha semipunctata in response to severe drought in a Mediterranean Eucalyptus Forest. Forests 6(11):3868–3881. https://doi.org/10.3390/f6113868 Shields MW, Johnson AC, Pandey S, Cullen R, González-Chang M, Wratten SD, Gurr GM (2019) History, current situation and challenges for conservation biological control. Biol Control 131:25–35. https://doi.org/10.1016/j.biocontrol.2018.12.010 Simeto S, Lupo S, Bettucci L, Pérez C, Gómez D, Torres D et al (2012) Desarrollo de bioinsecticidas (hongos entomopatógenos) para el control de la chinche del eucalipto Thaumastocoris peregrinus (Núm. 703; p. 8). INIA, Tacuarembó Simeto S, Gómez D, Martínez G, Balmelli G (2017) Nuevo módulo de consulta de la aplicación P-FOR INIA: el avance de una herramienta interactiva. Revista INIA 49:38–39 Simó M, Laborda A, Jorge C, Castro M (2011) Las arañas en agroecosistemas: Bioindicadores terrestres de calidad ambiental. INNOTEC 6:51–55 Slippers B, Hurley BP, Wingfield MJ (2015) Sirex Woodwasp: a model for evolving management paradigms of invasive forest pests. Annu Rev Entomol 60(1):601–619. https://doi.org/10.1146/ annurev-ento-010814-021118 Smith D, Hinz H, Mulema J, Weyl P, Ryan MJ (2018) Biological control and the Nagoya Protocol on access and benefit sharing—a case of effective due diligence. Biocontrol Sci Technol 28(10):914–926. https://doi.org/10.1080/09583157.2018.1460317 Talbot PHB (1977) The Sirex-Amylostereum-Pinus association. Annu Rev Phytopathol 15:41–54 Tellechea N (1999) Intercambio de controladores biológicos con la República de Sudáfrica. Uruguay Forestal 20:10–11 Tellechea N (2008 febrero 18) Personal interview [Recorded] Tiscornia S, Lupo S, Corallo B, Sánchez A, Bettucci L (2014) Neotropical leaf-cutting ants (Acromyrmex spp.): biological control under laboratory and field conditions. Trends Entomol 10:55–62 Torres D, Martínez G, Pérez G (2013) Una nueva oferta en servicios tecnológicos: Centro de Bioservicios Forestales (CEBIOF). Revista INIA 33:60–62 Trujillo A (1963) Breve historia entomológica uruguaya. C&Cia, Montevideo van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63(1):39–59. https://doi.org/10.1007/s10526-017-9801-4 Wang Q (1995) A taxonomic revision of the Australian genus Phoracantha Newman (Coleoptera: Cerambycidae). Invertebr Syst 9:865. https://doi.org/10.1071/IT9950865 Watt MS, Kirschbaum MUF, Moore JR, Pearce HG, Bulman LS, Brockerhoff EG, Melia N (2019) Assessment of multiple climate change effects on plantation forests in New Zealand. Forestry 92(1):1–15. https://doi.org/10.1093/forestry/cpy024 Willoughby I, Wilcken CF, Ivey P, O’Grady K, Katto F (2009) FSC Guide to integrated pest, disease and weed management in FSC certified forests and plantations (FSC Technical Series Núm. 2009–001; p 19). Recuperado de Forest Stewardship Council website: www.fsc.oeg Wingfield MJ, Slippers B, Hurley B, Coutinho T, Wingfield B, Roux J (2008) Eucalypt pests and diseases: growing threats to plantation productivity. South For J For Sci 70(2):139–144. https:// doi.org/10.2989/SOUTH.FOR.2008.70.2.9.537 Yemshanov D, Koch FH, Ben-Haim Y, Smith WD (2010) Detection capacity, information gaps and the design of surveillance programs for invasive forest pests. J Environ Manag 91(12):2535– 2546. https://doi.org/10.1016/j.jenvman.2010.07.009

Chapter 3

Past and Current Strategies for the Control of Leaf-Cutting Ants in Brazil Terezinha Maria Castro Della Lucia and Karina Dias Amaral

3.1  Introduction Leaf-cutting ants belong to the tribe Attini and subtribe Attina. They cultivate fungus for food, especially to feed their larvae  (Hölldobler and Wilson 2009). Unlike other fungus-growing ants, leaf-cutting ants harvest fresh parts of plants to serve as substrate for their symbiotic fungus, Leucocoprinus gongylophorus. The taxonomy of this basidiomycete was difficult to establish because it does not sporulate; instead, the fungus produces gongylidia (fruiting bodies), which the ants cut and ingest (Johnson 1999). Leaf-cutting ants are classified into two genera, Atta and Acromyrmex, considered the most important and damaging of the fungus-growing genera. Fungus-­ growing Trachymyrmex and Sericomyrmex have also been reported to cause damage to plants, such as Eucalyptus seedlings. Atta and Acromyrmex live in underground nests formed by various chambers connected by galleries that open to the surface. The exterior, visible part of the nest consists of a mound of loose soil resulting from material extracted during tunneling and chamber formation. Nests can reach 7 m in depth, as observed in Atta laevigata (Moreira et al. 2004). The workers of Atta have three pairs of dorsal spines and show great polymorphism among castes. The foundation of the colony is carried out by a sole queen, and it remains monogynic. Nest founding is claustral; that is, after the nest is established, the queen seals herself in a chamber to rear her first brood (Araújo et  al. 2011). Thirty-six months later, the first winged individuals (both males and females) emerge from the nest and mate, after which they drop to the ground, lose their wings, and attempt to start new nests.

T. M. C. Della Lucia (*) · K. D. Amaral Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil e-mail: [email protected] © Springer Nature Switzerland AG 2020 S. A. Estay (ed.), Forest Pest and Disease Management in Latin America, https://doi.org/10.1007/978-3-030-35143-4_3

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Acromyrmex workers have four to five pairs of dorsal spines. Polymorphism among castes is less noticeable than in Atta. Nests may be founded by one (monogyny) or several (polygyny) queens, and nest founding is semi-claustral (Araújo et al. 2011); that is, the queen forages for plant material for raising the fungus (Rissing et al. 1986). The nests are, in general, smaller (fewer chambers) and less deep than those of Atta. These individuals may be beneficial to ecosystems because they promote soil mixture, nutrient cycling, and mineralization of organic matter. Additional information on the benefits provided by leaf-cutting ants is given by Della Lucia and de Souza (2011). However, the habit of harvesting various types of fresh plants makes them severe pests of planted forests, agricultural fields, and grazing lands. Thus, their control becomes necessary. In Colombia, leaf-cutting ants are also regarded as urban pests, especially Atta cephalotes (Montoya-Lerma et al. 2012). This species has invaded plazas, playgrounds, streets, and even homes. Colonies can cause serious structural damage to buildings and infrastructure. Serrano et al. (1993) reported that, in Colombia, the establishment of cattle farms is frequently problematic because of the high density of A. cephalotes nests in the area. Leaf-cutting ants are native to South America and occur from the southern United States to Argentina. At present, 19 Atta species and 32 Acromyrmex species are described (Baccaro et al. 2015). Leaf-cutting ants do not occur in Chile, probably because the Andes is too great a barrier. In Argentina, Acromyrmex is more common than Atta (18 species versus 3) (Table  3.1). Acromyrmex lobicornis is the major pest of agricultural crops and planted forests. In regions where the native vegetation was cleared for conifers, nest density is considerably higher (Pérez et al. 2011). Damage by leaf-cutting ants was first reported in 1909; however, quantitative data on the losses inflicted by these pests in that period are not found in the literature (Bonetto 1959). Since 1940, Paraguay farmers are advised to eliminate all Atta and Acromyrmex nests that appear in their properties (Cassanelo 1998). Cassanelo (1998) tells of the inordinate damages caused by the insects but does not quantify the losses (Fowler and Robinson 1979). The author reports that leaf-cutting ants are mainly found in planted forests, fruit tree coppices, and urban areas and that the presence of ants in grasslands restricts use for cattle production and reduces the selling price of rural properties. In Uruguay, Acromyrmex leaf cutters are the most destructive and cause great economic losses (Zolessi and Philippi 1998), but no quantitative data are available. Acromyrmex lundi was reported as the most prejudicial leaf-cutting species (Zolessi and Gonzáles 1978; Zolessi and Philippi 1998). Three Atta and three Acromyrmex species (Table 3.1) are found in Venezuela, and all are considered pests of agri-silviculture systems. Atta laevigata is the most important; the damage is inflicted to pine plantations, generally affecting seedlings and young trees (Hernández and Jaffe 1995). In Brazil, reports on leaf-cutting ants began to appear a few years after the country was discovered. In 1560, the Jesuit priest Joseph of Anchieta claimed that “the ants (saúvas) can destroy a plantation from night to morning.” Several naturalists

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Table 3.1  Main species of leaf-cutting ants (Atta and Acromyrmex) found in the New World Genus Atta

Species A. bisphaerica (Forel, 1908) A. capiguara (Gonçalves, 1944) A. cephalotes (Linnaeus, 1758)

Distribution Brazil Brazil Brazil, Colombia, Ecuador, French Guiana, Guyana, Mexico, Nicaragua, Peru, Suriname, Venezuela A. colombica (Guérin-­Méneville, Colombia, Costa Rica, Ecuador, Panama 1844) A. laevigata (Smith, F. 1858) Brazil, Venezuela A. mexicana (Smith, F. 1858) El Salvador, Mexico, USA A. opaciceps (Borgmeier, 1939) Brazil A. sexdens (Linnaeus, 1758) Argentina, Brazil, French Guiana, Paraguay, Peru, Suriname, Venezuela A. texana (Buckley, 1860) Mexico, USA A. vollenweideri (Forel, 1893) Argentina, Bolivia, Brazil, Paraguay, Uruguay Acromyrmex Ac. ambiguus (Emery, 1888) Argentina, Brazil Ac. aspersus (Smith, F. 1858) Argentina, Brazil Ac. balzani (Emery, 1890) Argentina, Bolivia, Brazil, Paraguay, Venezuela Ac. coronatus (Fabricius, 1804) Argentina, Bolivia, Brazil, Costa Rica, Paraguay, Peru Ac. crassispinus (Forel, 1909) Argentina, Brazil, Paraguay, Uruguay Ac. disciger (Mayr, 1887) Brazil Ac. echinatior (Forel, 1899) Mexico, Panama Ac. fracticornis (Forel, 1909) Argentina, Brazil, Paraguay Ac. heyeri (Forel, 1899) Argentina, Brazil, Paraguay, Uruguay Ac. hispidus (Santschi, 1925) Argentina, Brazil, Peru Ac. landolti (Forel, 1885) Colombia, Peru Ac. laticeps (Emery, 1905) Argentina, Brazil, Peru Ac. lobicornis (Emery, 1888) Argentina, Bolivia, Brazil, Paraguay, Uruguay Ac. lundii (Guérin-­Méneville, Argentina, Bolivia, Brazil, Mexico, Paraguay, 1838) Uruguay Ac. niger (Smith, F. 1858) Brazil Ac. octospinosus (Reich, 1793) Brazil, Colombia, Cuba, French Guiana, Mexico, Venezuela Ac. rugosus (Smith, F. 1858) Argentina, Bolivia, Brazil, Colombia, Paraguay, Peru Ac. striatus (Roger, 1863) Argentina, Brazil, Paraguay, Uruguay Ac. subterraneus (Forel, 1893) Argentina, Brazil, Paraguay, Peru Ac. versicolor (Pergande, 1894) USA Source: Delabie et al. (2011)

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declared that “either the country defeats the ant or the ant destroys the country,” “Brazil is a very large anthill,” and “saúva is Brazil’s king” (Mariconi 1970). Most of the damage estimates for the country are provided by the forest sector. A study stated that 30% of forest management costs are attributed to ant detection and control. Previous reports on tree defoliation estimated that about US$ 8.20 is lost for every tree killed by ants (Della Lucia and de Souza 2011). A reduction of 11 mm in diameter growth and of 0.7 m in height growth resulted from the total defoliation of a young tree, which represents a loss of 13% of the final volume of the tree (Oliveira 1996). In this chapter, we review the various detrimental aspects of leaf-cutting ant behavior in Brazil, the state of the art of their control, and the possible use of new alternatives in the future.

3.2  Control of Leaf-Cutting Ants 3.2.1  History of Ant Control Methods Control attempts date back to the earliest recognition of leaf cutters as pests. The first products used were homemade recipes containing arsenicals, sulfur, chlorates, and highly toxic fumigants. The formulae included dry and wet powders, emulsions, toxic baits, and thermal fog. Details are given in Mariconi (1970). From 1965 to 1993, ants were controlled almost exclusively with granulated baits containing dodecachlor, considered efficient and of low cost (Della Lucia 1993). During these almost 30 years, methyl chloride and chlorate powder were also used. With the ban of dodecachlor in 1993, granulated baits began to contain mainly sulfluramid as active ingredient, followed by fipronil and chlorpyrifos. Deltamethrin was the recommended active ingredient for powders and chlorpyrifos for thermal fogging formulations. During the post-dodecachlor period, the search for alternative control methods intensified. The number of studies on toxic plants increased. Sesame (Sesamum indicum), sweet potato (Ipomoea batatas), and castor bean (Ricinus communis) were tested against the ants. Details on the various plants tested can be found in Bueno and Bueno (2011). Studies on parasitoid species identification and characteristics, parasitism rates, and population dynamics were carried out to investigate their potential as alternative control methods for leaf-cutting ants  (Bragança et al. 2002; Erthal and Tonhasca 2000; Tonhasca and Bragança 2000). Since 1922, several works were, and still are, conducted using parasitoids. An extensive review of the subject was performed by Bragança (2011). Predators such as the beetle Canthon virens and other ant species and nematodes received very little attention, however. The use of entomopathogenic fungi as biological control agents in the field has been also investigated, to a great extent, since 1988 (Diehl-Fleig et al. 1988).

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The search for ant pheromones intensified since the trail pheromone discovery in leaf cutters in 1959 (Sudd 1959). The use came in 1978, in an attempt to use the brood pheromone as a brood controlling substance (Robinson and Cherrett 1978). In this interim, we can conclude confidently that researches have had, as main concern, the reduction of the quantity of active ingredients in baits together with the use of products with lesser environmental impact. In forest companies, we notice the improvement of monitoring techniques, based on the pioneer work published in 1993 (Oliveira et al. 1993). As a consequence of all this, the amount of chemicals shrank. This was no doubt a result of the pressure exerted by the conscience and the need for preserving the habitats of the planet.

3.2.2  Current Control Strategies Here, we discuss the events of the past 5–6 years. Recent data on losses incurred from these pests revealed that colonies of Atta spp., in densities greater than 80 nests, can reduce Eucalyptus wood production by more than 50% (Zanetti et  al. 2003). Leaf-cutting ants were reported to kill up to 14% of trees in a Eucalyptus plantation, resulting in a loss of R$ 19.00 (US$ 4.87) for each tree attacked (Della Lucia and de Souza 2011). In Pinus taeda forests, plants severely defoliated by Acromyrmex spp. in the early stages of development can present losses of 13.3% in height growth and 20% in diameter growth (Reis Filho et al. 2011). In 2017, our research group carried out a survey among reforestation companies on the status of ants as pests and the control measures they used. The companies stated unanimously that ants are still a serious nuisance. Some even declared that leaf-cutting ants represented their major entomological problem. In addition, the companies reported that pest monitoring helped reduce losses. Several companies related problems associated with the lack of labor skilled in ant combat. They reported that training was insufficient because of the high turnover rate among workers, especially of contract workers. The number of people involved in fighting ants varied greatly: from 65 workers to supervise 73,000 infested ha/year to 200 workers to supervise 80,000 infested ha/year. The number and size of nests per hectare also varied greatly. Among the surveyed forest companies, as little as 25–30 m2 nests/ha to 100 m2 nests/ha were reported. Nest density can increase substantially the costs involved in pest control, varying from R$ 15.00/ha (US$ 3.84/ ha) to R$ 420.00/ha (US$ 107.69/ha), considering that sulfluramid baits cost R$ 7.00/kg (US$ 1.79/kg). According to  Zanuncio et  al. (2016), nest density in Eucalyptus forests in Minas Gerais varies from 13.4 to 39.2 m2 nests/ha. In addition, leaf-cutting ants attack several crops, including citrus, cocoa, and sugarcane. The facts that a single Atta nest can lead to a yield loss of 3.2 t/ha in a sugarcane plantation (Precetti et al. 1988) and that Brazil grows eight million ha of sugarcane (Companhia Nacional de Abastecimento [CONAB] 2018) provide an indication of the extent of agricultural losses caused by leaf-cutting ants in the country.

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Pastures, too, are damaged by these pests. A recent survey identified about 4600 nests of two Acromyrmex species per hectare of pasture in the state of Mato Grosso (Dr. Norivaldo dos Anjos, 2017, personal communication, Department of Entomology, UFV, Viçosa, MG, Brazil). A rather old article reported that ten nests of leaf cutters may mow some 25 kg of grass each day, thus reducing the carrying capacity of the plot to 1.2 heads of cattle per hectare. If so, the loss in cattle production is enormous, considering that it can reach 2.5 heads in very good plots. It should be mentioned, however, that there could be other variables interacting with vegetation cut to cause such a loss. For example, the nutritional quality and the density of forage grass are also important. It should be pointed out that there exists in the market no specific bait for grass cutters. Baits available in the market use citrus pulp as the main attractant, but this does not favor their transportation by ants that cut only monocotyledon plants. Some other attractants such as Hyparrhenia rufa (“Capim-jaraguá”) were tested and showed promising results but still remain unavailable for field use (Lima et al. 2003). There are no specific baits for control of ants in pastures. Commercially available baits contain citrus pulp as attractant and therefore are not likely to be well transported by ants that cut only monocotyledon plants. Despite the promising results obtained with Hyparrhenia rufa (jaragua grass) as attractant, baits targeting grass-­ cutter ants remain unavailable for field use.

3.2.3  Current Control Methods Control methods for leaf cutters include granulated baits, dry powders, and thermal fogging. Chemicals approved in Brazil for use in baits are sulfluramid, fipronil, and Tephrosia. This last formicide is prepared from the plant Tephrosia candida, native to Asia. Deltamethrin is available as dry powder, permethrin in a concentrated form for thermal fogging, and chlorpyrifos as thermal fogging and liquid electric repellent. Physical control methods have changed little over the years. In small properties, ant nests are commonly destroyed by digging. Old car tires used to be filled with water and placed around trees as a physical barrier to ants, but this practice fell into disuse because it favored the multiplication of Aedes aegypti and other mosquitoes. Nowadays, plastic bottles are sometimes cut in half, filled with water and detergent, and placed around trunks to prevent ants from crawling up the tree. Gels, greases, sticky materials, and other artifacts are used in some small areas, mostly in orchards. Formifita was introduced into the market about 3  years ago. It consists of an ultraviolet (UV)-resistant plastic strip with a sponge material on one side. The strip is wrapped around the trunk of a tree to serve as an obstacle to climbing ants. As with other physical barriers, the position of Formifita on the trunk needs to be carefully considered; otherwise, ants may get around the obstacle or may reach the leaves of the plant. Physical barriers need to be frequently inspected, as fallen leaves and branches, dirt, and dead insects may create “bridges” that allow ants to cross the barriers.

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3.2.4  A  Reflection on Control Methods and Future Perspectives A comparison of the products available for control of leaf-cutting ants soon after the prohibition of dodecachlor (1993) with those currently available revealed that little changed during this period (Table 3.2). Several aspects are considered here to explain the limitations in developing control strategies for leaf cutters. Ants are social insects and thus possess a series of innate behaviors that favor their adaptation. Their sophisticated communication system based on pheromone, touch, and sound signals is a barrier to their control. Investigation on pheromones of leaf-cutting ants persists; however, there is still a long way until this control strategy becomes available for field usage. One of the main reasons for this is the low number of researchers in this specific area throughout the world in addition to the lack of knowledge on leaf-cutting ant semiochemicals. The defense system that includes immune defense and hygienic manners, besides physical resistance, also contributes to an increase of the protection of these individuals against harsh conditions. Moreover, the “chemical shield” that includes the production of antibiotics by the metapleural  (Fernandez-Marin et al. 2006) and mandibular glands (Marsaro Júnior et al. 2001) cannot be disdained. The association with the symbiotic fungus and the fact that a diverse microbiota occurs in the symbiosis causes difficulty in combating the insects. Compounds produced by that microbiota are just beginning to be discovered, and their roles inside the nest, on the colony, and on the total association are far from complete elucidation. Studies on waste produced by leaf-cutting ants can be found in the literature (Bot et al. 2001; Farji-Brener and Sasal 2003; Zeh et al. 1999; Lacerda 2011; Lacerda et al. 2011). A few of them aim to understand the properties of this material for beneficial use to plants (Souto and Sternberg 2011). The great majority of studies investigated the relationship between waste handling habits and strategies used by ants to avoid colony contamination by pathogens  (Arenas and Roces 2016; Table 3.2  Products approved for control of leaf-cutting ants in the past (1993) and in the present (2019) Past (1993) Active ingredient Sulfluramid Fipronil Chlorpyrifos Deltamethrin

Formulation Granulated bait Granulated bait Granulated bait Dry powder, thermal fogging

Present (2019) Active ingredient Sulfluramid Fipronil Chlorpyrifos Deltamethrin

Formulation Granulated bait Granulated bait Thermal fogging, liquid electric repellent Dry powder, thermal fogging

Tephrosia Permethrin

Granulated bait Thermal fogging

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Lacerda et al. 2010a, b). It seems that the waste produced by the colony provides cues for recognition of harmful substrates (Arenas and Roces 2017). Investigation of control agents that could go unnoticed in refuse piles has not yielded successful results (Hughes et al. 2004; Lacerda et al. 2006; Ortiz and Camargo-Mathias 2006). The ants’ ability to learn and select which plants to harvest makes it even more difficult to combat them. Olfactory and gustatory stimuli from substrates deemed inadequate for the fungal garden are learned by ants, and these materials are avoided in subsequent harvests (Saverschek and Roces 2011). A novel control strategy has been aimed at disrupting ant digestive enzymes, such as laccases (De Fine Licht et al. 2013). However, this research is still at a preliminary stage. The reproductive strategy of leaf cutters has not been completely understood. For instance, the mechanism that triggers the nuptial flight is still mysterious, as is the existence of a messenger (a pheromone or another information-bearing signal) that acts on sexual attraction. The structure of the nest itself, with its array of underground chambers and galleries, hinders insecticide application and proper distribution inside the nest. To this should be added the gaps in the knowledge of leaf cutters, which span from taxonomy (for instance, of Acromyrmex) to bioecology, from nest size estimation to insecticide application methods (Della Lucia et al. 1995). The efficiency of control methods is decreased by the lack of knowledge of workers on how to apply formicides. In most cases, this is the result of high turnover rates, which can be as high as 40% per year. There are yet other challenges to researchers in the field of ant control. Most research groups are concentrated in southeastern Brazil, and the physical distance between any two groups is more than 200 km (Fig. 3.1). The lack of technically and scientifically qualified personnel adds to this difficulty. Most studies are conducted by graduate students in public universities. Projects are frequently discontinued because of the lack of interested students or because of time and money constraints. Research funds are scarcer now than in the past. In 2014, the Brazilian Ministry of Science, Technology, and Innovation allocated R$ 8 billion (US$ 2.05 billion) for scientific development. In 2018, this value plunged to R$ 0.26 billion (US$ 0.06 billion) (Portal da Transparência, Controladoria Geral da União [CGU] 2019). As very few research projects are financed by private companies, little investment is made in the field of leaf-cutting ant research. Currently, the most effective means of controlling leaf-cutting ants are chemical, either in the form of baits, dry powders, or emulsified liquids. Active ingredients are limited to a few compounds. As a matter of fact, sulfluramid has been proscribed and is in the second deferral period. Sooner or later, it will be removed from the market. The search for novel formicides continues. Plants that contain toxic and attractive molecules have been investigated. The search for entomopathogenic fungi such as Beauveria, Metarhizium, and Aspergillus will also continue, as will the search for fungi that would compete (e.g., Trichoderma) with the symbiotic, for parasitic fungi such as Escovopsis, for

3  Past and Current Strategies for the Control of Leaf-Cutting Ants in Brazil

39

Fig. 3.1  Distribution of research groups working on leaf-cutting ants in Brazil

endophytic fungi, etc. (Pagnocca et al. 2011). Escovopsis sp. is known as a parasite fungus exhibiting fast growth and which causes persistent infection (Currie 2001). The antagonism of these filamentous fungi and their metabolites against the symbiotic fungus of leaf-cutting ants has already been demonstrated. They also indeed show potential to be used in biological control of leaf-cutting ants  (Bizarria et al. 2018).

40

T. M. C. Della Lucia and K. D. Amaral

Natural enemies, other than parasitoids, are being studied, rather sporadically (Araújo et  al. 2011). The work with parasitoids is advancing but not in a high pace (Bragança et al. 2016; Farder-Gomes et al. 2017). More knowledge is needed on the reproductive characteristics of parasitoids for their mass rearing in the laboratory and subsequent dispersal in the field. The search for immune suppressors has been conducted to verify if there are applications for them in controlling leaf cutters. The cyclosporine, for example, favors the pathogenic action of the fungus Metarhizium anisopliae because it reduces the immune capacity of leaf-cutting ants (Dornelas et al. 2017). The combination of immunosuppressants and opportunistic fungi can become a promising control method. More research is needed on the action of these compounds. Recent studies on azadirachtin showed its effect on the oviposition of A. sexdens queens. The compound reduces egg size by decreasing reserve protein deposition. In addition, it affects the synthesis of vitellogenin, a precursor of the major protein found in the yolk. The negative effect of azadirachtin on the reproductive capacity of ant queens indicates that it might be valuable in controlling the insects (Amaral et al. 2018). The use of viruses and the development of resistant plant species remain terra incognita. In the integrated management of leaf-cutting ants, it is important to highlight the advance in monitoring tools with the use of drones, geoprocessing, and other specialized software (Zanetti 2011). However, it still lacks a greater integration in control tactics. To date, there are no advanced, well-established methods of fighting leaf-cutting ants. Therefore, we believe that future generations of myrmecologists, agronomists, and forest engineers will be faced with a real challenge of controlling leaf-cutting ants with both efficiency and environment cleaninless. Furthermore, greater effort is needed in the implementation of integrated pest management principles.

References Amaral KD, Martínez LC, Pereira Lima MA et al (2018) Azadirachtin impairs egg production in Atta sexdens leaf-cutting ant queens. Environ Pollut 243:809–814 Araújo MS, Pereira JMM, Gandra LC et al (2011) Predadores e outros organismos associados aos ninhos de formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 311–320 Arenas A, Roces F (2016) Learning through the waste: olfactory cues from the colony refuse influence plant preferences in foraging leaf-cutting ants. J Exp Biol 219:2490–2496 Arenas A, Roces F (2017) Avoidance of plants unsuitable for the symbiotic fungus in leaf-cutting ants: learning can take place entirely at the colony dump. PLoS One 12(3):1–16 Baccaro FB, Feitosa RM, Fernandez F et al (2015) Guia para os gêneros de formigas do Brasil. Editora INPA, Manaus Bizarria R, Moia IC, Montoya QV et al (2018) Soluble compounds of filamentous fungi harm the symbiotic fungus of leafcutter ants. Curr Microbiol 75:1602–1608 Bonetto AA (1959) Las hormigas ‘cortadoras’ de la provincia de Santa Fe (Atta y Acromyrmex). Ministerio de Agricultura y Ganadería, Dirección General de Recursos Naturales, Argentina

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Bot ANM, Currie CR, Hart AG et al (2001) Waste management in leaf-cutting ants. Ethol Ecol Evol 13:225–237 Bragança MAL (2011) Parasitóides de formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-­ cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 321–343 Bragança MAL, Tonhasca A Jr, Moreira DDO (2002) Parasitism characteristics of two phorid fly species in relation to their host, the leaf-cutting ant Atta laevigata (Smith) (Hymenoptera: Formicidae). Neotrop Entomol 31:241–244 Bragança MAL, Arruda FV, Souza LRR et al (2016) Phorid flies parasitizing leaf-cutting ants: their occurrence, parasitism rates, biology and the first account of multiparasitism. Sociobiology 63:1015–1021 Bueno OC, Bueno FC (2011) Plantas inseticidas: perspectivas de uso no controle de formigas-­ cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 359–372 Cassanelo AML (1998) As formigas cortadeiras no Paraguai. In: Filho BE, Mariconi FAM, Fontes LR (eds) Anais de Simpósio sobre formigas cortadeiras do Mercosul. FEALQ, Piracicaba, pp 77–83 Companhia Nacional de Abastecimento (2018) Acompanhamento da safra brasileira: cana-de-­ açúcar, vol 5. Safra 2018/19 N3—Terceiro levantamento Currie CR (2001) Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128:99–106 De Fine Licht HH, Schiott M, Rogowska-Wrzesinska A et al (2013) Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proc Natl Acad Sci U S A 110(2):583–587 Delabie JHC, Alves HSR, Reuss-Strenzel GM et al (2011) Distribuição das formigas-­cortadeiras dos gêneros Acromyrmex e Atta no Novo Mundo. In: Della Lucia TMC (ed) Formigas-­ cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 80–101 Della Lucia TMC (1993) As formigas cortadeiras. Folha de Viçosa, Viçosa Della Lucia TMC, de Souza DJ (2011) Importância e história de vida das formigas–cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 13–26 Della Lucia TMC, Oliveira MA, Araújo MS et al (1995) Avaliação da não preferência da formiga cortadeira Acromyrmex subterraneus subterraneus Forel ao corte de Eucalyptus. Rev Árvore 19(1):92–99 Diehl-Fleig E, da Silva ME, Pacheco MRM (1988) Testes de patogenicidade dos fungos entomopatogênicos Beauveria bassiana e Metarhizium anisopliae em Atta sexdens periventris (Santschi, 1919) em diferentes temperaturas. Cienc Cult 40:1103–1105 Dornelas ASP, de Almeida Sarmento R, Pedro-Neto M et al (2017) Susceptibility of Atta sexdens worker ants treated with the immunosuppressant Sandimmun Neoral to Metarhizium anisopliae. Pesq Agrop Bras 52:133–136 Erthal M, Tonhasca A (2000) Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leaf-cutting ant Atta laevigata. Entomol Exp Appl 95:71–75 Farder-Gomes CF, Oliveira MA, Gonçalves PL et al (2017) Reproductive ecology of phorid parasitoids in relation to the head size of leaf-cutting ants Atta sexdens Forel. Bull Entomol Res 4:1–6 Farji-Brener AG, Sasal Y (2003) Is dump material an effective small-scale deterrent to herbivory by leaf-cutting ants? Ecoscience 10:151–154 Fernandez-Marin H, Zimmerman JK, Rehner SA et al (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc Biol Sci 273(1594):1689–1695 Fowler HG, Robinson SW (1979) Field identification and relative pest status of Paraguayan leaf-­ cutting ants. Turrialba 29:11–16 Hernández JV, Jaffe K (1995) Dano econômico causado por populações de formigas Atta laevigata en plantações de Pinus caribaea Mor. elementos para o manejo da praga. An Soc Entomol Bras 24:287–298 Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. W.W. Norton & Company, New York

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Hughes WOH, Thomsen L, Eilenberg J et al (2004) Diversity of entomopathogenic fungi near leaf-­ cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertebr Pathol 85:46–53 Johnson J (1999) Phylogenetic relationship within Lepiota sensu lato based on morphological and molecular data. Mycologia 91(3):443–458 Lacerda FG, Della Lucia TMC, Lima ER et  al (2006) Waste management by workers of Atta sexdens rubropilosa (Hymenoptera: Formicidae) in colonies supplied with different substrates. Sociobiology 48:165–173 Lacerda FG, Della Lucia TMC, Pereira OL et al (2010a) Mortality of Atta sexdens rubropilosa (Hymenoptera: Formicidae) workers in contact with colony waste from different plant sources. Bull Entomol Res 100:99–103 Lacerda FG, Della Lucia TMC, Serrão JE et al (2010b) Morphometry of the metapleural gland of workers engaged in different behavioral tasks in the ant Atta sexdens rubropilosa. Anim Biol 60:229–236 Lacerda FG, Della Lucia TMC, de Souza DJ (2011) Biologia comportamental de operárias do lixo das colônias de formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 226–235 Lima CA, Della Lucia TMC, Guedes RNC et al (2003) Desenvolvimento de iscas granuladas com atraentes alternativos para Atta bisphaerica Forel, (Hymenoptera: Formicidae) e sua aceitação pelas operárias. Neotrop Entomol 32:497–501 Mariconi FAM (1970) As saúvas. Agronômica Ceres, São Paulo Marsaro Júnior AL, Della Lucia TMC, Barbosa LCA et al (2001) Efeito de secreções da glândula mandibular de Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) sobre a germinação de conídios de Botrytis cinerea Pers. Neotrop Entomol 30:403–406 Montoya-Lerma J, Giraldo-Echeverri C, Armbrecht I et  al (2012) Leaf-cutting ants revisited: towards rational management and control. Int J Pest Manag 58:225–247 Moreira AA, Forti LC, Andrade APP et al (2004) Nest architecture of Atta laevigata (F Smith, 1858) (Hymenoptera: Formicidae). Stud Neotrop Fauna Environ 39:109–116 Oliveira MA (1996) Identificação de formigas-cortadeiras e efeito do desfolhamento simulado em plantios de Eucalyptus grandis. Thesis, Universidade Federal de Viçosa, Viçosa Oliveira AC, Barcelos JAV, Moraes EJ et al (1993) Um estudo de casos: o sistema de monitoramento e controle de formigas cortadeiras na Mannesmann Fi-El Florestal Ltda. In: Della Lucia TMC (ed) As formigas cortadeiras. Folha de Viçosa, Viçosa, pp 242–255 Ortiz G, Camargo-Mathias MI (2006) Morpho-physiological differences of the spermatheca of Attini ants (Hymenoptera: Myrmicinae). Am J Agric Biol Sci 1(4):58–65 Pagnocca FC, Rodrigues A, Bacci M Jr (2011) Microrganismos associados às formigas-­cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 262–283 Pérez SP, Corley JC, Farji-Brener AG (2011) Potential impact of the leaf-cutting ant Acromyrmex lobicornis on conifer plantations in northern Patagonia, Argentina. Agric For Entomol 13:191–196 Portal da Transparência-Controladoria Geral da União (2019) Execução de despesas por área de atuação. Portal da transparência Precetti AACM, Oliveira JE, Palini JR (1988) Perdas de produção em cana-de-açúcar causadas pela saúva mata-pasto, Atta bisphaerica. Parte I Boletim Técnico Copersucar, Piracicaba 42:19–26 Reis Filho W, Santos F, Strapasson P et al (2011) Danos causados por diferentes níveis de desfolha artificial para simulação do ataque de formigas cortadeiras em Pinus taeda e Eucalyptus grandis. Pesqui Florest Bras 31:37–42 Rissing SW, Johnson RA, Pollock GB (1986) Natal nest distribution and pleometrosis in the desert leaf-cutter ant Acromyrmex versicolor (Pergande) (Hymenoptera: Formicidae). Psyche (New York) 93:177–186 Robinson SW, Cherrett JM (1978) The possible use of methyl 4-methylpyrrole-2-carboxylate, an ant trail pheromone, as a component of an improved bait for leaf-cutting ant (Hymenoptera: Formicidae) control. Bull Entomol Res 68:159–170

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Saverschek N, Roces F (2011) Foraging leafcutter ants: olfactory memory underlies delayed avoidance of plants unsuitable for the symbiotic fungus. Anim Behav 82(3):453–458 Serrano MS, Lapointe SL, Villegas A (1993) Caracterización del daño de la hormiga cortadora de pastos Acromyrmex landolti (Forel) (Hymenoptera: Formicidae) sobre el establecimiento de Andropogon gayanus em los Llanos Orientales de Colombia. Rev Colomb Entomol 19:21–26 Souto LS, Sternberg L (2011) Ciclagem de nutrientes por formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 249–261 Sudd JH (1959) Interaction between ants on a scent trail. Nature 183:1588 Tonhasca A, Bragança MAL (2000) Forager size of the leaf-cutting ant Atta sexdens (Hymenoptera: Formicidae) in a mature eucalyptus forest in Brazil. Rev Biol Trop 48:983–988 Zanetti R (2011) Amostragem e determinação do nível de dano econômico de formigas-cortadeiras em florestas cultivadas. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. Editora UFV, Viçosa, pp 373–399 Zanetti R, Zanuncio JC, Vilela EF et al (2003) Level of economic damage for leaf-cutting ants (Hymenoptera: Formicidae) in Eucalyptus plantations in Brazil. Sociobiology 42:433–442 Zanuncio JC, Lemes PG, Antunes LR (2016) The impact of the Forest Stewardship Council (FSC) pesticide policy on the management of leaf-cutting ants and termites in certified forests in Brazil. Ann For Sci 73(2):205–214 Zeh JA, Zeh AD, Zeh DW (1999) Dump material as an effective small-scale deterrent to herbivory by Atta cephalotes. Biotropica 31:368–371 Zolessi LC, Gonzáles L (1978) Observaciones sobre el género Acromyrmex (A) lundi (Guérin, 1838) (Hymenoptera: Formicidae) Revista da Faculdade de Humanidades e Ciencias. Ser Cienc Biol 7:9–28 Zolessi LC, Philippi ME (1998) Las hormigas cortadoras del Uruguay del género Acromyrmex (Hymenoptera: Formicidae). In: Filho BE, Mariconi FAM, Fontes LR (eds) Anais de Simpósio sobre formigas cortadeiras do Mercosul. FEALQ, Piracicaba, pp 93–98

Chapter 4

Remote Sensing for Insect Outbreak Detection and Assessment in Latin America Roberto O. Chávez and Ronald Rocco

4.1  W  hy Remote Sensing Is So Useful to Assess and Map Insect Outbreaks? Straight to the point. Remote sensing is useful to map and assess insect outbreaks because it is cheap (only a smart scientist and a decent computer with Internet are needed), satellite images are widely available (for the entire globe and most of them free of charge) and because it allows us (the remote sensing scientists or any other enthusiastic fellow) to make nice insect outbreak maps which are understandable for everybody. An example of a remote-sensing-based quantification of forest insect defoliation is provided in Fig. 4.1, where readers can not only see the affected area by an outbreak of Ormiscodes amphimone caterpillars in Patagonian forests (Southern Chile) but also the level of defoliation in different intensities of red colors. We can deliver such maps every 8 days in what is now called “near real time” (Sakamoto et al. 2014; Tang et al. 2019; Xin et al. 2013), i.e., as soon as the satellite acquires the image and makes it available at the Geo-portal. To perform this analysis, we used about 800 satellite composites (a sum of patches of cloud-free images over a time frame) from the MODIS sensor on board of the Terra and Aqua satellites from NASA. This dataset provides information from 2000 till the present time, from which we studied the normal annual leaf phenology of the forest and detected punctual defoliation events (see Chávez et al. (2019) for more technical details). Marvelous, isn’t it? However, not always this abundant satellite data was so easy to get. About 20 years ago, only a very rich scientific agency, mainly in developed countries, or the owners of the satellite data and space agencies as the National Aeronautics and Space Administration (NASA) or the European Space Agency (ESA) were able to make

R. O. Chávez (*) · R. Rocco Laboratorio de Geo-Información y Percepción Remota, Instituto de Geografía, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile e-mail: [email protected]; [email protected] © Springer Nature Switzerland AG 2020 S. A. Estay (ed.), Forest Pest and Disease Management in Latin America, https://doi.org/10.1007/978-3-030-35143-4_4

45

46

R. O. Chávez and R. Rocco

Fig. 4.1  A remote-sensing-based map (d); ground (a, b) and aerial (c) pictures of an outbreak of the moth Ormiscodes amphimone that occurred in Nothofagus pumilio forests (Southern Patagonia, Chile) during the austral summer 2018–2019 (unpublished data)

such amazing maps. Data was expensive for anyone else, especially for scientists in Latinoamerica and not only data but software as well. Twenty years ago, all analyses were done using expensive licensed software such as ArcView (nowadays ArcGIS), ERDAS Imagine, or ENVI-IDL. Now things have changed and remote sensing assessments can be done using free software such as R, Orfeo Toolbox, or QGIS (e.g., analyses done in Fig. 4.1 were done in R and maps designed in QGIS). What changed? Basically, policy—policy regarding remote sensing data distribution as a consequence of the United Nations Convention on Climate Change and more recently the Convention on Biological Diversity. These two conventions have enabled the creation of a new framework on data policy, boosting the remote sensing science in general and remote sensing for insect outbreak detection and assessment in particular. Nevertheless, to date, most of the research on detecting and mapping insect outbreaks has been done in the Northern Hemisphere, while in the Southern Hemisphere, very little is known. This is particularly the case in Latin America, and we believe there is a relevant research gap that needs to be filled. In the next chapters, we introduce the basic principles for the use of satellite data for insect outbreak detection and mapping (Chap. 2), continue with a review of what has been done on this matter in Latin America (Chap. 3), and finish with a reflection about the “state of the art,” research gaps, recommendations, and outlook (Chap. 4).

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47

4.2  W  hat Insect Outbreak Effects on Vegetation Can Be Actually Measured from Space? Although a little bit technical for ecologists or entomologists, in order to apply remote sensing for insect outbreak detection, it is crucial and unavoidable to understand which effects or symptoms an insect outbreak can cause on vegetation that are actually measurable from space. I will provide a (hopefully) not so technical overview of remote sensing basis for insect disturbance detection and mapping. For those eager to read more about this exiting topic, please refer to the papers of Rullan-Silva et al. (2013) and Stone and Mohammed (2017). All satellite sensors measure electromagnetic radiation reflected or emitted from the Earth. The primary source of electromagnetic radiation is the sun, and many sensors have been designed to measure reflected solar radiation. These are the so-­ called optical sensors which typically measure incoming radiation between 350 and 2400  nm. Different biophysical parameters of vegetation control the amount of radiation reflected or emitted back to space (Baret et al. 2007). For example, leaf pigments (chlorophylls and carotenoids) absorb most of the solar radiation between 400 and 700  nm (the photosynthetically active radiation or PAR), causing a low reflection back to space at these wavelengths (Thomas and Gausman 1977). In contrast, a high leaf area index (LAI) and more air layers in the intercellular parenchyma of leafs cause higher reflection between 700 and 1200  nm (near-infrared spectral region) (Slaton et  al. 2001). Water in plants has also specific radiation absorption features at 910–1070 nm and 1100–1280 nm (Clark and Roush 1984). There are also the so-called active sensors where pulses of radiation are emitted and read back. In this group, we have the LiDAR (light detection and ranging) and Radar (transmits and receives radio waves) sensors, measuring three-dimensional architecture of vegetation, from which insect effects on the vegetation structure can be quantified. In summary, different forest canopy properties can be assessed using radiometer devices from space. Examples of optical sensors are the Landsat family from NASA with the Thematic Mapper (TM), the Enhanced Thematic Mapper Plus (ETM+), and the Operational Land Imager (OLI) on board of Landsat 5, 7, and 8, respectively. Altogether, sensors from the Landsat program provide the longest record (about 50 years) of satellite imagery worldwide at medium spatial resolution (30 m), and it is one of the most valuable for insect outbreak detection and assessment. Other relevant optical sensors useful for outbreak detection are the Moderate Resolution Imaging Spectroradiometer (MODIS) sensor, also from NASA, on board of the Terra (launched in 2000) and Aqua (launched in 2003) satellites, delivering daily images (each, two per day when used combined) at 250-m resolution, and the Multispectral Instrument (MSI) from ESA on board of the Sentinel-2A (launched in 2015) and Sentinel-2B (launched in 2017), which, when combined, provide data at 10-m resolution. Commercial satellites from companies such as Maxar—DigitalGlobe (QuickBird, WorldView-2 and 3, GeoEye, etc.) or Airbus (Pléiades, SPOT, DMC) offer also optical imagery at very high spatial resolution (i.e., 300 ha) in Latin America

2007

2016

2015

2012

2012

Year of the attack 2015

17,531

17,850

20,738

21,963

22,275

Total affected area (ha) 24,388

Affected area in one growing Method used to season (ha) quantify the area 24,388 MODIS EVI time series analysis and ground control 22,275 MODIS EVI time series analysis and ground control 21,963 MODIS EVI time series analysis and ground control 20,738 MODIS EVI time series analysis and ground control 17,850 MODIS EVI time series analysis and ground control 17,531 MODIS EVI time series analysis and ground control Estay et al. (2019)

Chávez et al. (2019)

Estay et al. (2019)

Estay et al. (2019)

Estay et al. (2019)

Source Estay et al. (2019)

50 R. O. Chávez and R. Rocco

Lago Verde, Chile

13

71° 36′ W Ormiscodes amphimone

72° 14′ W Ormiscodes amphimone

Cerro Castillo, 46° 06′ Chile S

12

44° 30′ S

72° 36′ W Ormiscodes amphimone

45° 24′ S

72° 14′ W Ormiscodes amphimone

46° 06′ S

Ormiscodes amphimone

71° W

40–41° S

Puerto Aysén, Chile

Nahuel Huapi National Park, Argentina Cerro Castillo, Chile

72° 14′ W Ormiscodes amphimone

46° 06′ S

Latitude Longitude Attacker 18° 04′ 46° 20′ W Thyrinteina S arnobia

11

10

9

Rank Location 7 Presidente Olegario and Joao Pinheiro, Brazil 8 Cerro Castillo, Chile

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Type of damage Forest host Defoliation Eucalyptus sp.

2003

2009

2009

2012

1986

2015

Year of the attack 1981

4731

5444

10,138

10,344

11,600

12,294

Total affected area (ha) 15,000

4731

5444

10,138

10,344

11,600

12,294

Estay et al. (2019)

Estay et al. (2019)

Estay et al. (2019)

Paritsis et al. (2011) Estay et al. (2019)

Estay et al. (2019)

(continued)

MODIS EVI time series analysis and ground control Supervised classification of Landsat data MODIS EVI time series analysis and ground control MODIS EVI time series analysis and ground control MODIS EVI time series analysis and ground control MODIS EVI time series analysis and ground control

Affected area in one growing Method used to season (ha) quantify the area Source 15,000 No information Anjos et al. (1987) 4  Remote Sensing for Insect Outbreak Detection and Assessment in Latin America 51

72° W Ormiscodes amphimone

2° 30′ S 79° 44′ W Oiketicus kirbyi

Los Glaciares 49 °S National Park, Argentina

72° W

49 °S Ormiscodes amphimone

47° 59′ W Thyrinteina arnobia

Ormiscodes amphimone

23° 52′ S

20

19

18

7

Los Glaciares National Park, Argentina São Miguel Arcanjo, Brazil Los Glaciares National Park, Argentina Ecological Reserve of Churute, Ecuador

72° W

72° 14′ W Ormiscodes amphimone

49 °S

Cerro Castillo, 46° 06′ Chile S

Latitude Longitude Attacker 21° 10′ 47° 48′ W Thyrinteina S arnobia

16

15

Rank Location 14 Ribeirao Preto, Brazil

Table 4.1 (continued)

2001

1973

2003

2007

Defoliation Rhizophora mangle, 1989 Avicennia germinans, Laguncularia racemosa, Conocarpus erectus Defoliation Nothofagus pumilio 2005

Defoliation Nothofagus pumilio

Defoliation Eucalyptus sp.

Defoliation Nothofagus pumilio

Defoliation Nothofagus pumilio

Type of damage Forest host Defoliation Eucalyptus sp.

Year of the attack 1973

976

976

Supervised classification of Landsat data

Paritsis et al. (2011)

Affected area in one Total Method used to affected growing area (ha) season (ha) quantify the area Source 4500 4500 No information Anjos et al. (1987) Estay 3944 3944 MODIS EVI et al. time series (2019) analysis and ground control Paritsis 2052 2052 Supervised classification of et al. (2011) Landsat data 1800 1800 No information Anjos et al. (1987) Paritsis 1202 1202 Supervised classification of et al. (2011) Landsat data 1200 1200 Aerial survey Gara (1990)

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Coronel Fabriciano, Brazil

24

49° 03′ W Thyrinteina arnobia

42° 37′ W Thyrinteina arnobia

22° 18′ S

19° 31′ S

Thyrinteina arnobia

Attacker Ormiscodes amphimone

Non-remote-sensing-based studies are highlighted in gray

Bauru, Brazil

23

Rank Location Latitude Longitude 72° W 21 Los Glaciares 49 °S National Park, Argentina 22 Itu, Brazil 23° 15′ 47° 17′ W S Defoliation Eucalyptus sp.

Defoliation Eucalyptus sp.

1967

1948

1973

Type of damage Forest host Defoliation Nothofagus pumilio

Defoliation Eucalyptus sp.

Year of the attack 1999

448

600

448

600

No information

No information

Affected area in one Total Method used to affected growing area (ha) season (ha) quantify the area 973 973 Supervised classification of Landsat data 827 827 No information Source Paritsis et al. (2011) Anjos et al. (1987) Anjos et al. (1987) Anjos et al. (1987)

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Fig. 4.2  Latin American forest insect outbreaks classified by affected area and survey method (red circles using remote sensing and black circles using other methods)

literature review. We ranked the reported outbreaks by size to check whether the Ormiscodes amphimone defoliations in Patagonia were actually the largest in Latin America (see Table  4.1 and Fig.  4.2). Besides the Ormiscodes amphimone outbreaks, relevant insect outbreaks have also taken place in Brazil and Ecuador as reported by Anjos et al. (1987) and Gara (1990), respectively. In different localities of the Minas Gerais state in Brazil, the defoliator Thyrinteina arnobia affected large areas of Eucalyptus sp. plantations ranging from 450 to 1500 ha (Anjos et al. 1987), while in Ecuador, the defoliator Oiketicus kirbyi attacked different tree species of a

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mangrove forest, affecting an area of about 1200 ha of the Ecological Reserve of Churute (Anjos et al. 1987). We believe that there would be more insect outbreaks in Latin America that have not been studied yet. For the moment, the Ormiscodes amphimone outbreaks in Argentinian and Chilean Patagonia are the most extensive and frequent insect disturbances reported in Latin America (Table 4.1 and Fig. 4.2).

4.4  I nsect Outbreak Detection and Mapping in Latin America: Why So Little? Research Gaps, Recommendations, and Outlook In many countries of Latin America, fast-growing exotic plantations have been established for intensive timber production, which are susceptible to suffer insect outbreaks considering the large and continuous area of insect available host. In fact, South America is the second world area (after Asia-Pacific) where plantation expansion has increased the most: 67% between 1990 and 2010 (Kröger 2014). Only in Brazil, official reports indicate that plantations occupy approximately 6.7 million hectares, from which about 77% corresponds to Eucalyptus sp. and 23% to Pinus sp. monocultives (ABRAF 2012), although some authors claim that it could be more (Kröger 2014). In Chile, timber monocultives have increased rapidly since 1970, especially between 1995 and 2009, and currently, exotic plantations of Pinus radiata and Eucalyptus sp. have reached about 2.5 million hectares (Zamorano-­ Elgueta et al. 2015). Argentina and Uruguay have followed the same trend and used the same species, reaching about 1.3 (SM 2019) and 1.2 million ha (SM 2019), respectively. Under this scenario of expanding monocultives in Latin America, it is hard to believe that insect outbreaks of exotic plantation pests are not an issue in this region of the world. It seems that there are some advances towards remote sensing assessments of insect outbreaks in plantations: a recent work of dos Santos et al. (2017) demonstrated the capability of the Landsat 8 OLI instrument to map Thaumastocoris peregrinus attacks in Eucalyptus plantations in Brazil. This exotic insect pest was first reported in 2008 and now is present in Eucalyptus plantations in at least seven states of Brazil: São Paulo; Rio Grande do Sul, Parana, Minas Gerais, Rio de Janeiro, Espírito Santo, and Mato Grosso do Sul (Wilcken et  al. 2010). For sure we will hear more about remote-sensing-based studies of Thaumastocoris peregrinus outbreaks in Eucalyptus and other relevant plantation pests in Latin America in the near future. Perhaps a limitation to publish remote sensing surveys of pest plantations is the fact that timber companies do not want to expose or inform large-scale sanitary problems in order to avoid restrictions to timber commercialization, for example, in countries with severe sanitary regulations and controls, or simply to avoid sharing sensitive information with competitors, environmental agencies, or general public. If that is the case, an important role of the national forest services of Latin American countries is required to make insect outbreaks in plantations transparent to the

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s­cientific community and public in general. A focused effort of remote sensing capacity building must be done in these governmental institutions to build up national forest health databases and not only for plantations but for native forests as well. In the case of Latin American native forests, the lack of remote sensing studies of insect outbreaks could also be explained by the fact that forest pests are not considered as a main threat for Latin American forests compared to deforestation (especially in the Amazon rainforest). Just to illustrate the magnitude of this global problem, we want to cite a recent comment article of Fuchs et al. (2019) in Nature explaining how the ongoing commercial war between China and the USA could lead to a huge deforestation pressure in the Amazon rainforest. In 2018, the USA introduced a 25% tariff to Chinese imported products, and as a response, China imposed the same extra tariff to US products, from which soybean is a main product exported to China. By 2016, 50% of the soybeans imported by China came from Brazil, and therefore, this country is an alternative to cover a shortage of US soybean in the Chinese market, leading to an estimated increase of 39% of the current soybean farming area, i.e., 13 million hectares in the Amazon. We may end up seeing papers of remote-sensing-based studies of soybean insect outbreaks instead. Nevertheless, in the long term, the sanitary condition of Latin American native forest should be relevant as well, and in this regard, the current trends of open access data and software can help in implementing cost-efficient sanitary monitoring systems of Latin American forests. Here, there is a big challenge for the remote sensing and entomological scientific community to work together and fill this research gap. Acknowledgments  This research was funded by Fondo Nacional de Desarrollo Científico y Tecnológico of Chile, Grant Number: 1160370; CONICYT PAI Number: 82140001; Fondecyt Iniciación Grant Number: 11171046. The authors also want to thank Matías Olea for making Fig. 4.2.

References ABRAF (2012) Anuário estatístico da ABRAF 2012: ano base 2011. ABRAF, Associação Brasileira de Produtores de Florestas, Brasilia Anees A, Olivier JC, O’Rielly M et al (2013) Detecting beetle infestations in pine forests using MODIS NDVI time-series data. In: International geoscience and remote sensing symposium (IGARSS), pp 3329–3332 Anjos N, Santos GP, Zanuncio JC (1987) The eucalyptus defoliator Thyrinteina arnobia Stoll 1782 (Lepidoptera: Geometridae). Boletim Tecnico, Empresa de Pesquisa Agropecuaria de Minas Gerais 25(56):1–56 Babst F, Esper J, Parlow E (2010) Landsat TM/ETM+ and tree-ring based assessment of spatiotemporal patterns of the autumnal moth (Epirrita autumnata) in northernmost Fennoscandia. Remote Sens Environ 114(3):637–646 Barbosa P, Letourneau D, Agrawal A (2012) Insect outbreaks revisited. Wiley, Chichester Baret F, Houlès V, Guérif M (2007) Quantification of plant stress using remote sensing observations and crop models: the case of nitrogen management. J Exp Bot 58(4):869–880 Chávez RO, Estay SA, Riquelme G (2017) npphen: an R package for estimating annual phenological cycle. UACH, PUCV, Chile

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Chávez OR, Rocco R, Gutiérrez GÁ et  al (2019) A self-calibrated non-parametric time series analysis approach for assessing insect defoliation of broad-leaved deciduous Nothofagus pumilio forests. Remote Sens 11(2):204 Clark RN, Roush TL (1984) Reflectance spectroscopy—quantitative analysis techniques for remote sensing applications. J Geophys Res 89:6329–6340 dos Santos A, Oumar Z, Arnhold A et  al (2017) Multispectral characterization, prediction and mapping of Thaumastocoris peregrinus (Hemiptera: Thamascoridae) attack in Eucalyptus plantations using remote sensing. J Spat Sci 62(1):127–137 Estay SA, Chávez RO (2018) npphen: an R-package for non-parametric reconstruction of vegetation phenology and anomaly detection using remote sensing. BioRxiv 301143 Estay SA, Chávez RO, Rocco R et al (2019) Quantifying massive outbreaks of the defoliator moth Ormiscodes amphimone in deciduous Nothofagus-dominated southern forests using remote sensing time series analysis. J Appl Entomol 143(7):787–796 Fassnacht FE, Latifi H, Ghosh A et al (2014) Assessing the potential of hyperspectral imagery to map bark beetle-induced tree mortality. Remote Sens Environ 140:533–548 Fuchs R, Brown C, Cossar F et al (2019) US-China trade war imperils Amazon rainforest. Nature 567:451 Gara RI (1990) Defoliation of an Ecuadorian mangrove forest by the bagworm, Oiketicus kirbyi Guilding (Lepidoptera: Psychidae). J Trop For Sci 3(2):181–186 Garreaud R, Lopez P, Minvielle M et  al (2013) Large-scale control on the Patagonian climate. J Clim 26(1):215–230 Hall RJ, Castilla G, White JC et al (2016) Remote sensing of forest pest damage: a review and lessons learned from a Canadian perspective. Can Entomol 148(S1):S296–S356 Jamali S, Jönsson P, Eklundh L et al (2015) Detecting changes in vegetation trends using time series segmentation. Remote Sens Environ 156:182–195 Kröger M (2014) The political economy of global tree plantation expansion: a review. J Peasant Stud 41(2):235–261 Lausch A, Heurich M, Gordalla D et al (2013) Forecasting potential bark beetle outbreaks based on spruce forest vitality using hyperspectral remote-sensing techniques at different scales. For Ecol Manag 308:76–89 Paritsis J, Veblen TT, Smith JM et al (2011) Spatial prediction of caterpillar (Ormiscodes) defoliation in Patagonian Nothofagus forests. Landsc Ecol 26(6):791–803 Rullan-Silva CD, Olthoff AE, Delgado de la Mata JA et al (2013) Remote monitoring of forest insect defoliation: a review. For Syst 22(3):377–391 Sakamoto T, Gitelson AA, Arkebauer TJ (2014) Near real-time prediction of US corn yields based on time-series MODIS data. Remote Sens Environ 147:219–231 Senf C, Seidl R, Hostert P (2017) Remote sensing of forest insect disturbances: current state and future directions. Int J Appl Earth Obs Geoinf 60:49–60 Shendryk I, Broich M, Tulbure MG et al (2016) Mapping individual tree health using full-­waveform airborne laser scans and imaging spectroscopy: a case study for a floodplain Eucalyptus forest. Remote Sens Environ 187:202–217 Slaton MR, Hunt ER Jr, Smith WK (2001) Estimating near-infrared leaf reflectance from leaf structural characteristics. Am J Bot 88(2):278–284 SM (2019) Inventario nacional de plantaciones forestales por superficie. Secretaría de Modernización (SM): Presidencia de la Nación, Argentina Solberg S, Næsset E, Hanssen KH et al (2006) Mapping defoliation during a severe insect attack on Scots pine using airborne laser scanning. Remote Sens Environ 102(3–4):364–376 Spruce JP, Sader S, Ryan RE et al (2011) Assessment of MODIS NDVI time series data products for detecting forest defoliation by gypsy moth outbreaks. Remote Sens Environ 115(2):427–437 Stone C, Mohammed C (2017) Application of remote sensing technologies for assessing planted forests damaged by insect pests and fungal pathogens: a review. Curr For Rep 3(2):75–92 Tang X, Bullock EL, Olofsson P et al (2019) Near real-time monitoring of tropical forest disturbance: new algorithms and assessment framework. Remote Sens Environ 224:202–218

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Thomas JR, Gausman HW (1977) Leaf reflectance vs leaf chlorophyll and carotenoid concentrations for eight crops. Agron J 69(5):799–802 Townsend PA, Singh A, Foster JR et al (2012) A general Landsat model to predict canopy defoliation in broadleaf deciduous forests. Remote Sens Environ 119:255–265 Vastaranta M, Kantola T, Lyytikäinen-Saarenmaa P et al (2013) Area-based mapping of defoliation of scots pine stands using airborne scanning LiDAR. Remote Sens 5(3):1220–1234 Verbesselt J, Hyndman R, Newnham G et al (2010) Detecting trend and seasonal changes in satellite image time series. Remote Sens Environ 114(1):106–115 Wilcken C, Soliman E, De Sá L et al (2010) Bronze bug Thaumastocoris peregrinus Carpintero and Dellapé (Hemiptera: Thaumastocoridae) on Eucalyptus in Brazil and its distribution. J Plant Protect Res 50(2):201–205 Xin Q, Olofsson P, Zhu Z et al (2013) Toward near real-time monitoring of forest disturbance by fusion of MODIS and Landsat data. Remote Sens Environ 135:234–247 Zamorano-Elgueta C, Rey Benayas JM, Cayuela L et al (2015) Native forest replacement by exotic plantations in southern Chile (1985–2011) and partial compensation by natural regeneration. For Ecol Manag 345:10–20

Part II

Pests of Natural Forests

Chapter 5

Ormiscodes amphimone Outbreak Frequency Increased Since 2000 in Subantarctic Nothofagus pumilio Forests of Chilean Patagonia Álvaro G. Gutiérrez, Roberto O. Chávez, Javier A. Domínguez-Concha, Stephanie Gibson-Carpintero, Ignacia P. Guerrero, Ronald Rocco, Vinci D. Urra, and Sergio A. Estay 

5.1  Introduction In recent decades, insect outbreaks have been recognized as major agents modifying forest health worldwide (Trumbore et al. 2015). Due to global warming, insect outbreaks in forests are expected to become more severe and frequent (Bale et al. 2002; Pureswaran et al. 2018). For example, insect outbreaks have defoliated millions of hectares in recent decades in different areas of temperate forests such as western North America, Europe, and South America (Millar and Stephenson 2015). The impacts of the change in frequency of insect outbreaks on forest dynamics are partially understood, particularly on how climate change is driven these changes. There are numerous studies showing the impact of insect outbreaks on forests in the Northern Hemisphere (Haynes et al. 2014; Weed et al. 2013) and fewer studies documenting insect outbreaks in the southern forests of New Zealand, Australia, and South America (Hosking and Hutcheson 1988; Loch and Floyd 2001; Milligan Á. G. Gutiérrez (*) · J. A. Domínguez-Concha · S. Gibson-Carpintero I. P. Guerrero · V. D. Urra Facultad de Ciencias Agronómicas, Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile e-mail: [email protected] R. O. Chávez · R. Rocco Laboratorio de Geo-Información y Percepción Remota, Instituto de Geografía, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile e-mail: [email protected]; [email protected] S. A. Estay Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile Center of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile e-mail: [email protected] © Springer Nature Switzerland AG 2020 S. A. Estay (ed.), Forest Pest and Disease Management in Latin America, https://doi.org/10.1007/978-3-030-35143-4_5

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1974; Paritsis and Veblen 2011). Thus, more knowledge needs to be gained on ­spatial extent, synchronization, and temporal periodicity of insect outbreaks, particularly in hitherto overlooked regions, such as the Southern Hemisphere. Recently, outbreaks of the native moth Ormiscodes amphimone (Fabricius) (Lepidoptera: Hemileucinae) defoliated thousands of hectares in the Southern Cone of South America (Chávez et al. 2019; Estay et al. 2019; Paritsis and Veblen 2011). In 2015, a massive and spatially extensive Ormiscodes outbreak in the valley of El Furioso river occurred (near Mallín Grande, Aysén Region, Chile, 46.8°S, Fig. 5.1a). The outbreak event in 2015 nearby Mallín Grande has been reported as the most extensive single and spatially continuous event in the Southern Hemisphere affecting a natural forest by a native insect species (Estay et al. 2019). One open question regarding this disturbance event is why a disturbance event of such large magnitude was not reported before. Estay et al. (2019) hypothesized that these outbreaks are a relatively new ecological phenomenon triggered by climate change. In southern South America (south of 42°S), instrumental temperature records have followed the global warming trend, and atmospheric circulation patterns appear to be anomalous (Rosenblüth et al. 1997; Villalba et al. 2003). Particularly the Chilean Patagonia (Aysén Region) is being affected by global warming via increased drought conditions and increasing temperatures (Garreaud 2018), which suggest the forests in the region are more vulnerable to global warming and insect outbreaks (Olivares-Contreras et al. 2019). For example, in 2016, a 60% precipitation deficit occurred, a 1 °C increase in mean annual temperature has been observed between 1901 and 2010, and minimum temperatures increased dramatically (ca. 4  K) since 2000 (Álvarez et  al. 2015; Garreaud 2018; Olivares-Contreras et  al. 2019). Possibly the occurrence of O. amphimone outbreaks can be related to this warming trend over N. pumilio forests in Aysén, as this defoliator performance responds positively to dry and warm springs (Paritsis and Veblen 2011). Here, we explore the hypothesis that if this scenario of rising temperature in the last three decades is affecting Ormiscodes population dynamics, the subantarctic forests of Nothofagus pumilio will be impacted by an increasing number of defoliation events. We combined tree-ring and remote sensing analysis to provide insights into the changes in temporal patterns of Ormiscodes amphimone outbreaks since 1900 in the valley of El Furioso river. In order to understand the effect of recent climate change, we explored the relative contribution of climatic factors forcing Ormiscodes outbreaks of the last decades.

5.2  Materials and Methods 5.2.1  Study Species Ormiscodes amphimone (Lepidoptera: Saturniidae) is a native phytophagous moth that feeds on several plant hosts such as Nothofagus spp., Populus spp., Prunus spp., Juglans spp., Cryptocarya alba, and Pinus spp., among many other tree species

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Fig. 5.1  Forest defoliation caused by Ormiscodes amphimone in El Furioso river valley in Aysén region, Chile. (a) General view of Eloy stand studied in this research, (b) Ormiscodes amphimone feeding on Nothofagus pumilio leaves, (c) a completely defoliated tree of Nothofagus pumilio, (d) an understory view of Eloy stand. Picture credits: Álvaro G. Gutiérrez

(Angulo et al. 2004). In Chile, moth adults fly from January to June and are mainly distributed between 30 and 48°S (Angulo et al. 2004). Ormiscodes amphimone is considered detrimental for tree growth and timber production, can kill saplings, and potentially causes crown dieback on Nothofagus spp. if defoliation is severe (Baldini and Pancel 2002; Bauerle et al. 1997; Veblen et al. 1996). In this study, we addressed

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the impact of Ormiscodes amphimone defoliation on Nothofagus pumilio (Nothofagaceae) (Fig.  5.1b, c). This broad-leaved, deciduous tree species is the most widespread Nothofagus tree species in South America distributed from 35°S to 56°S (Moreira-Muñoz 2011). N. pumilio usually forms monospecific stands, and it is a common species in Andean treelines (Veblen et al. 1996). N. pumilio is the main host of O. amphimone and in monospecific forests dominated by this tree species spatially extensive Ormiscodes defoliations can occur (Artigas 1972; Bauerle et al. 1997; Estay et al. 2019; Paritsis and Veblen 2011). Furthermore, robust tree-ring chronologies have been developed with N. pumilio (Lara et al. 2001; Villalba et al. 2003), thus, there is a great potential for studying Ormiscodes outbreak dynamic using tree rings.

5.2.2  Study Area This study focused on the valley of El Furioso river near Mallín Grande town (Aysén Region, Chile), which is close to the southern shore of General Carrera Lake (Fig. 5.2). The valley is dominated by monospecific forests of Nothofagus pumilio (Nothofagaceae) and offers the opportunity to investigate Ormiscodes defoliations along an altitudinal gradient from 500 to 1200 m. First human settlements in the area were established in the 1930s. Since then, the valley has had low human impact, which is mostly none toward its upper part. Soils were originated from volcanic ash and are thin in general, with large amounts of semi-decomposed organic matter, acids, and poor nutrients (Hildebrand-Vogel et al. 1990). In El Furioso valley, annual precipitation sum is 910 mm, and mean annual temperature is 4.2 °C, with a mean summer temperature of 9 °C and a mean winter temperature of −0.4 °C (1976–2019 time period).

5.2.3  Mapping Ormiscodes Defoliations We first mapped the defoliated area caused by Ormiscodes outbreaks using remote sensing techniques. We used the Moderate Resolution Imaging Spectroradiometer (MODIS) 16-day composites of the Enhanced Vegetation Index (EVI) product, which is sensitive to changes in green biomass or leaf area index (Huete et al. 2002; Zhang et al. 2006, 2014). MODIS EVI has been successfully used for insect outbreak mapping in the Northern Hemisphere (Anees et  al. 2013; de Beurs and Townsend 2008; Verbesselt et al. 2010) and more recently for Ormiscodes outbreak mapping in Chile (Chávez et al. 2019; Estay et al. 2019). MODIS EVI 16-day composites provide data with 250-m pixel resolution and 16-day temporal resolution. We downloaded, pre-processed, and analyzed 365 MODIS EVI scenes from the Terra satellite, spanning the period 2000–2015.

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Fig. 5.2  Defoliated areas by Ormiscodes amphimone between 2000 and 2015 in the Aysén region (right panel). The upper left panel shows the defoliated area within the study area (El Furioso river valley, near Mallín Grande town) during the growing seasons 2011–2012, 2012–2013, and 2014– 2015. The lower left panel shows the defoliated area per growing season in the study area

We detected Ormiscodes outbreaks using the concept of “phenological anomaly,” following the nonparametric approach implemented in the R package “npphen” (Estay and Chávez 2018). In this approach, a spectral index, such as EVI, is used to (1) set the normal phenological cycle of the forest (most probable value) and its confidence intervals (e.g., 90%) using a kernel density estimator and (2) calculate a deviation from the normal behavior. The kernel estimator allows to indicate the probability of the anomaly to fall out from the normal phenological behavior. Using this approach, we neglected all anomalies with a probability 90% based on the EVI historical records. A detailed explanation of this approach can be found in Chávez et al. (2019). We calculated EVI anomalies and anomaly probabilities over the complete time series using a “leave-one-out” iterative procedure, in which we remove the growing season we want to analyze and calculate the reference annual phenology using the rest of the EVI time series. Then, we calculated EVI anomalies and anomaly probabilities per pixel and per date for the growing season of interest. We followed this procedure for the 15 growing seasons (2000–2001 till 2014–2015; note that austral growing season runs from September to March). Finally, for each growing season, we accumulated the pixels

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with significant (>90% anomaly probability) anomalies during the austral summer (January to March) to obtain the final area with significant negative anomalies per growing season. Ormiscodes outbreaks within the study area were flagged as large areas with negative anomalies.

5.2.4  Field Sampling Using the resulting defoliation map (Fig. 5.2, upper left panel), we sample forest stands where EVI anomalies were highly frequent (>5 anomalies, e.g., Fig. 5.1d) and infrequent (20 cm of stem diameter at 1.3 m height (DBH) found in the plot using increment borers. We obtained two radii per living tree at a height of about 1.3 m from the trunk base. Notes from each of the sampled trees were taken considering tree health, canopy position, and DBH, together with any sign showing insect damages. We sought with the core sampling to cover most of tree DBH classes present in the stand. Table 5.1  Site characteristics and descriptive statistics for tree-ring chronologies

Latitude (°S) Longitude (°W) Elevation (m a.s.l.) Period covered by the chronology Trees included (number of radii) Mean sensitivity Mean Rbar Year of EPS >0.9

Eloy 46° 51′ 50″ 72° 28′ 4″ 710 1752–2015 74 0.391 0.361 1850

Valle Largo 46° 56′ 52″ 72° 27′ 53″ 1000 1716–2015 44 0.312 0.417 1850

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5.2.5  Tree-Ring Analysis We mounted cores and prepared them with a core microtome (Gärtner and Nievergelt 2010), sanded using sandpaper of the finest grit, and dated following standard dendrochronological techniques (Stokes and Smiley 1996). Tree-ring widths were measured under a microscope to the nearest 0.001 mm and stored in a computer. We used the computer program COFECHA to detect measurement and cross-dating errors (Holmes 1983). For dating purposes, we followed the convention for the Southern Hemisphere, which assigns to each tree ring the date of the year in which radial growth started (Schulman 1956). Once the tree-ring series were dated, we selected the best correlated trees (>30 trees, Pearson correlation >0.5) and the common time period with >0.9 expressed population signal (EPS) to develop a tree-ring chronology at each site (Table 5.1). We used the dplR package in R to analyze the tree-ring series (Bunn 2010). A similar standardization process was carried out for all the series in both sites in order to eliminate the trend of biological age and the individual response of the trees and to incorporate and compare trees of different ages in each chronology (Fritts 1976). Standardization involves fitting the observed ring-width series with a theoretical curve and computing an index by subtracting the logarithms of the expected from the observed values (Cook and Kairiukstis 1990). For the standardization, we fitted a nonlinear function (exponential, spline, or polynomial) to each individual series, so that the relationship between growth and the adjusted value produces a dimensionless index, with a mean equal to 1 and stationary variance.

5.2.6  Climatic Influence on Tree Radial Growth We explored the common climatic signal on radial growth of the control chronology using a principal component analysis (PCA) for the common growth period 1850–2015 (Richman 1986; Rodríguez-Catón et al. 2016). We selected all tree-ring series from Valle Largo that were significantly correlated with the first component PC1 (r ≥ 0.45, 89 series) and used to develop the control chronology. We then constructed the chronologies by averaging standardized tree-ring series with biweight robust estimation. In the case of the host chronology (Eloy, lower elevation site), the PCA was not conducted to conserve all radial growth variation in the chronology. The control chronology (Valle Largo, upper elevation site) was correlated with local climatic variables using the bootstrap method to analyze the climatic response at multiple time intervals and evaluate the seasonality of such responses (Zang and Biondi 2013). For this analysis, we obtained climate data from the climatic grid database CR2Met (data obtained in March 2019 from  http://www.cr2.cl/datos-­ productos-­grillados/) for mean monthly temperature, monthly rainfall sum, maximum monthly temperature, and minimum monthly temperature. We correlated climatic variables as a function of radial growth in years t and t − 1 (Fritts 1976), as

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radial growth in any specific year is influenced by the climate of the current (t) and previous (t − 1) years. Correlations were calculated for the common time period of the chronology and climatic data (1979–2015). We also related the control and host chronologies using a cross-correlation function analysis (Venables and Ripley 2002).

5.2.7  Ormiscodes Outbreak Reconstruction We reconstructed Ormiscodes defoliation events following the hierarchical approach proposed by Paritsis et al. (2009). Insect defoliation events generate specific anatomical structures produced by damage at the cellular level generating abnormal xylematic tissue (Paritsis et al. 2009; Schweingruber 1996). Tree rings with abnormal anatomy can be identified to date defoliation events (Paritsis et al. 2009) because it is characterized by the presence of white color along the late wood of a tree ring, followed by a single micro or absent ring (Fig. 5.3). This micro ring is produced Fig. 5.3  The abnormal wood anatomy pattern found in Nothofagus pumilio tree rings affected by Ormiscodes amphimone defoliation events. The white arrow indicates the white ring commonly observed in the year of defoliation, followed by a narrow or absent ring in the next year (gray arrow)

5  Ormiscodes amphimone Outbreak Frequency Increased Since 2000…

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because 1 year after the Ormiscodes defoliation (the growing season period starting in the next austral spring), defoliated trees grow significantly less (41% less basal area increment than normal) (Piper et  al. 2015). We visually inspected all cores obtained at both sites to search for this anatomical pattern using a Leica stereomicroscope. We recorded the calendar year when we detected the presence of any of the three types of observable wood anatomical anomalies suggesting a defoliation event, i.e., absent or partially absent ring, intra-annual white band in late wood, and micro-ring. We used the recorded calendar years to develop a defoliation event chronology based on this anatomical inspection. A second step was conducted using wavelet decompositions of radial growth time series (Mallat 1989). We used this method to detect statistical significant reduction in radial growth of ring width series of each tree (raw series, without standardization). A bootstrap of each series was performed to determine if unusual changes in the time series were not expected by chance (p 70% of collected trees evidenced strong reductions in radial growth in the following year of the attack and changes in anatomical wood patterns (Fig.  5.4). We also detected previous events that influenced >50% of sampled trees with strong reductions in growth in 1948, 1960, and 1982 (Fig. 5.4). These events were not recorded in the radial growth of trees growing at Valle Largo where Ormiscodes defoliation has not occurred as suggested by the remote sensing analysis (Figs. 5.1 and 5.4). From this result, we suggest that outbreak events have increased in the last decade, with at least four events affecting the Eloy site compared to three events affecting the site between 1940 and 2010. Prior to 1949, we did not find a discernible growth or anatomical pattern that could be inferred as an outbreak event. Our result is consistent with a low number of outbreak events found in other dendroecological reconstructions in southern Patagonia before 2000 (Paritsis and Veblen 2011; Paritsis et al. 2009) and an increase in outbreak frequency since 1979  in southern Patagonia (Paritsis and Veblen 2011).

5.3.2  Climatic Patterns Triggering Ormiscodes Outbreaks We found that both the control and host chronology were significantly correlated with monthly precipitation at late spring and early summer of the previous growing season (r2 > 0.2, p  900 mm A1—Preferential area with restrictions. Low disease incidence. Caution is required for the establishment of rubber tree plantations due to seasonal water deficits (Da = 200–300 mm) B—Marginal area with super humid conditions. Moderate to high disease incidence. Obligate phytosanitary control. Da = 0 mm, RHs > 80%, mean temperature of the coldest month (Tf) > 20 °C (e.g., South Coast of Bahia) B1—Marginal area with super humid conditions. Moderate to high disease incidence in clonal gardens, nurseries and new plantations, or adult plantations with cultivars that do not adequately shed their leaves (hybrids of H. benthamiana). It differs from the previous region by having Tf