Ecologically-Based Management of Rodent Pests ECOLOGICALL V-BASED MANAGEMENT of RODENT PESTS

Ecologically-based Management of Rodent Pests ECOLOGICALL V-BASED MANAGEMENT OF RODENT PESTS

Edited by: Grant R. Singleton, Lyn A. Hinds, Herwig Leirs and Zhibin Zhang

Australian Centre for International Agricultural Research Canberra 1999 The Australian Centre for International Agricultural Research (ACIAR) was established in June 1982 by an Act of the Australian Parliament. Its primary mandate is to help identify agricultural problems in developing countries and to commission collaborative research between Australian and developing country researchers in fields where Australia has special competence.

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ACIAR MONOGRAPH SERIES

This peer-reviewed series contains the results of original research supported by ACIAR, or deemed relevant to ACIAR's research objectives. The series is distributed internationally, with an emphasis on the Third World

©Australian Centre for International Agricultural Research GPO Box Canberra, ACT 2601.

Singleton, C.R., Hinds, L.A., Leirs, H. and Zhang, Z.ed. 1999. Ecologically-based management of rodent ACIAR Monograph No. 59, 494p.

ISBN 1 86320 262 5 Editing and design by Arawang Communication Croup, Canberra Printed by Brown Prior Anderson, Melbourne, Australia page

Author Contact Details 8 Abbreviations 12 List of Species 13 Preface 15

1. Ecologically-based Management of Rodent Pests-Re-evaluating 17 Our Approach to an Old Problem Grant R. Singleton, Herwig Leirs, Lyn A. Hinds and Zhibin Zhang

Section 1 Basic Research - the Foundation for Sound Management 31

2. Current Paradigms of Rodent Population Dynamics- 33 What Are We Missing? Charles J. Krebs

3. The Behaviour and Ecology of Rattus norvegicus: from Opportunism to 49 Kamikaze Tendencies David W. Macdonald, Fiona Mathews and Manuel Berdoy

4. Models for Predicting Plagues of House Mice (Mus domesticus) 81 in Australia Roger P. Pech, Greg M. Hood, Grant R. Singleton, Elizabeth Salmon, Robert I. Forrester and Peter R. Brown

5. Rodent-Ecosystem Relationships: a Review 113 Chris R. Dickman

6. The Role of Rodents in Emerging Human Disease: Examples 134 from the Hantaviruses and Arenaviruses James N. Mills

5 Ecologically-based Rodent Management

Section 2 Methods of Management 161

7. Rodenticides Their Role in Rodent Pest Management in 163 Tropical Agriculture Alan P. Buckle 8. Physical Control of Rats in Developing Countries 178 Grant R. Singleton, Sudarmaji, Jumanta, Tran Quang Tan and Nguyen Quy Hung

9. Ecological Management of Brandt's Vole (Microtus brandti) in 199 Inner Mongolia, China Wenqin Zhong, Mengjun Wang and Xinrong Wan

10. Biological Control of Rodents- the Case for Fertility Control Using 215 Immunocontraception Usa K. Chambers, Ma/co/m A. Lawson and Lyn A. Hinds

11. Urban Rodent Control Programs for the 21st Century 243 Bruce A. Colvin and William B. Jackson

Section 3 Case Studies in Asia and Africa 259

12. Rodent Pest Management in Agricultural Ecosystems in China 261 Zhibin Zhang, Anguo Chen, Zhendong Ning and Xiuqing Huang

13. Rodent Pest Management in the Qinghai-Tibet Alpine Meadow 285 Ecosystem Naichang Fan, Wenyang Zhou, Wanhong Wei, Quanye Wang and Yongjin Jiang

14. Ecologically-Based Population Management of the Rice-Field 305 Rat in Indonesia Luke K.P. Leung, Grant R. Singleton, Sudarmaji and Rahmini

15. Population Ecology and Management of Rodent Pests in 319 the Mekong River Delta, Vietnam Peter R. Brown, Nguyen Quy Hung. Nguyen Manh Hung and Monica van Wensveen

16. Rodent Management in Thailand 338 Puangtong Boonsong, Sermsakdi Hongnark, Kornkaew Suasa-ard, Yuvaluk Khoprasert, Prasarttong Promkerd, Greangsak Hamarit, Piyanee Nookarn and Thomas Jakel

6 Contents

17. Farmer Participatory Research on Rat Management in Cambodia 358 Gary C. Jahn, Mak Solieng, Peter G. Cox, and Chhom Nel

18. Rodents in Agriculture in the Lao PDR a Problem with 372 an Unknown Future John M. Schiller, Bounneuang Douang Boupha and Onechanh Bounnaphol 19. Populations of African Rodents: Models and the Real World 388 Herwig Leirs

20. Ecophysiology and Chronobiology Applied to Rodent Pest 409 Management in Semi-arid Agricultural Areas in Sub-Saharan West Africa Bruno Sicard, Wamian Diarra and Howard M. Cooper

21. The Rodent Problem in Madagascar: Agricultural Pest and Threat to 441 Human Health Jean-Marc Duplantier and Daniel Rakotondravony

22. Rodent Pest Management in East Africa-an Ecological Approach 460 Rhodes H. Makundi, Nicho/as O. Oguge and Patrick S. Mwanjabe

23. Ecologically-based Rodent Management in Developing Countries: 477 Where to Now? Herwig Leirs, Grant R. Singleton and Lyn A. Hinds

Index 485

7 Berdoy. Manue!, Wildlife Conservation Research Chhom, 'Je!, Cambodia-IRRI-Australia Project Unit, Department of Zoology, and Department of (ClAP), PO Box 1, Phnom Penh, Cambodia. Veterinary Services, clo University Laboratory of Email.: IRRI -CAMBODIA®CGIAR.ORG Physiology, University of Oxford, South Parks Road, Fax: +85523211728 Oxford, OXl 3PT, UK. Email: manuel.berdoy®Vet.ox.ac.uk Colvin, Bruce A., 16 Temple Road, Lynnfield, MA 01940, USA. Boonsong, Puangtong, Agricultural Zoology Email: [email protected] Research Group, Division of Entomology and Fax: +1 781 334 5782 Zoology, Department of Agriculture, PO Box 9-34, Bangkok 10900, Thailand. Cooper, Howard M., INSERc'vf (Institut National Email: agrizoo®bkkl.loxinfo.co.th pour la Sante et la Recherche Medicale), U37!, Fax: +662 9405396 Cerveau et Vision, Bron, France. Email: [email protected] Bounnaphol, Onechanh, Agriculture and Forestry Fax: +33472913461 Service, Luang Prabang, Lao PDR. Fax: +856 71 212635 Cox, Peter G., Cambodia-IRH.l-Australia Project (ClAP), PO Box 1, Phnom Penh, Cambodia. Brown, Peter R, CSIRO Wildlife and Ecology, GPO Email: [email protected] Box 284, Canberra, ACT 2601, Australia. Fax: +85523211728 Email: [email protected] Fax: +61 26242 1505 Diarra, Wamian, CNRST (Centre National de la Recherche Scientifique et Technologique), BP 3052, Buckle, Alan P., Zeneca Agrochemicals, Fernhurst, Bamako, Mali. Haslemere, Surrey GU27 3JE, UK. Email: [email protected] Dickman, Chris R., Institute of Wildlife Research, Fax: +44 14286555668 School of Biological Sciences, University of Sydney, New South Wales 2006, Australia. Chambers, Lisa K., Vertebrate Biocontrol Email: [email protected] Cooperative Research Centre, CSIRO Wildlife and Fax: + 612 93514119 Ecology, GPO Box 284, Canberra, ACT 2601, Australia. Douang Boupha, Bounneuang, Department of Email: [email protected] Agriculture and Extension, Vientiane, Lao PDR. Fax: +612 6242 1505 Email: j.m.schiller@cgiaLorg Fax: +856 21414373 Chen, Anguo, Changsha Institute of Agriculture Modernization, Chinese Academy of Science, Duplantier, Jean-Marc, Programme RAMSE, IRD

\...ll'HI!Plld, Hunan 410125, P.R China. (Institut de Recherche pour le Developpement, ex Fax: +86 731 4612685 ORSTOM), BP 434, Antananarivo, Madagascar. Email: [email protected] Fax: +261202240451

8 Author Contact Details

Fan, Naichang, Department of Biology, Zhejiang Jackson, William B., Department of Biological Normal University, Jinhua, Zhejiang 321004, P.R. Sciences, Bowling Green State University, Bowling China. Green, OH 43403, USA. Fax: +1419 372 2024 Forrester, Robert I., CSIRO Mathematical and Information Sciences, GPO Box 664, Canberra, ACT Jahn, Gary c., Cambodia-IRRI-Australia Project 2601, Australia. (ClAP), PO Box 1, Phnom Penh, Cambodia. Email: [email protected] Email: [email protected] Fax: 61 26216 7111 Fax: +85523211728

Hamarit, Greangsak, Agricultural Zoology Research Jakel, Thomas, German Technical Cooperation Group, Division of Entomology and Zoology, (GTZ, Deutsche Gesellschaft fur Technische Department of Agriculture, PO Box 9-34, Bangkok Zusammenarbeit), 65726 Eschborn, Germany. 10900, Thailand. Email: [email protected] Email: [email protected] Fax: +66 2 9405396 Jiang, Yongjin, Northwest Plateau Institute of Biology, Chinese Academy of Sciences, Xining Hinds, Lyn A., CSIRO Wildlife and Ecology, GPO 810001, P.R. China. Box 284, Canberra, ACT 2601, Australia. Fax: +869716143282 Email: [email protected] Fax: +61 26242 1505 Jumanta, Research Institute for Rice, West Java, h,donesia. Hongnark, Sermsakdi, Agricultural Zoology Email: [email protected] Research Group, Division of Entomology and Fax: +62260520157 Zoology, Department of Agriculture, PO Box 9-34, Bangkok 10900, Thailand. Khoprasert, Yuvaluk, Agricultural Zoology Email: [email protected] Research Group, Division of Entomology and Fax: +66 2 9405396 Zoology, Department of Agriculture, PO Box 9-34, Bangkok 10900, TI1ailand. Hood, Greg M., CSIRO Wildlife and Ecology, GPO Email: [email protected] Box 284, Canberra, ACT 2601, Australia. Fax: +6629405396 Email: [email protected] Fax: +61 262421505 Krebs, Charles, J. Department of Zoology, University ofBritishCoiumbia, Vancouver, RC V6T lZ4, Huang, Xiuqing, Guandong Institute of Plant Canada. Protection, Chinese Academy of Agricultural Email: [email protected] Science, Guangzhou, Guangdong 510640, PR China. Fax: +1 6048222416 Fax: +862087561757 Lawson, Malcolm A., Pest Animal Control Hung, Nguyen Manh, Institute of Agricultural Cooperative Research Centre, Microbiology Science of South Vietnam, Ho Chi Minh City, Department, University of Western Australia, QEII Vietnam. Medical Centre, Nedlands, WA 6009, Australia. Email: [email protected] Email: [email protected] Fax: +84 8 829 7650 Fax: +61893462912

Hung, Nguyen Quy, Institute of Agricultural Science Leirs, Herwig, Danish Pest Infestation Laboratory, of South Vietnam, Ho Chi Minh Vietnam. Skovbrynet 14, DK-2800 Lyngby, Denmark. Email: [email protected] Email: h.leirs@ssLdk Fax: +84 8 829 7650 Fax: +4545 931155

9 Ecologica .. y-based Rodent Management

Leung, Luke K.-P., CSIRO Wildlife and Ecology, Oguge, Nicholas 0., Department of Zoology, GPO Box 284, Canberra, ACT 2601, Australia. Kenyatta University, PO Box 43844, Nairobi, Kenya. Email: [email protected] Email: [email protected] [email protected] Macdonald, David W., Wildlife Conservation Research Unit, Department of Zoology, University of Pech, Roger P., CSIRO Wildlife and Ecology, GPO Oxford, South Parks Road, Oxford, OX1 3PT, UK. Box 284, Canberra, ACT 2601, Australia. Fax: +44 1865 310447 Email: [email protected] Fax: +61 26242 1505 Mak, Solieng, Carnbodia-IRRI-Australia Project (ClAP), PO Box 1, Phnom Penh, Cambodia. Promkerd, Prasarttong, Agricultural Zoology Email: [email protected] Research Group, Division of Entomology and Fax: +85523211728 Zoology, Department of Agriculture, PO Box 9-34, Bangkok 10900, Thailand. Makundi, Rhodes H., Rodent Research Unit, Email: [email protected] Sokoine University of Agriculture, PO Box 3110, Fax: +66 2 9405396 Morogoro, Tanzania. Email: [email protected] Rahmini, Research Institute for Rice, Departemen Fax: +255563748 Pertanian, JI. Raya No. 9, Sukamandi, Subang 41256, Indonesia. Mathews, Fiona, Wildlife Conservation Research Email: [email protected] Cnit, Department of Zoology, University of Oxford, Fax: +62260 520157 South Parks Road, Oxford, OXl 3PT, UK. Email: [email protected] Rakotondravony, Daniel, Departement de Biologie Fax: +44 1865310447 Anirnale, Universite d' Antananarivo, BP 906, Antananarivo, M'ldShanxi Institute of Plant ORSTOM (Institut de Recherche pour le Protection, Chinese Academy of Agricultural Developpement, French Scientific Research Institute Science, Taiyuan, Shanxi 030031, P.R China. for Development through Cooperation), BP 84, Fax: +860351 7127683 Bamako, Mali. Email: [email protected] Nookam, Piyanee, Agricultural Zoology Research Fax: +223227588 Group, Division of Entomology and Zoology, Department of Agriculture, PO Box 9-34, Bangkok Singleton, Grant R, CSIRO Wildlife and Ecology, 10900, Ihailand. GPO Box 284, Canberra, ACT 2601, Australia. Email: [email protected] Email: [email protected] Fax: +66 2 405396 Fax: +61 262421505

10 Author Contact Details

Suasa-ard, Kornkaew, Agricultural Zoology Wang, Quanye, Northwest Plateau Institute of Research Group, Division of Entomology and Biology, Chinese Academy of Sciences, Xining Zoology, Department of Agriculture, PO Box 9-34, 810001, P.R. China. Bangkok 10900, Thailand. Email: [email protected] Wei, Wanhong, Northwest Plateau Institute of Fax: +66 2 9405396 Biology, Chinese Academy of Sciences, Xining 810001, P.R. China. Sudarmaji, Research Institute for Rice, Departemen Fax: +86971 6143282 Pertanian, JI. Raya No. 9, Sukamandi, Subang 41256, Indonesia. Zhang, Zhibin, National Key Laboratory of Email: [email protected] Integrated Pest Management on Insects and Rodents, Fax: +62 260520157 Institute of Zoology, Chinese Academy of Sciences, Zhongguancun Lu #19, Haidian District, Beijing Tan, Tran Quang, Nationallnstitute for Plant 100080, People's Republic of China. Protection, Hanoi, Vietnam. Email: [email protected] Email: tuat®hn.vnn.vn Fax: +8610 62556418 Fax: +84 4 836 3563 Zhong, Wenqin, Institute of Zoology, Chinese van Wensveen, Monica, CSIRO Wildlife and Academy of Sciences, Beijing 100080, People's Ecology, GPO Box 284, Canberra, ACT 2601, Republic of China. Australia. Email: [email protected] Emai]: [email protected] Fax: +861062555689 Fax: +61 262421505 Zhou, Wenyang, Northwest Plateau Institute of Wan, Xinrong, Institute of Zoology, Chinese Biology, Chinese Academy of Sciences, Xining Academy of Sciences, Beijing 100080, P.R. China. 810001, P.R. China. Email: [email protected] Fax: +869716143282 Fax: +86 10 62555689

Wang, Mengjun, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, P.R. China. Fax: +86 10 62555689

11 ACIAR Australian Centre for IPM integrated pest management International Agricultural IRD- Institut de Recherche pour le Research ORSTOM Developpement; the French AHF haemorrhagic fever Scientific Research Institute for AZRG Zoology Research Development through Group (Thailand) Cooperation ClAP Cambodia-IRRI-Australia Project IRRI International Rice Research CRS Catholic Relief Service Institute CSIRO Commonwealth Scientific and LaoPDR Lao People's Democratic Republic Industrial Research Organisation MCMV murine cytomegalovirus (Australia) MIA Murrumbidgee Irrigation Area EBRM ecologically-based rodent (Australia) management PICA Predict, Inform, Control, Assess ECC endogenous circadian clock (strategy) ECTV ectromelia virus RPM rodent pest management EWS early wet season (crop) SNV Sin Nombre virus GMO genetically modified organism TBS trap-barrier system GTZ Deutsche Gesellschaft fUr TBS+TC TBS plus trap crop Technische Z usammenarbeit TBW total body water (German Technical Cooperation) VVIC viral-vectored HFRS haemorrhagic fever with renal immunocontraception syndrome ZP zona pellucida (glycoproteins) HPS hantavirus pulmonary syndrome

12 Species name Common Name Species name Common Name

Acomys cahirinus spiny mouse Hystrix cristata crested porcupine Apodemus agrarius striped field mouse Hystrix indica Indian crested Apodemus flavicolfis yellow-necked field porcupine mouse Apodemus sylvaticus wood mouse; long- Uomys salvin/ Salvin's spiny pocket tailed field mouse mouse Arvicanthis niloticus unstriped grass rat; Nile grass rat Mastomys coucha multimammate rat Mastomys erythroleucus multimammate rat Band/cota bengaJensis lesser bandicoot rat Mastomys huberti multimammate rat Bandicota indica large bandicoot rat Mastomys nataJensis multimammate rat Bandicota savilei Marmota himaJayana Himalayan marmot Bolomys obscurus dark field mouse Meriones unguiculatus Mongolian gerbil; Brachyuromys ramiroh/tra clawedjird Micromys minutus harvest mouse CaJomys callosus "Iaucha grande" Microtus brandti Brandt's vole Calomys musculinus corn mouse Microtus califomicus California vole Castor canadensis North American Microtus fortis oriental vole beaver Microtus mandarinus brown vole Castor fiber Eurasian beaver Microtus oeconomus root vole CiteJ/us dauricus Daure ground squirrel Microtus pennsyJvanicus meadow vole Clethrionomys glareolus bank vole Mus caroli rice mouse Clethrionomys rufocanus red backed vole Mus cervicolor ryukyu mouse Cricetomys gambianus African giant Mus domesticus house mouse pouched rat Mus musculus house mouse Cricetulus barabensis striped hamster Muscardinus aveJ/anarius dormouse Cricetulus Jongicaudatus lesser long-tailed Myocastor coypus coypu; nutria hamster Myospalax baileyi plateau zokor Cricetulus triton rat-like hamster Myospalax fontanieri Chinese zokor Cynomys Judovicianus plains prairie dog Nesokia indica short-tailed Dipodomys panamintinus Panamint kangaroo bandicoot rat rat Nesomys rufus Notomys alexis spinifex hopping Geomys bursarius eastern American mouse pocket gopher; plains pocket gopher Ochotona cansus Gansu pika Gerbil/us nigeriae Nigerian gerbil Ochotona curzoniae plateau pika; black- lipped pika Ochotona daurica Daurian pika

13 Ecologically-based Rodent Management

Species name Common Name Species name Common Name

Oligoryzomys /ongicaudatus long-tailed pygmy rice Rattus rattus diardii Malaysian house rat rat Rattus tanezumi (formerly Philippine rice-field Ondatra zibethicus muskrat Rattus rattus mindanensis) rat Onychomys spp. grasshopper mice Rattus tiomanicus Malayan wood rat Perognathus parvus Great Basin pocket Rattus villosissimus long haired rat mouse Rhabdomys pumilio Peromyscus boym Peromyscus maniculatus deer mouse Sigmodon a/stoni Alston's cotton rat Peromyscus truei big eared cliff Sigmodon hispidus cotton rat; Hispid mouse; Pinyon cotton rat mouse Solomys spp. tree rats Pitymys irene Spa/ax ehrenbergi blind mole-rat Pseudomys sandy inland mouse Suncus murinus common shrew hermannsburgensis Tachyoryctes splendens African mole rat Rattus argentiventer rice-field rat Tatera indica Rattus bowers; Bower's rat Taterillus graciliS gerbil Rattus colletti dusky rat Taterillus petteri gerbil Rattus exu/ans Polynesian rat Taterillus pygargus gerbil Rattus flav{pectus buff breasted rat Thomomys bottae western American Rattus germaini pocket gopher; valley Rattus koratensis Sladen's rat pocket gopher Rattus losea lesser rice-field rat Thomomys talpoides northern pocket Rattus nitidus Himalayan rat gopher Rattus norvegicus Norway rat; brown rat Thryonomys spp. cane rat; cutting Rattus rattoides Synonym for lesser grass rat rice-field rat and Turkestan rat Xerus erythropus ground squirrel Rattus rattus black rat; house rat; roof rat Zygodontomys brevicauda cane mouse

14 HE SEED FOR this book was sown in Morogoro, Tanzania, in 1996, following the strong ecological theme that emerged at an international T workshop: Rodent Biology and Integrated Pest Management in Africa. Herwig Leirs and Grant Singleton were encouraged that the theme of ecologically-based rodent research came through strongly as the future direction for rodent management in developing countries in both Africa and Asia. The opportunity to germinate the seed arose in 1997 when Zhibin Zhang approached Grant Singleton and Lyn Hinds to co-convene an international conference on rodent biology and management. The focus would be broader than the Morogoro workshop and it was obvious that to augment the charm and appeal of Beijing in early autumn, an impressive line-up of international speakers would be required to attract participants to the conference. The Australian Centre for International Agricultural Research (ACIAR), the Chinese Academy of Sciences and the Commonwealth Scientific and Industrial Research Organisation (CSIRO) Wildlife and Ecology each pledged support for the conference. This led to a successful recruiting drive with all the speakers we approached accepting an invitation to present a paper at the First International Conference on Rodent Biology and Management held in Beijing in October 1998. In January 1998, the editors approached ACTAR with the concept of a book on ecologically-based management that would bring together leading researchers of the basic biology of rodents and those charged with developing and implementing management strategies for rodent pests, especially in developing countries. The book consists primarily of a selection of papers presented at the Beijing conference and comprises three sections. Section 1 sets the scene with contributions from leading small mammal biologists interested in theory and current paradigms of rodent biology and management. Section 2 covers state­ of-the-art technologies of the different approaches to management of rodent pests-rodenticides, physical control, urban management and biological control. Section 3 describes regional case studies of rodent pest problems and progress wi th their management for a selection of developing countries in Asia and Africa.

15 Ecologically-based Rodent Management

Internationally, there have been two previous books of note on rodent pest management: one edited by Ishwar Prakash, published in 1988, the other edited by Alan Buckle and Robert Smith, published in 1994. Both provided a good mix of papers on the principles and practices of rodent pest management, and are compulsory reading for students and practitioners of rodent biology and management. Our book differs from these two books in providing a considerably stronger emphasis on (i) ecologically-based management, (H) recent developments in innovative approaches to biological control, and (iii) the problems, progress and challenges of rodent pest management in developing countries. One important element missing in our book, and in the previous two books, is a substantial contribution on rodent management in Central and South America. We hope that this void is filled in the near future. In the interim, we hope that our book is of interest and practical value to researchers in that region of the world. This has been a challenging project with more than half of the contributing authors not having English as their native language. We thank these authors for their perseverance in the face of obvious frustration in not being able to write in Bahasa, Cantonese, Flemish, French, Kiswahili, Lao, Mandarin, Thai, Vietnamese etc. We commend them for their responsiveness to our requests for many points of clarification and in keeping to a tight schedule. All chapters were refereed by two people and then edited. We thank fellow authors for their contributions to the reviewing and editing process as well as David Spratt, Abigail Smith, Wang Zuwang, Lam Yuet Ming, David Freudenberger, Alison Mills, Christopher Hardy and Geoffrey Shellam. The support and enthusiasm of John Copland and Peter Lynch have ensured that the seed of an idea developed into a bountiful crop-a crop which it is hoped will be eyed despairingly by rodents in our ecologically-led quest to battle their impact on our lives.

Grant Singleton LynHinds Herwig Leirs Zhibin Zhang March 1999

16 Grant R. Singleton, Herwig leirs, lyn A. Hinds and Zhibin Zhang

Abstract

Rodent pest management has gone through a period of stagnation mainly because there has been too little research effort to understand the biology, behaviour and habitat use of the species we are attempting to manage. There is a growing demand, particularly in developing countries, for rodent control strategies that either have less reliance on chemical rodenticides or can better target their use. Similar concerns exist with the control of insect and weed pests. This has led to the development of the concept of ecologically-based pest management (EBPM) which builds on the progress made with integrated pest management (lPM). We analyse this idea for rodent pests and provide examples where research on the basic biology and ecology of rodent pests has provided management strategies that are more sustainable and environmentally benign. The theme of ecologically-based rodent management (EBRM) was foremost in our minds when we invited people to contribute to this book. The other significant considerations were a focus on rodent pest management in developing countries and the importance of marrying basic and applied research on rodents. If in developing countries we can foster the importance of population ecology and an emphasis on management directed at the agro­ ecosystem level, then we are confident that the next decade will see rapid advances in rodent pest management.

Keywords

Rodent management; IPM; rodent ecology; ecologically-based rodent management

17 Ecologically-based Rodent Management

INTRODUCTION habitat use of the respective species we are attempting to manage. Armed with such knowledge we will be able to focus on HE GENESIS of this book was a disentangling the major factors that limit the common concern on the lack of growth of pest populations. This requires T progress in rodent pest experimental field studies conducted at an management over the past 20 years in both appropriate scale and for an appropriate developing countries and elsewhere. This length of time. Recently there has been some has occurred despite the advent in the 1970s progress in the assessment of rodent of sophisticated chemical rodenticides and management methods using replicated, effective strategies for their use (see Buckle manipulative field studies based on our 1988; Buckle and Smith 1994). understanding of the ecology of the pest We contend that rodent pest species (e.g. Singleton and Chambers 1996; management has gone through a period of Brown et a1. 1998; White et a1. 1998; Fan et aI., stagnation for four primary reasons. First, Chapter 13), but there is still much to be there has been too great an emphasis on how done. to develop, use, compare and market In the interim, there has been a marked rodenticides, with particular attention on attrition in the number of wildlife commensal rodents in industrialised researchers working on rodent pests. Ishwar countries. In developing countries, on the Prakash (1988) noted this trend in his other hand, the lack of a critical approach to introduction to the pioneering book Rodent the use of rodenticides for particular species Pest Management. has in some instances led to an unreasonable It is also felt that this work ... will trigger more aversion to rodenticide use. Second, the research effort for the benefit of mankind, ... development of rodent control strategies (which) it appears has dampened during the generally has been based on short-term last few years. experiments where immediate declines in Unfortunately, his plea did not arrest this rodent numbers were seen as a success, trend. without much consideration of long-term Since 1993 there has been encouraging consequences or ecosystem effects. Third, evidence of an increase in the number of field studies have rarely progressed beyond young wildlife researchers interested in the alpha-level, descriptive population studies biology and management of rodent pests in (see Krebs, Chapter 2). Fourth, the developing countries. This has been due recommended management protocols have primarily to funding support provided by been too prescriptive. They rarely take into the Australian Centre for International account the particular characteristics of the Agricultural Research in Southeast Asia, the pest species or of the socioeconomic European Union, Belgium and Denmark in constraints of the end-users of the eastern Africa and ORSTOM (French technology. Scientific Research Institute for What has been lacking is a solid Development through Cooperation) in understanding of the biology, behaviour and Western Africa. We are pleased that some of

18 Re-evaluating Our Approach to an Old Problem

these researchers have been able to A meeting on rodent pest management in contribute to this book. Southeast Asia was held in early 1998 at the China, through necessity, also has seen a International Rice Research Institute (IRRI) marked increase in research effort on rodent in the Philippines. Reports of present-day pests. Rodent problems increased in severity rodent problems were presented for in the 1980s resulting in rodent control being Australia, Cambodia, East Africa, Indonesia, listed as one of the top three priorities for the Lao People's Democratic Republic (PDR), national plant protection program in 1985. Malaysia, Philippines, Thailand and Since 1985, rodent control has been listed in Vietnam; the accounts were impressive in three successive national five-year-plans their extent and impact. Rodent problems (1985-1990;1991-1995;1996-2000). There ranged from eruptive populations of mice in are now approximately 100 scientists with south-eastern Australia and rats in the the Chinese Academy of Sciences, Ministry uplands of Lao PDR, to the chronic problems of Agriculture and universities working on that occur annually in the rice fields of most rodent control. Many of these are young Southeast Asian countries. scientists, who received their degree in There were two telling commentaries biology or post-graduate qualifications in from the meeting in the Philippines, which the 1990s. place in context the impact of rodent pests in In this opening chapter we will set the developing countries. One reported that scene with a brief overview of the although rodents were not the most magnitude of the impact of rodent pests, the important pre-harvest pest to Laotian concept of ecologically-based management farmers, they were the pest they felt they had and the aims and structure of the book. the least control over. The other presented losses caused by rodents in Cambodia not in monetary terms but in how much rice could RODENT PESTS -STILL A PROBLEM have been available for annual human The quest to control the depredations of consumption if not for rat depredations. If rodents, especially in agricultural systems, we apply this line of reasoning to Indonesia has been ongoing for thousands of years. where rats cause annual pre-harvest losses Aristotle (384-322 BC) recounts of approximately 17%, then rats consume The rate of propagation of field mice in country enough rice annually to feed more than 25 places, and the destruction that they cause, are million Indonesians for a year. In countries beyond all telling. such as Indonesia, rice provides 50-60% of Although the last 50 years in particular have the daily energy requirements for people. provided good progress with rodent pest In some cases, the 'official' national level management, rural people in many of annual pre-harvest losses caused by countries still rank rodents in the top three of rodents is not high. For example, 3-5% losses their most important pests. Of particular are reported in Malaysia (Singleton and concern are the losses caused in developing Petch 1994) and 1-3% in the Philippines countries where rodents are literally (Sumangil1990; Wilma Cuaterno, April competing with humans for food. 1998, pers. comm.). However, when detailed

19 Ecologically-based Rodent Management

damage assessment is conducted, the centuries, farmers have learned to accept the damage caused by rats generally is more depredations caused by rats. A common severe. For example, Buckle (1994b) reported response is, a conservative loss estimate of 7.3% in the for every eight rows of rice we sow for our entire Penang State of Malaysia. Also, both family, we sow two for the rats. in the Philippines and Malaysia, the patchy Unfortunately, with the increasing nature of rodent damage often results in human population and the shortage of food farmers losing more than 60% of their crop, in developing countries, this level of loss can which means that rodents are still a no longer be tolerated. significant national problem (Lam 1990). In Clearly, rodents are still an important other places, rodent damage may vary problem, and this is without consideration of widely with limited damage in most years, the losses they cause post-harvest, and the and the most extreme losses of more than role they play as reservoirs for debilitating 80% of the harvest in outbreak years (e.g. diseases of humans and their livestock. Boonaphol and Schiller 1996). In countries that live at the brink of subsistence, such IPM, RODENTICIDES AND figures are a constant threat to food security. ECOLOGICALLY-BASED MANAGEMENT This book contains detailed accounts of the magnitude and importance of the impact Integrated pest management (rPM) is simply of rodent pests, particularly in agricultural the integration of a range of management systems. This information in itself is practices that together provide more important because it provides a spotlight on effective management of a pest species than rodent problems that generally have a lower if they are used separately. IPM was profile than insect, weed and disease developed with the aim of promoting impacts on agricultural crops. The latter methods for managing insect pests and plant group of problems has a higher profile for diseases that were least disruptive to the two reasons. One is that, in developing ecology of agricultural systems (Smith and countries, there are many entomologists, van den Bosch 1967). botanists and plant pathologists who are able to identify, quantify and sell the need Ecologically-based pest management for research, education, extension and action In 1996, a review of pest management of in their respective fields. In comparison, insects and weeds by the Board on there are few rodent biologists; most of these Agriculture of the National Research have an entomological training and there is a Council (NRC) of the United States of poor infrastructure for research on rodent America, highlighted that the practice of pests. IPM has generally not been consistent with The second reason is that farmers have a the underlying philosophy of IPM. They stronger identity with rodents than other contend that there has been too much focus pests. Rodents are perceived as 'intelligent' on pest scouting and precise application of pests, which learn to counter whichever pesticides. They argue that there is a need to control measures farmers use. Over the refocus objectives from pest control to pest

20 Re-evaluating Our Approach to an Old Problem

management and this requires greater Also, biological control needs to be emphasis on ecological research and a viewed in the context of ecologically-based systems approach (National Research management of pests because often it is Council 1996). This extension and refocusing limited in its specificity and This is of the ecological aspects of IPM led the NRC supported by a review of one of the success to develop a concept termed' ecologically­ stories of biological control, the weevil­ based pest management' (EBPM). The Cyrtobagous saiviniae, for controlling the fundamental goals of EBPM are threefold. floating fern salvinia (Salvinia molesta). One is to minimise adverse effects on non­ Following its establishment in South Asia in target species and the environment. The 1939, salvinia was spread by man to second is to develop an approach that is Southeast Asia and Australasia. It severely economic for end-users, particularly disrupts the lives of people by forming farmers, in both the developed and dense mats a metre thick, choking slow developing world. The third is to establish moving waterways, rice fields and lakes (see an approach that is durable. Thomas and Room 1986 for details). Efforts The development of IPM for rodents has to develop biological control were thwarted followed a similar path to IPM for insects. initially because the fern was incorrectly The primary foci have been the development identified, resulting in the testing of the of simple monitoring systems to decide wrong herbivores. In 1978, salvinia was whether or not to instigate a baiting found in Brazil where it is relatively rare. campaign, and the development of effective Field studies identified three potential patterns of use for particular rodenticides. herbivores and one of these, C. saiviniae, was Generally, the focus in rodent control has released into a lake in northern Queensland been mostly to achieve a visible increase in and destroyed 30,000 t of salvinia within a mortality, without appropriate attention to year (Room et a1. 1981). other demographic processes or ecological When tested in other waterways the compensation mechanisms. There have been weevil was not a success. Subsequently, a attempts to develop rodent IPM based on an combination of ecological and laboratory understanding of the habitat use and studies revealed that, if the level of nitrogen population dynamics of rodent pests (see was too low in the fern, the weevil Wood and Liau 1984 a,b; Redhead and population declined. Nitrogen was added to Singleton 1989; Whisson 1996; Brown et a1. waterways which increased the weevil ' White et a1. 1998) or the use of population, until it eventually reached a biological control (e.g. Lenton 1980; critical density at which the damage it Singleton and Chambers 1996), but with the caused to the plant resulted in a sufficient possible exception of Rattus tiomanicus in oil increase in nitrogen in the plant itself for the palm plantations (Wood and Liau 1984a,b), weevil population to be self-sustaining these have not been adopted successfully (Room 1990). This was an unexpected result over a large area. The progress of rodent IPM because higher levels of nitrogen generally in Southeast Asia and Australia has been make weed problems worse. The salvinia reviewed by Singleton (1997). story highlights how taxonomic and

21 Ecologically-based Rodent Management

ecological research provided a strong basis (EBRM). The contributions by Pech et al. for a successful systems approach for pest (Chapter 4) and Hinds et al. (Chapter 10) management. further portray the advantage of having a strong ecological understanding of the Ecologically-based rodent biology of both the rodent pest and the management disease agent when developing techniques For rodents, an ecological basis for control for biological control. In this instance, the was suggested many years ago (Hansson focus is on developing fertility control of and Nilsson 1975; see also Redhead and house mice. Without a multi-disciplinary Singleton 1988) but the implementation of approach, the requisite knowledge of those early ideas has been largely reproductive biology, social behaviour overlooked. One success was the eradication patterns and population dynamics of the of coypu (Myocastor coypus), an introduced wild house mouse could not be consolidated rodent pest, in Britain in the 1980s. After to allow full development of a product several decades of unsuccessful control, a which can then be tested for efficacy. new strategy was developed based on a Rodenticide-based control strategies long-term population dynamics study and have a clear need for a good biological basis biological simulations. A complete solution to build upon. Toxicity of active ingredients of the problem was obtained in less than six and bait palatability are obvious factors years through integrating knowledge about which have been studied under laboratory the animal's biology and behaviour with a conditions for many decades (see e.g. Buckle well-organised control scheme with 1994a; Johnson and Prescott 1994). Less attractive incentives for trappers (Gosling common, but equally important, is a proper and Baker 1989). There are other good understanding of how poisons can be examples in the rodent literature which delivered. For example, rodenticides in illustrate the importance of ecological, Hawaiian macadamia orchards were taxonomic and behavioural studies for commonly distributed by broadcasting on developing effective strategies for managing the ground. Recently, population and rodent pests. We provide some further behavioural studies of the black rat, Rattus examples later in this chapter, with more rattus, revealed that those rats which detailed case studies provided in the damage the nuts forage only in the trees. ensuing chapters (Macdonald et aI., Chapter This information led to placement of bait 3; Leung et aI., Chapter 14). stations in trees leading to more efficient use The advantages of viewing biological of rodenticides for controlling damage control of rodents as part of an integrated (Tobin et al. 1997). ecologically-based approach to rodent In China, chemical rodenticides, mostly management rather than a single panacea anticoagulants, are still the routine weapons for control has been reviewed by Singleton for controlling rodents in farmland and and Brown (1999). For simplicity, we grassland. However, such rodent control propose that this strategy be termed campaigns in the absence of a sound 'ecologically-based rodent management' ecological knowledge of the pest species

22 Re-evaluating Our Approach to an Old Problem

have generally only achieved short periods demographic importance of each patch and (6-9 months) of respite from the ravages of the timing and rates of movements by rats the rodents. In the rice fields of southern between patches (Singleton and Petch 1994). China the effects have been even shorter This metapopulation approach to rodent (Huang and Feng 1998). Indeed, many control is achieving more attention (see studies (Liang 1982; Liang et al. 1984; Zhang Smith 1994), but appropriate field studies of 1996; Huang and Feng 1998; Qi et al. 1998) the spatial dynamics of rodent populations have shown that the response of rodent in agro-ecosystems in developing countries populations after chemical control is non­ (e.g. Leirs et al. 1997b) are few. linear. Killing some individuals may reduce the population numbers initially, but the Ethology in rodent pest management remaining animals compensate with better The development of resistance by rodent survival and better breeding performance. pest species to first and second generation For example, following an 88% reduction in anticoagulants explicitly necessitated an a popUlation of the Mongolian gerbil integrated approach to rodent management, (Meriones unguiculatus), the body mass at where use of one poison type was first pregnancy was reduced from 58 g to 35- complemented or alternated with the use of 50 g (Wang et al. 1998). other poison types, physical control In Malaysia, populations of the Malayan methods, exclusion, or other control wood rat (R. tiomanicus) also showed a rapid measures (Greaves 1994). Here again, more population response after control, with a full attention was paid to short-term, and indeed recovery in population density occurring often urgently needed, quick solutions like over 12-18 months. In this case, knowledge changing to a stronger poison. Much less of the population dynamics and factors effort has been directed towards preventing limiting population growth resulted in an the development of, or containing the effective management program of rats in oil geographical distribution of, resistance. So­ palm plantations. Management consisted of called 'behavioural resistance', where an intensive baiting campaign followed by rodents refuse to eat the poisonous baits, recurrent placement of baits every six poses other challenges. In the Birmingham months (see Wood and Liau 1984a). restaurant area, house mice were impossible Re-invasion is another factor resulting in to control until detailed studies revealed that populations returning quickly to pre-control they had difficulties in digesting starch and densities (e.g. Guruprasad 1992). This is were therefore unlikely to eat grain-based particularly a problem in developing baits; changing to fish baits solved the countries where farmers often manage their problem quickly (Humphries et al. 1996). own rodent problems on small plots of land The Chinese zokor (Myospalax fontanieri) (0.25-2 ha) at different times to their provides another practical example of the neighbours. The land use patterns on these importance of understanding rodent small holdings also generally result in a behaviour in developing effective patchy landscape. We therefore need management. In the farmland of Northwest ecological studies to examine the relative Loess Plateau, the zokor, which lives

23 Ecologically·based Rodent Management

underground, shows a cautious response to RE-EMERGENCE OF POPULATION chemical baits. Less than 70% of a zokor ECOLOGY OF RODENT PESTS population can be killed by using the best possible baiting technique for this species: The current book builds on the strong setting baits in their underground tunnels ecological theme that emerged at an (Zou et al. 1998). Further improvement in international workshop on rodent biology this kill rate depends on a better and integrated pest management in Africa, understanding of the behavioural aspects of held in Morogoro, Tanzania, in 1996 (for feeding for this species, particularly in published proceedings see Belgian Journal overcoming its neophobic response to baits of Zoology Volume 127, Supplement). Africa (Zhang and Wan 1997) or perhaps whether is an economically poor continent and they show social learning of food control strategies which rely primarily on preferences (see Galef 1994; Berdoy 1994 for rodenticides are unrealistic. This has reviews). sparked interest in a more integrated A good ecological basis to management ecological approach to rodent pest strategies can help to provide excellent management. One of the conclusions of the rodent damage control without interfering workshop was, however, that such strategies with rodent demography. Wood mice cannot materialise without the availability of (Apodemus sylvaticus) in Germany can be population data from long-term studies lured away from sugar beet seeds during the (more than three years) (Leirs 1997). In West short period after sowing when they are Africa, much iniormation was collected by prone to rodent damage by providing an Hubert and co-workers in the 1970s (e.g. attractive, unpoisoned alternative food in Hubert 1982), while in East Africa it is only the periphery of the fields (Pelz 1989). As all in the past few years that long-term the above examples show, however, ecological studies have begun to provide solutions are often specific and require a insights into the main factors driving rodent detailed knowledge of the biology, ecology population dynamics (Leirs et a1. 1996, and behaviour of the pest species. Obtaining 1997a). Building on these insights, the focus such knowledge is a laborious yet rewarding has now switched to experimental field task that will allow the development of new studies. damage control strategies. The workshop in Morogoro formulated Further examples of the benefits of recommendations, many of which are combining knowledge of the ecology and relevant to the present book (Leirs 1997a). ethology of rodent species for developing The key recommendations are as follows: better integrated control are provided by • The taxonomy of many pest rodents must Santini (1994) for three European species of be clarified so that control actions can rodents in agriculture and forestry, and target the correct species. Buckle et al. (1997) for the Malayan wood rat in oil palm plantations. • Life-history studies and physiological comparisons between these species are imperative.

24 Re-evaluating Our Approach to an Old Problem

.,.,. Experimental ecological studies, properly AIMS AND STRUCTURE OF THE BOOK designed with appropriate controls, must be set up to evaluate management This book has four broad aims: strategies and, in the first place, test our Ill> to raise the profile of the importance of hypotheses (or, rather, unsubstantiated basic research for developing effective, beliefs) about rodent population applied management of rodent pests; dynamics. .,.,. Poisons in this framework are not Ill> to argue the need for an ecologically-based considered as something to avoid, but as approach to rodent pest management; only one of the possible approaches which should be used more effectively and .,.,. to raise the profile of rodent pest integrated with other approaches. management in developing countries; and The development of the concept of EBPM Ill> to spark interest in prospective students in is important, because it builds on the solid a challenging but rewarding field of foundations developed by IPM. In effect, endeavour. EBPM is refocusing IPM towards understanding the population biology of the The book begins with a section on theory pest and the agro-ecosystem in which it and current paradigms of rodent biology lives. From the viewpoint of a population and management. ecologist, one wonders what all the fuss is This section includes contributions from about; EBPM is self-evident. However, when leading small mammal ecologists. Krebs one moves into applied wildlife (Chapter 2) provides a thought-provoking management, especially of rodents, then the paper on the different phases of small need to sell a concept such as ecologically­ mammal ecology and concomitant shifts in based management of rodent pests becomes research paradigms. Macdonald and a reality (Singleton and Brown 1999). coworkers (Chapter 3) present the results of Unfortunately, too often there is a divide a series of novel studies used to disentangle between practitioners, who are more the interesting social behaviour of Norway concerned with the details of how to apply rats. Dickman (Chapter 5) examines, at the specific control technologies, and wildlife ecosystem level, the positive role rodents researchers who focus on understanding the play as 'ecosystem engineers' through their theory and the context of the problem impact on the chemical and structural (Sinclair 1991). We have provided a mix of attributes of the environment. Mills in his pure (Section 1 and parts of 2) and applied chapter on arenaviruses and hantaviruses (Sections 2 and 3) rodent biology in this book (Chapter 6), and Pech and his coworkers in an attempt to bridge this divide. through their synthesis of models for predicting mouse plagues in Australia (Chapter 4), both provide a different perspective of the need for strongly focused population studies of rodents.

25 Ecologically-based Rodent Management

One common theme is addressed by all ecosystems (see contribution by Schiller et authors-the importance of basic research al., Chapter 18). The contributions in this for developing effective management of section comprise a mix of biological studies rodents. aimed directly at management, and general The second section covers broad methods overviews of rodent problems and how they of management-rodenticides, physical are currently being managed in various control and biological control. This section developing countries. provides overviews on the state-of-the-art In seeking contributions for this book we technologies for fertility control (Chambers were heartened by the enthusiasm that it et al., Chapter 10), chemical control (Buckle, generated from researchers across the Chapter 7) and the control of rodent pests in spectrum of pure and applied research. We urban environments (Colvin and Jackson, received no 'knock backs' from contributors Chapter 11). Reviews are provided also on we targeted. Indeed, we had to limit the physical methods of control, particularly in contributions that were on offer. What rice agro-ecosystems in developing pleasantly surprised us was the strong countries (Singleton and coworkers, Chapter interest by 'pure' scientists in hoping their 8) and on the ecological management of work would not only be of heuristic value. Brandt's vole in the grassland of Inner They were keen for their findings to be Mongolia (Zhong and coworkers, Chapter 9). The common theme for this section is accessible to researchers in developing ecologically-based pest management. countries because they felt their research could make a significant contribution to In a conscious effort to ensure the book is tackling the problem of rodent pests in these relevant to developing countries, regional regions. So perhaps Oenis Chitty is indeed case studies of rodent problems and the correct in stating "pure and applied science progress with associated research are differ mainly in aims, not methods". If this provided for Asia and Africa in Section 3. book acts as a catalyst for pure and applied This section has contributions from selected countries edited by G.R. Singleton and Z. scientists to work together towards a Zhang (Asia-contributions from common aim of reducing the impact of Cambodia, China, Indonesia, Lao POR, rodent pests in agricultural ecosystems of Thailand and Vietnam) and H. Leirs developed and developing countries, then (Africa -contributions from Burkina Faso, we will be more than satisfied with our toil. Kenya, Madagascar, Mali and Tanzania). The information on the biology and REFERENCES management of rodent pests in developing countries, and the infrastructure for research Berdoy, M. 1994. Ma king decisions in the wild: and extension, varies considerably. In some constraints, conflicts and communication in countries, such as Cambodia and Lao POR, foraging rats. In: Galef, B.G., Mainardi, M. and Valsecchi, P., ed., Behavioural aspects of the problem is only just being defined and it feeding: basic and applied research in is still not known which species cause the mammals. Switzerland, Harwood Academic major problems in the different agro- Publishers, 289-313.

26 Re-evaluating Our Approach to an Old Problem

Boonaphol, O. and Schiller, J.M. 1996. Rodent Greaves, J.H. 1994. Resistance to anticoagulant problems and research priorities in Laos. rodenticides. In: Buckle, AP. and Smith, RH., Paper for ACIAR Project Planning Meeting ed., Rodent pests and their control. Walling­ on Management of Rodent Pests in Southeast ford, UK, CAB International, Asia, 10-12 January 1996, UPM Malaysia, 197-217. 14p. Gosling, L.M. and Baker, S.J. 1989. The eradica­ Brown, P.R, Singleton, G.R, Dunn, S.C and tion of muskra ts and coypu from Britain. Jones, D.A 1998. The management of house Biological Journal of the Linnean Society, 38, mice in agricultural landscapes using farm 39-51. managment practices: an Australian perspec­ Guruprasad, E.K. 1992. I~einfestation of Bandi­ tive. In: Baker, RO. and Crabb, AC, ed., cota bengalensis (Gray) in irrigated field Proceedings of the 18th Vertebrate Pest habitat. In: Borrecco, J.E. and Marsh, RE., ed., Conference, Costa Mesa, California, USA, 2-5 Proceedings of 15th Vertebrate Pest Confer­ March 1998. Davis, University of California, ence,3-5 March 1992, Newport Beach, 156-159. California. Davis, University of California, Buckle, A.P. 1988. Integrated management of rice 277-279. rats in Indonesia. FAO (Food and Agriculture Hansson, L. and Nilsson, B. (eds) 1975. Biocon­ Organization of the United Nations) Plant trol of rodents. Ecological bulletins, No 19, Protection Bulletin, 36, 111-118. Swedish Natural Science Research CounciL Buckle, AP. 1994a. Rodent control methods: 306p. chemical. In: Buckle, AP. and Smith, RH., Huang, X.Q. and Feng, Z.Y. 1998. Ecology and ed., Rodent pests and their controL Walling­ management strategies for Rattus losea. In: ford, UK, CAB International, Zhibin Zhang and Zuwang Wang, ed., 127-160. Ecology and management strategies of Buckle, A.P. 1994b. Damage assessment and rodent pests in agriculture. Beijing, China damage surveys. In: Buckle, AP. and Smith, Ocean Press, 178-194 (in Chinese). RH., ed., Rodent pests and their control. Hubert, B. 1982. Dynamique des populations de Wallingford, UK, CAB International, 219- deux especes de rongeurs du senegal, Masto­ 248. mys erythroleucus et Taterillus gracilis (Roden­ Buckle, AP. and Smith, R.H. (ed.) 1994. Rodent tia, Muridae et Gerbillidae). I. Etude and their control. Walling ford, UK, demographique. Mammalia, 46,137-166. CAB International,405p. Humphries, RE., Sibly, RM. and Meehan, AI'. Buckle, AP., Chia, T.H., Fenn, M.G.P. and 1996. The characteristics of 'behavioural Visvalingam, M. 1997. Ranging behaviour resistance' and bait avoidance in house mice and habitat utilisation of the Malayan wood in the UK. Proceedings of Brighton Crop rat (Rattus tiomanicus) in an oil palm planta­ Protection Conference-Pests and Diseases, tion in Johore, Malaysia. Crop Protection, 16, 157-164. 467-473. Johnson, RA. and Prescott, CV. 1994. The Chitty, D. 1996. Do lemmings commit suicide? laboratory evaluation of rodenticides. In: Beautiful hypotheses and ugly facts. New Buckle, AP. and Smith, RH., ed., Rodent York, Oxford University Press, 268p. pests and their controL Wallingford, UK, Galef, E.G. Jr 1994. Olfactory communication CAB International, 161-179. about foods among rats: a review of recent Lam, Y.M. 1990. Cultural control of rice field rats. findings. In Galef, E.G., Mainardi, M. and In: Quick, G.R, ed., Rodents and rice. Report Valsecchi, P., ed., Behavioural aspects of and proceedings of an expert panel meeting feeding: basic and applied research in on rice rodent control, 10-14 Sept. 1990. Los mammals. Switzerland, Harwood Academic Banos, Philippines, IRRI (International Rice Publishers, 83-101. Research Institute), 65-72.

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Leirs, H. 1997. Preface. Rodent biology and Redhead, T.D. and Singleton, G.R 1988. The integrated pest management in Africa. PICA Strategy for the prevention of losses Proceedings of the International Workshop caused by plagues of A,ius domesticus in rural held in Morogoro, Tanzania, 21-25 October Australia. EPPO (European Plant Protection 1996. Belgian Journal of Zoology, 127(suppL), Organization) Bulletin, 18, 237-248. 3-5. Room, P.M. 1990. Ecology of a simple plant­ Leirs,H.,Stenseth,N.C, Nkhols,J.D., Hines,J.E., herbivore system: biological control of Verhagen,Rand W.N.1997a. Salvinia. Trends in Ecology and Evolution,S, Seasonality and non-linear density-depend­ 74-79. ence in the dynamics of African Mastomys rats. Nature, 389,176-180. Room, P.M., Harley, K.L., Forno, 1. W. and Sands Leirs,H., Verhagen, R, Sabuni, CA., Mwanjabe, D.P.A. 1981. Successful biological control of P. and Verheyen,W.N. 1997b. Spatial dynam­ the floating weed salvinia. Nature, 294, 79-80. ics of Mastomys natalensis in a field-fallow Santini, L. 1994. Knowledge of feeding strategies mosaic in Tanzania. Belgian Journal of as the basis for integrated control of wild Zoology, 127(suppL), 29-38. rodents in agriculture and forestry. In: Galef, Leirs,H., Verhagen,R, Verheyen, W., B.G., Mainardi, M. and Valsecchi, P., ed., Mwanjabe,P. and Mbise, T. 1996. Forecasting Behavioural aspects of feeding: basic and rodent outbreaks in Africa: an ecological basis applied research in mammals. Switzerland, for Mustomys control in Tanzania. Journal of Harwood Academic Publishers, 357-368. Applied 33,937-943. Sindair, A.RE. 1991. Science and the practice of Lenton, GM. 1980. Biological control of rats by wildlife management. Journal of Wildlife owls in oil palm and other plantations. Management, 55,767-773. Biotrop Publication No. 12,87-94. Liang, J.R 1982. Population recovery of Chinese Singleton, G.R 1997. Integrated management of zokor (Myospalax fantanieri) and plateau pika rodents: a Southeast Asian and Australian (Oci1atona curzaniae). In: Wuping Xia, cd., perspective. Belgian Journal of Zoology, 127, Alpine Gansu, Gansu People's 157-169. Publishing Press, 93-100 (in Chinese). Singleton, G.R and Brown, P.R. 1999. Manage­ Liang, J.R, Zhou, L., Wang, Z.W. and Song, RY. ment of mouse plagues in Australia: integra­ 1984. Mathematical model of population tion of population ecology, bio-control and recovery of Chinese Zokor (Myospalux fOl1 tani­ best farm practice. In: Cowan, D.P. and Feare, eri) and plateau pika (Ochotona curzoniae). c.J., ed., Advances in vertebrate pest manage­ Acta Ecologica Sinica, 4,1-11 (in Chinese). ment. Fiirth, Filander - Verlag, 189-203. National Research Council 1996. Ecologically Singleton, G.R. and Chambers, L.K. 1996. A large based pest management: new solutions for a scale manipulative field study of the effect of new century. Washington, D.C, National Capillaria hepatica on wild mouse populations Academy Press, 144p. in southern Australia. International Journal Pelz, H.-J. 1989. Ecological aspects of sugar beet for Parasitology, 26,383-98. seeds by Apodemus sylvaticus. In: Putrnan, RJ., ed., Mammals as pests. London, Chapman Singleton, G.R. and I'etch, D.A.1994. A review of and Hall, 34-48. the biology and of rodent pests Prakash, I. (cd.) 1988. Rodent pest management. in Southeast Asia. Canberra, ACIAR Techni­ Boca Raton, CRC Press, 48Op. cal Reports No. 30, 65p. Qi,G'x', Yao, W.L., Wang,J. and Yang, B. 1998. Smith, R.H. 1994. Rodent control methods: non­ Research on population dynamics and chemical and non-lethal chemical. In: Buckle, control strategies for rodents in cities and A.I'. and Smith, R.H., ed., Rodent pests and towns of southern China. Acta Therio-Iogica their controL Wallingford, UK, CAB Interna­ Sinica, 18, 226-230 (in Chinese). tional, 109-125.

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Smith, RP. and van den Bosch, R 1967. Whisson, D. 1996. The effect of two agricultural Integrated control. In: Kilgore, W.W and techniques on popu la lions of the canefie Id rat Doutt, RT., ed., Pest control: biological, (Rattus sordidus) in sugarcane crops of north physical, and selected chemical methods. Queensland. Wildlife Research, 23,589-604. New York, Academic Press, 295-340. Wood, B.J. and Liau, 55. 1984a. A long term Sumangil, rp. 1990. Control of rice field rats in the study of Rattus tiomanicus populations in an Philippines. In: Quick, C.R, ed., Rodents and oil palm plantation in Johore, Malaysia. n. rice. Report and proceedings of an expert Recovery from control and economic aspects. panel meeting on rice rodent control, 10-14 Journal of Applied Ecology, 21,465-472. Sept. 1990. Los BaflOs, Philippines, IRRl Wood, B.}. and Liau, 55. 1984b, A long term (International Rice Research Institute), 35-47. study of Rattus tiomanicus populations in an Thomas, P.A. and Room, P.M. 1986. Taxonomy oil palm plantation in Johore, Ylalaysia. Ill. and control of Salvinia malesta. Nature, 320, Bionomics and natural regulation. Journal of 581-584. Applied Ecology, 21, 473-495. Zhang, Z.B. 1996. Techniques and strategies for Tobin, M. E., Sugihara, RT. and Koehler, A.E. rodent control by contraception. In: Zuwang 1997. Bait placement and acceptance by rats in Wang and Zhibin Zhang, ed., Theory and macadamia orchards. Crop Protection, 16, practice of rodent pest management. Beijing, 507-510. Science Press, 367-368. Wang, M.J., Zhong, W.Q. and Wan, X.R 1998. Zhang, Z.B. and Wan, Y.L. 1997. Ten years' Ecology and management strategies for review on rodent pest management in China. Mongolia gerbils (Meriones unguiculatus). In: In: Nou, 0.5, Lou, Z.P., Wan, Y.L. and Tang, Zhibin Zhang and Zuwang Wang, ed., H.Y., ed., Research on agricultural biology Ecology and management strategies of and sustainable development of agriculture. rodent pests in agriculture. Beijing, China Beijing, Science Press, 146-151 (in Chinese). Ocean Press, 225-240 (in Chinese). Zou, B., Ning, Z.D., Wang, T.t. and Chang, W.Y. White, J., Horskins, K. and Wilson, J. 1998. The 1998. Ecology and management strategies of control of rodent damage in Australian Chinese zokor (Myospa/ax jontanieri). In: macadamia orchards by manipulation of Zhlbin Zhang and Zuwang Wang, ed., adjacent non-crop habitats. Crop Protection, Ecology and management strategies of 17,353-357. rodent pests in agriculture. Beijing, China Ocean Press, 41-64 (in Chinese).

29 Section 1

Basic Research - the Foundation for Sound Management

Pure and applied science differ mainly in aims, not methods

Chitty 1.996 Charles J. Krebs

Abstract

Rodent population studies have played a key role in developing our understanding of population dynamics. The proximal stimulus to this understanding is to alleviate problems of rodent pests in agriculture and disease transmission to humans.

Ideas about rodent population dynamics have gone through three phases. In the 1930s there were almost no quantitative data, and population control was believed to be caused by biotic agents that operated in a density-dependent manner. By the 1950s a new paradigm of social control of numbers emerged with emphasis on physiological stress and social aggression within populations. By the 1970s a synthesis of sorts had emerged suggesting that multiple factors caused population changes. Experimental manipulation of field populations in the 1960s enlarged our outlook on the complexities of rodent populations, and the emergence of modelling and rigorous statistical analyses of survival and reproduction in the 1980s and 1990s has shown again that rodents have been the Drosophila of population ecology. But as precision has increased over time, generality and simplicity have declined to near extinction. What is missing and what do we need to do in the next 20 years? Experimentation is the key to understanding, and no study should be undertaken without a clear set of experimental predictions. The era of alpha-level descriptive population studies should be over. We need large-scale, extensive studies coupled with short-term experimental studies. Rodents are good candidates for studies of spatial dynamics, a strongly emerging subdiscipline in ecology. Also, rodent management should focus on the factors limiting populations and use an experimental approach. The era of pest eradication via killing alone should be over and we need to be smarter in developing our management options. The development of genetiC resistance to anticoagulants and chemical poisons is a call to the ecologists of the 21st century to think more clearly about how we might outwit rodent pests. The accumulated knowledge of the phYSiology, behaviour, and genetics of rodents needs to be integrated into our management options. There is much to be done both to understand and to outsmart these clever mammals.

Keywords

Population regulation, population limitation, food, predation, social behaviour, rodents. pest management

33 Ecologically-based Rodent Management

INTRODUCTION strengths and weaknesses, and suggest some paths for future growth.

OPULATION DYNAMICS is WHAT ARE THE PROBLEMS? without question the most highly Ecological questions are complex and one developed of the sub disciplines of P thing we have learned is to ask very specific ecology. From abstract mathematical models questions about populations so that we can to field experiments, ecologists have made answer them clearly. Three major questions progress over the last 50 years in analysing have formed the focus of population population changes in many species. In dynamics (Krebs 1994, p. 322; Krebs 1995): particular, rodents have been model organisms for studies of population ... What stops population growth? dynamics for three reasons. First, they are ... What limits average abundance? conveniently short-lived so that a scientist or a postgraduate student can accomplish ... What constrains geographical something within the constraints of a 3-4 distributions? year time window. Second, they are To find out what stops population ubiquitous, occur in abundance nearly growth, we must compare a growing everywhere, and are relatively cheap to population to one that is not growing, and study, and are often of economic importance the usual approach is to look for some (Singleton et al., Chapter 1). Third, they do factors causing negative feedback in the interesting things such as have population form of density dependence. The second outbreaks that occur frequently enough that question is very broad and is answered by even politicians think that something must the use of the comparative approach in be done about them, at least when they are which a high-density population is superabundant. All these features have compared with a low-density population to combined to produce a very large literature see what factors are associated with the on rodent population dynamics that is observed differences in density. In both somewhat overwhelming to the novice. It is these cases an experimental approach is important therefore to step back and ask useful to answering the question most what we have accomplished with these quickly and avoiding spurious correlations studies, how useful it has been for pest (Underwood 1997). control, and what is to be done next. This Most academic rodent ecologists have book brings together ecologists, addressed the first question-the problem physiologists, and ethologists with a of regulation (Berryman 1986; Sinclair 1989), common interest in rodent biology and thus and this has engendered much discussion provides an ideal time to address these about density dependence in natural larger issues for rodents. populations. Fewer ecologists have worked After a historical overview I will on the second question-limitation of summarise the three current paradigms of numbers, and yet this is the critical question rodent population dynamics, assess their for pest management. In a simple world, the

34 Rodent Population Dynamics

same ecological factors would limit and Uvarov 1931). The winners were the regulate a population, but this has never Nicholsonians with their focus on regulation been found in the real world. Limitation via density-dependent processes, in which often comes from habitat factors that the main agents were predators, parasites, students of regulation seldom consider, as diseases, and food shortage. The habitat was we shall see. In a sense these two aspects of nowhere to be seen, and weather was noise population dynamics correspond to the two for population dynamics. Most of this early statistical concepts of the mean and the discussion was about insect populations, variance of a set of measurements. We shall and rodents were not a part of the be repeating history to complain, as do many discussions. This was an age of data-free statisticians, that scientists are often ecology, and the arguments were typically preoccupied with the mean and tend to theoretical in the bad sense of this word with forget about the variance. no experiments on natural populations The question of what constrains available. I have referred to the Nicholsonian geographic distributions has fallen out of world-view as the density-dependent favour until fairly recently when the paradigm (Krebs 1995). consequences of global warming on north­ It is important to remember that from the south geographical distribution boundaries start all ecologists implicitly believed that a became a hot topic of worry. It is an population can be identified, that important issue that I cannot deal with here, community interactions are all direct and and there has been much discussion of the easily definable, and that population consequences of these biological invasions processes are repeatable in space and in (Ehrlich 1989; Ruesink et al. 1995; Vitousek time. These are three gigantic leaps of faith et al. 1996). that came back later to challenge simplistic models. HISTORICAL OVERVIEW Phase 11 Population dynamics has gone through three phases during the last 75 years. They The second phase of population dynamics have overlapped little in time but have began in the 1940s when ecologists began to phased into one another, with an abundance realise that social processes could affect of outliers of the 'flat-earth' society type that births, deaths and movements. Among the bedevils ecology in general. leaders of this phase were David E. Davis and John Christian in the United States and Phase I Dennis Chitty in England (Christian 1950; Chitty 1952; Davis 1987). Rodents were the The first phase began with the debate in the key to this new phase, which built partly on 1920s and 1930s about the role of biotic and the earlier recognition by some abiotic factors in population regulation. The ornithologists that territoriality could champions were A.J. Nicholson (1933) for regulate the breeding density of some bird the biotic school and a variety of opponents species. Attention turned in this phase to for the abiotic school (e.g. Thompson 1929; studying the physiological and behavioural

35 Ecologically-based Rodent Management

impacts of individuals on one another. One be regulated by the conventional of the early striking experiments was done Nicholsonian predators, parasites, or food on rats in Baltimore by Davis and Christian shortages (Chitty 1960). These studies (1956,1958) who showed that one could interfaced well with emerging work in reduce the population of rats in a city block ethology and behavioural ecology, which by adding rats to the population (Figure 1), a indicated the complex social structure of completely counterintuitive result for the many mammal populations, and the interest 1950s. Social strife for breeding space in population geneticists began to show in the rodents became a hot topic, and John dynamics of natural populations (Ford 1975). Calhoun suggested crowded mice and rats There was, among many ecologists, as potential models for people in cities considerable scepticism that social processes, (Calhoun 1949). Much of this early work was in contrast to the extrinsic factors of done on house mice and rats in enclosures, predators, food supplies and parasites, might and one of the dominant themes of criticism explain changes in numbers. A series of was that these enclosures were very high elegant experiments on bird populations (e.g. density, artificial environments and of little Watson and Moss 1970; Moss and Watson relevance to what went on in natural 1980) helped to convince some sceptics, and populations. parallel work on rodents (e.g. Krebs et a1. Social regulation of population size arose 1969; Tamarin and Krebs 1969; Gaines and as an alternative explanation of population Krebs 1971) strongly supported the concept changes in populations that did not seem to of social limitation of population density.

130

120

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60 0 5 10 15 20 25 30 Week Figure 1. Introduction experiments of Norway rats (Rattus norveg;cus) Into two city blocks in Baltimore in .1954. Adding rats to a stationary population did not increase numbers but caused them to drop (after Davis and Christian .1956).

36 Rodent Population Dynamics

Phase III The solution to these problems is fairly straightforward. We should encourage By 1970 nearly all the ideas about population multifactor models of limited complexity, regulation and limitation were on the table for quantitative predictability, and feasible consideration and a synthesis began by experimental tests. Note that there are two suggesting that everyone might be correct, that distinct types of multi-factor models of multiple factors could be involved in both population limitation. regulation and limitation (Lidicker 1973, 1988). Two developments accompanied this phase of Several independent factors limit population studies. First, experimental testing average abundance of hypotheses in field situations became the The key point in this alternative is that norm in ecology. Second, mathematical the several factors that affect abundance are models began to be applied to specific independent in a statistical sense. In practice questions about rodent systems in order to this means hypothetically that if you change explore assumptions with rigour (e.g. Stenseth factor A and double numbers, and change 1978, 1981b). The question then became how to factor B and triple numbers, you expect that articulate multiple factor hypotheses within if you change both factor A and factor B at the paradigm of experimental ecology. All the same time you will change numbers by ecologists are happy to conclude that the the simple multiple (2 x 3) or 6 times. world is a complex multivariate system, but almost all agree that we must abstract from Several interacting factors limit average this complexity to some order to make abundance progress. This is the most complex alternative Many multiple-factor hypotheses suffer hypothesis since it postulates a statistical from three deficiencies. Excessive complexity interaction between some factors. In practice is the first lethal deficiency. A good example you would recognise an interactive occurs with many flow chart models of explanation by the fact that changing factor population processes. Batzli (1992), for A and factor B at the same time does not example, lists 22 hypotheses for rodent result in their joint effect being predictable. population cycles and gives a complex flow In the above example, changing factor A and chart to illustrate some of the factor B might change numbers much less interrelationships involved. Limited than 6 times, or much more than 6 times. If predictability is a second problem with this hypothesis applies to your rodent multiple-factor hypotheses. It does us no population, interest centres on exactly how service to tell managers that we cannot predict the ecological interaction of factor A and anything about their potential pest problems factor B operates mechanistically. because the world is complex. Third, many A straw poll among rodent ecologists multiple-factor hypotheses are impossible to would probably find most of them test experimentally. Without an experimental supporting multi-factor hypotheses of approach rodent ecology will make little regulation and limitation. If this turns out to progress. be the most frequent model for rodents, it

37

------.... -~.-- ..... ------~-- Ecologically-based Rodent Management

raises the multifactor dilemma that it is rodents eat and how much of it is out there difficult to deal with more than three factors in their habitat. These are themselves in any realistic modeL There are two complex issues since diets change seasonally possible solutions to this dilemma. First, we and may be affected by an individual's sex can hope that all factors operate and age and also by changes in plant independently (hypothesis 1 above), so that productivity from year to year and season to if we have four or five significant factors for season. A test of the food paradigm is done a particular herbivore, the factors do not most easily by supplementing food supplies interact. Second, we can hope that for artificially, although these experiments systems with interactions only two or at themselves can be called into question if the most three factors show interactive effects food given is not adequate nutritionally. (hypothesis 2). The food paradigm cannot be tested as a The recent history of rodent population unit and needs to be applied to specific cases studies has been a history of reduced to make predictions that can be falsified. For generality, increased precision, and example, the average abundance of a rodent decreased simplicity. Philosophers would be pest might be higher where more food is appalled at this, but ecologists should be available. Ecologists often pyramid happy to see us move away from superficial hypotheses about food supplies. A recent generality and simplicity. The touchstone of example is the hypothesis about Lyme our progress must be the management of disease in eastern United States of America rodent pests, and we must try to answer this (Ostfeld 1997; Iones et a1. 1998): food important question: supplies in the form of acorns from oak trees how much have our ivory tower studies of are postulated to limit the average rodents in the laboratory and in the field helped abundance of deer mice (Peromyscus us to solve problems of rodent pests? maniculatus), trigger outbreaks of these mice (when acorn crops are heavy), and regulate THREE CURRENT PARADIGMS density through starvation. Boutin (1990) There are three current paradigms that concluded in his review of feeding represent the dominant focus of work today experiments that, by adding food to on small rodent populations. terrestrial herbivore populations, one could increase density two to three-fold but not

The food paradigm morel so that clearly for some populations food limits density over some restricted The food paradigm states that both the range only. Ecologists tend to despair when quantity and the quality of food supplies their favourite explanation does not apply to regulate rodent population density. Food all species in all situations. We should be supplies also limit the average density of more modest in our aims. Food is clearly one populations, and outbreaks of rodents are of the dominant ecological factors limiting caused by changes in their food supplies. and regulating rodent populations, and the The most important thing you need to know, question is which populations and under under this paradigm, is what do your exactly what conditions.

38 Rodent Population Dynamics

The predator paradigm The usual argument against predation as a regulating factor has been that rodents Many things eat rodents and some ecologists look to these trophic links to explain have such a high rate of reproduction, that it regulation and limitation of populations. is impossible for predators to kill enough of them (e.g. Chitty 1938, 1996; but see The predator paradigm states that mortality Korpimaki and Norrdahl1998). It is caused by predation regulates rodent certainly correct that sufficient numerical populations, that generalist predators limit and functional responses must be present for the average density of populations below the predation to be a potential regulator of limits that might be set by food supplies, and that outbreaks of rodents are caused by rodent populations (Hanski and Korpimaki 1995). From a practical viewpoint the key is predator control activities, artificial or to manipulate predator numbers. For natural. The most important thing you need example, to see if they could reduce crop to know, under this paradigm, is who eats whom in your community. Since this can damage by house mice in Australia, Kay et al. (1994) provided perches in agricultural vary seasonally, and predators are often crops for raptors. The important point is not selective for sex and age groups, obtaining to be convinced that predators are limiting this information with quantitative rigour is not easy. or regulating numbers just because Paul Errington presented the most predators kill many rodents. It is convenient politically to show lots of dead rodents to serious challenge to the predator paradigm our political masters, but scientifically more than 50 years ago by suggesting that dubious to infer from these piles of dead predators consumed only the doomed bodies that predators are helping to alleviate surplus from rodent populations (Errington 1946). This question has been restated more pest problems. recently as the question of whether The social paradigm predation mortality is additive or compensatory (e.g. Bartmann et al. 1992). The social structure of a rodent population Errington suggested that it was often can affect its ecology. The social paradigm compensatory. This question can be states that social interactions between answered directly by removing predators or individuals can lead to changes in indirectly by showing what fraction of physiology and behaviour that reduce mortality is due to predation kills. There are births, and increase deaths, and thereby considerable problems with inferring regulate populations. In particular, predation limitation from predator kills territoriality may limit the average density alone. If territoriality causes dispersal of rodent populations. Outbreaks of rodents movements, or parasites cause debilitation, are postulated in this paradigm to be caused or food shortage causes poor condition, by changes in the social environment (e.g. predators may be the executioners rather Krebs et al. 1995). The social paradigm is the than the primary cause of population least popular of the three paradigms under changes (Murray et al. 1997). which population ecologists operate. This is usually because ecologists assume that the

39 Ecologically-based Rodent Management

social environment is primarily determined sensitive to reductions in k"Cundity rather by habitat which is highly correlated with than increases in mortality rates (Figure 3) food supplies. Thus, for example, food (Stenseth 1981a; Lebreton and Clobert 1991). supplies determine territory size and The fence effect (Krebs et a1. 1969) is one territory size limits population density. The example of an experimental result that was problem is that other factors may influence completely unanticipated by the food or the social behaviour as well, and thus the predator paradigms (Krebs 1996). If fencing linkage of habitat to social processes can be a vole population without altering the food very loose. supply or the predator fauna could produce Practical problems of rat and mouse a 3-4--fold increase in population density, control had highlighted already by the 1940s what role are immigration and emigration that killing of rats and mice often did not playing in population regulation? Lidicker result in control, especially when the pests (1962) had raised this question long ago but were at high density (Chitty 1954, p. 6; Elton few rodent workers have responded to 1954). Achieving controls in rat populations analyse this phenomenon (Ostfeld 1994). has typically involved intensive large-scale Unfortunately if you are interested in pest campaigns of killing rats either directly or by control you do not wish to find a procedure poisoning (see Singleton et aL Chapter 8). that will increase rodent density! My point is Only recently has the possibility of using that surprise results that are unexpected other methods of control like parasites under the conventional wisdom can result (Singleton and McCallum 1990) or from ignoring social processes in rodent immunocontraception (Caughley et aL 1992; populations. Chambers et a1. 1997) been able to be I do not wish to argue the merits of the explored. social paradigm here. The important point The social paradigm has highlighted the for those interested in pest control is role of immigration in local population whether or not it suggests any kinds of dynamics. Removal experiments on rodents manipulations that could reduce pest and other small mammals have illustrated numbers. To date the major contribution of the difficulties of controlling rodents by the social paradigm to rodent pest increasing mortality. Figure 2 illustrates one management has been to show that dispersal of the first experimental field removal and social structure can render useless studies on voles. In spite of very high and simple forms of control via mortality continuous mortality imposed by removals, (e.g. Sullivan and Sullivan 1986). the vole population continued to maintain high density and grow via immigration. OPTIMAL POPULATION STUDIES Sullivan and Sullivan (1986) obtained a Given these three paradigms, what ought we similar result for snowshoe hares. After a to be doing in rodent population studies? series of laboratory and field studies it We can start by asking what an ideal world became clear to ecologists that pest species of population data would look like. It would with high turnover (high reproduction, high have four components. mortality, short generation times) are most

40 Rodent Population Dynamics

700

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500 cO .r: Cii 400 D- .£ Cl) c 300 Q) 0 200

100

0

90

C 60 eQ) Q) 0... 30

0 Nov. Feb. May Aug. Nov. Feb. May Aug. 1962 1963 1964 Figure 2 . A removal experiment on the California vole (Microtus californicus). All adult voles were removed every two weeks from the removal area of 0.8 ha. From November 1962 to July 1963 an average of 62% of the population was removed every two weeks with little impact on population growth because of immigration (after Krebs 1966).

1.00 c 0 .~ 0.75 ii2 0(1j o.~ -.r::: Figure 3 . 0- 0.50 >,3: Relative sensitivity of the population growth _0 :~ rn rate to survival after weaning and to 'Vi 0.25 c fecundity for mammal populations. The Q) shaded area is the zone occupied by many (f) 0.00 rodent pests (modified after Lebreton and 0.0 0.5 1.0 1.5 2.0 Clobert 1991). Generation time

41 Ecologically-based Rodent Management

Time scale obtain this understanding only by having detailed data on individuals. This point is We would like to have data covering at least 10 of the population events shown by the too rarely recognised in pest control studies. species. If we are studying an annual cycle of The critical data needed on individuals rice rats in Indonesia, we would like 10 years depends on the mechanisms proposed to of detailed data to show the kind of variation explain the dynamics. If you are concerned about the role of barn owls as predators we might expect in the system. ,-"'-V1l)l'ol::>l" like to think that they can completely sample causing population changes, YOLlmust the range of behaviours of populations in a measure the difference in rodent numbers few years. We should be more modest. between places with and places without barn owls. If you think infanticide reduces Spatial scale early juvenile survival, you must obtain data on the frequency of infanticidal intrusions in We would like data from many populations different populations (Wolff and Cicirello spread over the geographic range of the 1989). species. The spatial resolution of these data would depend on the covariation among Community scale sites in a given neighbourhood. There are so few data of this type available for small Most rodent studies are single-species population studies but we should consider rodents that it is a necessary part of future that it may be more fruitful to analyse work. In a few cases we have these data­ interactions between species in the house mouse outbreaks in Australia (Mutze 1990), Clethrionomys rufocanus on Hokkaido community as potential influences on (Stenseth et a1. 1996). In particular pest dynamics. We typically think only of predators but should consider parasites and control problems the spatial scale may seem diseases as well (Saitoh and Takahashi 1998). to be irrelevant, but it is not if we remember In most pest rodent studies, competition for that the local spatial scale can also be critical resources between species is presumed to be (Stenseth 1981a). The concern about minimal and single-species interactions are dispersal and population structure has paramount so that these community focused attention on the need to find out interactions can be ignored. Generalist what a local population is and how predators are perhaps the most common extensively we need to manipulate factor operating on small mammals in which populations to solve pest problems (Lidicker community interactions, including indirect 1995). I think it is fair to conclude that effects (Menge 1997), need to be considered. virtually all field studies of small rodents to date have been done on too small a spatial scale. WHAT DO WE HAVE ALREADY? Given this ideal world, we should take stock Individual scale of what we have already accomplished and We need to understand the mechanisms then move on to what we are lacking. Three behind population changes, and we can strengths stand out.

42 Rodent Population Dynamics

.. Population ecologists are fortunate in methods for analysing survival rates are having a set of good quantitative methods available (Lebreton et a1. 1993), and for dealing with the arithmetic of statistical methods for analysing population change. From the Leslie matrix reproductive changes and separating to metapopulation models, there is immigration from births are being quantitative rigour in abundance. The developed (Nichols and Pollock 1990; importance of this is not always Nichols et a1. 1994). We have the appreciated by population ecologists, yet it demographic tools to understand rodent is one of the great intellectual achievements populations with a level of precision that of this century. We can use this arithmetic was not available 25 years ago. to balance the books. If we know the birth rates and death rates of a population (as WHAT ARE WE LACKING? well as immigration and emigration) we I address here six problems that I think are can compute exactly the rate of population central to future studies on rodent increase or decrease. We need to use this populations. They are not in any particular more often to check on our estimates of order of importance, since some are more these parameters (e.g. Haydonet a1.1999). relevant than others to particular situations. For many rodent pests, control through increasing mortality is the only option Good methods for spatial dynamics available. For these cases quantitative demographic models can estimate the One of the contributions of the social mortality required to reduce a population a paradigm to rodent population dynamics specified amount in order to plan an has been the stress on the importance of optimal control program. immigration and emigration for understanding population changes. But we .. Second, we have a set of good paradigms still lack good methods for studying the for analysing population regulation and spatial aspects of populations. Radio­ limitation. I have outlined these above, and telemetry has made it possible to get some others can be articulated. The importance data on individual movements, but we are of being able to articulate clear, testable rarely able to do it on a scale that would be hypotheses is underappreciated in ecology sufficient to get a broad picture of landscape (Platt 1964; Undenvood 1997). Prediction, dynamics. We know too little about how we absolutely essential for scientific should structure our studies of spatial respectability, is almost unknown in processes. Should we have many small population ecology (Peters 1991). trapping grids or a few very large grids? .. Third, we have good field methods for How large an area should we attempt to estimating population parameters to feed study? What fraction of movements that we into quantitative models and into statistical can document are genetically effective (i.e. analysis of our experiments. Population the immigrant individual survives, breeds estimation methods have been extensively and leaves offspring rather than dies after improved (Pollock et a1. 1990), elegant immigrating)? We have much to learn about

43 Ecologically-based Rodent Management

just how to study spatial dynamics logical consequences of assumptions we successfully in rodents, yet spatial processes make in field experiments, and provide a underlie all of the problems of pest quantitative estimation of the anticipated management. If we can reduce rats on one effect sizes. I think it is particularly rice farm, will the neighbouring farms be important that rodent pest control studies affected or not? Much empirical work needs incorporate both adequate controls and to be done on these questions. We can model modelling studies as part of their overall pest populations as metapopulations in approach. space but if we do not know the linkage parameters for these popuiations, our Methods for evaluating weather­ models will not be very usefuL driven hypotheses Climatic change is the wave of the future Long-term experiments on limitation and we should be more concerned that our There are no long term experiments on understanding of rodent systems will be population limitation in any rodent species. transient and modified by weather changes. If we feed a population for two years, we Hypotheses about weather-driven events often get a population increase (Boutin are difficult to test. Post-hoc correlational 1990). What happens if we continue this studies are useful but inconclusive. They test experiment for 10 years? Is the system in more the cleverness of the statistician than equilibrium after two years so that we will the reality of the biological cause. We need to learn nothing more from the longer study? state weather hypotheses clearly so they can There are numerous examples in ecology of be tested next year, not last year, and we short-term effects that were not sustained or need to abide by the simple rules of even were reversed in the longer term experimental falsification when our (Norby et a1. 1992; Wilsey 1996). There are predictions faiL Ad hoc explanations are also many examples from pest control in available by the shipload for ecological which initial encouraging results were systems, and we should not get in the habit followed by failures (DOT resistance, of using them to bailout our failures of anticoagulants). The message is to be understanding. The exact mechanisms by cautious about long-term conclusions. which weather acts on populations need to be determined, since we need to know Good interplay of models and whether births or deaths are driving the field studies change. Many ecologists have lamented the lack of interaction between field ecologists and Economic and environmental modellers (e.g. Kareiva 1989). There are analyses of pest control alternatives signs that this is finally breaking down This is not my area of specialty but I would (Stenseth and Saitoh 1998) but I think it is a like to think that we should aim in pest failure on both sides that holds back control work to achieve the best gain for the progress. Models can help us to explore the least cost-both environmental and

44 Rodent Population Dynamics

economic. If we cannot achieve this, e.g. millennium are three. We need to apply the because the lowest economic cost method insights of theoretical ecology, behavioural produces the highest environmental ecology, physiology, and genetics to rodent damage, we need to state this clearly so that pest problems. A promising start in this the public can make an informed decision direction is immunocontraception, about alternatives. (Chambers et al. 1997; Chambers et al., Chapter 10). We need studies of tropical Strategies for analysing the pest species in varied tropical environments, community of crops since much of our knowledge of rodent In viewing rodent pests as single-species ecology comes from the Temperate Zone (c.f. populations we overlook the broader Leirs et al. 1996). Finally, we need more strategy of looking at the whole community studies of parasites and diseases in field of pests of a particular crop. If the pests are populations. Conventional wisdom suggests truly independent, we can work on them one that they are of little impact on highly fecund by one. But community interactions have rodents, but their potential for biological ways of producing surprises via indirect control is largely untested (d. Singleton and effects (Holt 1987; Menge 1995), and we McCallum 1990). There are many should be preemptive in looking for these experiments waiting to be done and much possibilities. promising modelling ahead with the goal of understanding population processes in rodents and at the same time alleviating the CONCLUSION suffering caused by rodent pests around the The ivory tower of basic research studies on world. rodents has contributed little to the practical successes of rodent pest management, either REFERENCES short or long term. Much more insight has flowed in the opposite direction, and our Bartmann, RM., White, G.c. and Carpenter, L.H. 1992. Compensatory mortality in a Colorado understanding of rodent dynamics has been mule deer population. Wildlife Monographs, greatly improved by the practical studies of 121,1-39. rodent pest control. What basic ecology can Batzii, G.D. 1992. Dynamics of small mammal contribute to pest management is in the populations: a review. In: McCullough, D.R and Barrett, RH., ed., Wildlife 2001: popula­ methods of study needed. The need for clear tions. New York, Elsevier Applied Science, hypotheses, rigorous experimental tests 831-850. based on good knowledge of natural history, Berryman, A.A. 1986. Stabilization or regulation: a sceptical view of existing ideas, and the what it all means! Decologia, 86,140-143. need to measure our successes and Boutin, S. 1990. Food supplementation experi­ failures-all of these features of good ments with terrestrial vertebrates: patterns, problems, and the future. Canadian Journal science should be part and parcel of rodent of Zoology, 68, 203-220. management. Calhoun, J.B. 1949. A method for self-control of The major deficiencies of rodent population growth among mammals living population studies as we move into the new in the wild. Science, 109,333-335.

45 Ecologically-based Rodent Management

Caughley, G., Pech, Rand Grice, D. 1992. Effect Ford, E.B. 1975. Ecological genetics, 4th edition. of fertility control on a population's produc­ London, Chapman and Hall. tivity. Wildlife Research, 19, 623-627. Gaines, MS. and Krebs, CJ. 1971. Genetic Chambers, L., Singleton, G. and Hood, G. 1997. changes in fluctuating vole populations. Immunocontraception as a potential control Evolution, 25, 702-723. method of wild rodent populations. Belgian Hanski, Land Korpimaki, E. 1995. Microtine Journal of Zoology, 127, 145-156. rodent dynamics in northern Europe: param­ Chitty, D. 1938. A laboratory study of pellet eterized models for the predator-prey intera­ formation in the short-eared owl (Asio tion. Ecology, 76, 840-850. flammeus). Proceedings of the Zoological Haydon, D.T., Gillis, E.A. and Krebs, CJ. 1999. Society of London Series A, 108,267-287. Biases in the estimation of the demographic Chitty, D. 1952. Mortality among voles (Microtus parameters of a snowshoe hare population. agrestis) at Lake Vyrnwy, Montgomeryshire Journal of Animal Ecology, 68,501-512. in 1936-9. Philosophical Transactions Royal Holt, RD, 1987. Population dynamics and evolu­ of London, 236, 505-552. tionary processes: the manifold roles of Chitty, D. 1954. Control of rats and mice, vo!. 1. habitat selection. Evolutionary Ecology, 1, Rats. Oxford, Clarendon Press, 305p. 331-347. Chitty, D. 1960. Population processes in the vole lones, CC., Ostfeld, RS., Richard, M,p., Schau­ and their relevance to general theory. ber,E.M.and Wolff,J.o.1998. Chain reactions Canadian Journal of Zoology, 38, 99-113. linking acorns to gypsy moth outbreaks and Chitty, D. 1996. Do lemmings commit suicide? Lyme disease risk. Science, 279, 1023-1026. Beautiful hypotheses and ugly facts. New Kareiva, P. 1989. Renewing the dialogue between York, Oxford Cniversity Press. theory and experiments in population Christian, J.J. 1950. The adreno-pituitary system ecology. In: Roughgarden, J., May, RM. and and population cycles in mammals. Journal of Levin, S.A., ed., Perspectives in ecological Mammalogy, 31, 247-259. theory. New Jersey, Princeton University Davis, D.E. 1987. Early behavioral research on Press, 68-88. populations. American Zoologist, 27, 825- Kay, B.J., Twigg, L.E., Korn, T.]. and Nico!, H.I. 837. 1994. The use of artificial perches to increase Davis, D.E. and Christian, J.J.1956. Changes in predation on house mice (Mus domesticus) by N orwa y ra t popula tions induced by the intro­ raptors. Wildlife Research, 21, 95--106. duction of rats. Journal of Wildlife Manage­ Korpimiiki, E. and Norrdahl, K. 1998. Experi­ ment, 20, 378-383. mental reduction of predators reverses the Davis, D.E. and Christian, J.J. 1958. Population crash phase of small-rodent cycles. Ecology, consequences of a sustained program 79,2448-2455. for Norway rats. Ecology, 39, 217-222. Krebs, C]. 1966. Demographic changes in fluctu­ Ehrlich, P.R 1989. Attributes of invaders and the ating populations of Microtus californicus. invading processes: vertebrates. In: Drake, Ecological Monographs, 36, 239-273, J.A., ed., Biological invasions: a global Krebs, C]. 1994. Ecology: the experimental perspective. New York, John Wiley and Sons, analysis of distribution and abundance. New 315-328. York, Harper Collins. Elton, C 1954. Research on rodent control by the Krebs, CJ. 1995. Two paradigms of population Bureau of Animal Population September regulation. Wildlife Research, 22, 1-10. 1939 to July 1947. In: Chitty, D., ed., Control of Krebs, CJ. 1996. Population cycles revisited. rats and mice, vol. 1. Rats. Oxford, Clarendon Journal of Mammalogy, 77, 8-24. Press, 1-24. Krebs, CJ., Chitty, D., Singleton, G.R and Errington, P.L.1946. Predation and vertebrate Boonstra, R 1995. Can changes in social populations. Quarterly Review ofBiology,21, behaviour help to explain house mouse 144-177,221-245. plagues in Australia? Oikos, 73, 429-434.

46 Rodent Population Dynamics

Krebs, C]., Keller, B.L. and Tamarin, RH. 1969. Murray, D.L., Cary,].R and Keith, L.B. 1997. Microtus population biology: demographic Interacti ve effects of sublethal nematodes and changes in fluctuating populations of M. nutritional status on snowshoe hare vulnera­ ochrogaster and M. pennsylvanicus in southern bility to predation. Journal of Animal Indiana. Ecology, 50, 587-607. Ecology, 66,250-264. Lebreton, J.D.,Pradel, Rand Clobert, J.1993. The Mutze, G.J. 1990. Mouse plagues in South statistical analysis of survival in animal Australian cereal-growing areas. I. Occur­ populations. Trends in Ecology and Evolu­ rence and distribution of plagues. Australian tion, 8, 91-94. Wildlife Research, 16,677-683. Lebreton, J.-D. and Clobert, J. 1991. Bird popula­ Nichols, rD., Hines,] .E., Pollock, K.H., Hinz, RL. tion dynamics, management, and conserva­ and Link, W.A. 1994. Estimating breeding tion: the role of mathematical modelling. In: proportions and testing hypotheses about Perrins, CM., Lebreton, l-D. and Hirons, G., costs of reprod uction with capture-recapture ed., Bird population studies: relevance to data. Ecology, 75, 2052-2065. conservation and management. Oxford, Nichols, J.o. and Pollock, KH. 1990. Estimation Oxford University Press, 105-125. of recruibnent from immigration versus in Leirs, H., Verhagen, R, Verheyen, W., situ reproduction using Pollock's robust Mwanjabe, P. and Mbise, T. 1996. Forecasting design. Ecology, 71,21-27. rodent outbreaks in Africa: an ecological basis Nicholson, A.J. 1933. The balance of animal for Mastomys control in Tanzania. Journal of populations. Journal of Animal Ecology, 2, Applied Ecology, 33, 937-943. 132-178. Lidicker, W.A.J. 1988. Solving the enigma of Norby, RI., Gunderson, CA., Wullschleger, microtine If cycles". Journal of Mamma!ogy, S.D.,O'Neill,E.G.andMcCracken,M.K.1992. 69,225-235. Productivity and compensatory responses of , Lidicker, W.Z.J. 1962. Emigration as a possible yellow-poplar trees in elevated CO2 Nature, mechanism permitting the regulation of 357,322-324. population density below carrying capacity. Ostfeld, RS. 1994. The fence effect reconsidered. American Naturalist, 96, 29-33. Oikos, 70,340-348. Lidicker, W.Z.J. 1973. Regulation of numbers in Ostfeld, RS. 1997. The ecology of Lyme-disease an island population of the California vole, a risk. American Scientist, 85, 338-346. problem in community dynamics. Ecological Peters, RH. 1991. A critique for ecology. Monographs, 43, 271-302. Cambridge, Cambridge University Press. Lidicker, W.Z.J. 1995. The landscape concept: Platt, J.R 1964. Strong inference. Science, 146, something old, something new. In: Lidicker, 347-353. W.Z.J., ed., Landscape approaches in Pollock, KH., Nichols, 1.0., Brownie, C. and mammalian ecology and conservation. Hines, J.B. 1990. Statistical inference for Minneapolis, University of Minnesota Press, capture-recapture experiments. Wildlife 3-19. Monographs, 107, 1-97. Menge, B.A. 1995. Indirect effects in marine Ruesink/ Parker, I.M., Groom, M.J. and rocky intertidal interaction webs: patterns J.L., Kareiva, P.M. 1995. Reducing the risks of and importance. Ecological Monographs, 65, nonindigenous species introductions. 21-74. BioScience, 45, 465-477. Menge, B.A. 1997. Detection of direct versus Saitoh, T. and Takahashi, K 1998. The role of vole indirect effects: were experiments long populations in prevalence of the parasite enough? American Naturalist, 149, 801-823. (Echinococcus multilocularis) in foxes. Moss, Rand Watson, A. 1980. Inherent changes Researches on Population Ecology, 40, 97- in the aggressive behaviour of a fluctuating 105. red grouse Lagopus scoticus popula­ tion. Ardea, 68, 113-119.

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Sinclair, A.RE. 1989. Population regulation in Tamarin, RH. and Krebs, CJ. 1969. Microtus animals. In: Cherrett, J.M., ed., Ecological population biology. H. Genetic changes at the concepts. Oxford, Blackwell Scientific, 197- transferrin locus in fluctuating populations of 24l. two vole species. Evolution, 23, 183-21l. Singleton, G.R and McCallum, H.!. 1990. The Thompson, W.R 1929. On natural control. potential of Capillaria hepatica to control Parasitology, 21, 269-28l. mouse plagues. Parasitology Today, 6, 190- Underwood, A.J. 1997. Experiments in ecology: 193. their logical design and interpretation using Stenseth, N.C 1978. Demographic strategies in analysis of variance. Cambridge, Cambridge fluctuating populations of small rodents. University Press. Oecologia, 33, 149-172. Uvarov, B.P. 1931. Insects and climate. Transac­ Stenseth, N.C 1981a. How to control pest tions of the Entomological Society of London, species: application of models from the 79,1-247. theory of island biogeography in formulating Vitousek, P.M., D'Antonio, CM., Loope, L.L. and pest control strategies. Journal of Applied Westbrooks, R 1996. Biological invasions as Ecology, 18, 773-794. global environmental change. American Stenseth, N.C 1981b. On Chitty's theory for Scientist, 84, 468-478. fluctuating populations: the importance of Watson, A. and Moss, R 1970. Dominance, genetic polymorphism in the generation of spacing behaviour and aggression in relation regular density cycles. Journal of Theoretical to population limitation in vertebrates. In: Biology, 90, 9-36. Watson, A., ed., Animal populations in Stenseth, N.C, Bjornstad, O.N. and Saitoh, T. relation to their food resources. Oxford, 1996. A gradient from stable to cyclic popula­ Blackwell,167-220. tions of Clethrionomys rufocanus in Hokkaido, Wilsey, B.J. 1996. Plant responses to elevated Japan. Proceedings of the Royal Society of atmospheric CO2 among terrestrial biomes. London Series B, 263, 1117-1126. Oikos, 76,201-206. Stenseth, N.C and Saitoh, T. 1998. The popula­ Wolff, J.O. and Cicirello, D.M. 1989. Field tion ecology of the vole Clethrionomys rufoca­ evidence for sexual selection and resource nus: a preface. Researches on Population competition infanticide in white-footed mice. Ecology, 40,1-3. Animal Behaviour, 38, 637-642. Sullivan, T.P. and Sullivan, D.S. 1986. Resiliency of snowshoe hares to population reduction. Journal of Applied Ecology, 23, 795-807.

48 3. The Behaviour and Ecology of Rattus norvegicus: from Opportunism to Kamikaze Tendencies

David w. Macdonald, Fiona Mathews and Manuel Berdoy

Abstract

While rat population management is clearly possible in the absence of a knowledge of rat biology, we aim to show in this review how control is likely to prove more effective if woven into a robust framework of understanding. For example, rats have flexible population dynamics and can delay the onset of fertility in times of food shortage. Detailed observations have demonstrated the presence of stable, near­ linear dominance hierarchies, where male social status tends to be age-related. We discuss how the success of poisoning strategies are crucially dependent on the foraging decisions which are made against this background of dominance hierarchies and competition for mates. Feeding patterns also can be altered in order to avoid predators. Rats are notoriously neophobic, and poor bait uptake is one of the main reasons that control strategies fail. Our review highlights the importance of social cues and Toxoplasma gondii infection in the modulation of neophobic responses. The potential impact of ill-planned rat control operations on the spread of zoonotic diseases is also considered. Finally, we discuss the development of behavioural and physiological resistance by rats in the face of continued poisoning pressure, and the apparent evolution of a new type of resistance which benefits the rat even in the absence of poison.

Keywords

Rattus norvegicus, rats, behaviour, society, neophobia, resistance, disease

49 Ecologically-based Rodent Management

INTRODUCTION diagnosed annually in Asia is doubtless just the tip of an epizootiological iceberg. These threats are not confined to the developing XPLOSIVE DEMOGRAPHY, world: the 1973 wave of deaths through adaptable ecology and hantavirus with pulmonary syndrome E opportunistic behaviour are amongst healthy young Americans led to the capacities that cause rats to rank high discovery of hantavirus in the deer mouse, amongst those mammals that have most Peromyscus maniculatus (Childs et al. 1987). affected the course of human history. Today Hantavirus infection has also been rats exact an immense toll on society discovered in Norway rats in rural Britain worldwide, whether through the costs of (Webster and Macdonald 1995a). prophylactic or remedial control, or through Amongst the diversity of problems disease transmission and damage to crops and stored food. Throughout Southeast caused by rodents, the Norway rat (Rattus Asia, for example, pre-harvest damage norvegicus), ranks high amongst the caused by the rice-field rat, Rattus miscreant species. Originally from Southeast argentiventer, is reckoned to reduce crop Asia, the Norway rat's versatility rivals yields by 17%, a figure which translates into mankind's and our two species have, in the squandered rice requirements of in the company, spread around the globe. order of 20 million people (Singleton 1997). Trawling bibliographic indices reveals that Such losses may also have indirect some 24,000 technical publications refer environmental costs; lower yields forcing annually to R. norvegicus (Berdoy and larger areas into production and accelerating Macdonald 1991). This stunning total is, the cultivation of wilderness with however, neither a fitting tribute to the consequent threats to biodiversity. More fascination of its adaptability nor directly, rats threaten the survival of recognition of the enormity of its pest status; endemic fauna on a number of islands, from rather it stems largely from the utility of its the Galapagos to Guam (e.g. Amarasekare domestic form as a model for studies 1993; Robertson et al. 1994; Cree et al. 1995); ranging from biochemistry to experimental alien species are, second only to habitat loss, psychology. Publications on wild-type the greatest contemporary force for Norway rats largely concern toxicological extinction. Finally, the enormity of the threat studies of candidate poisons, while the posed to humanity by rat-borne disease is behaviour and ecology of the species in the heightened in the context of our huge wild -which is where it actually does populations, rapid transportation and damage-account for scarcely a handful of antibiotic resistance. Amongst the emerging those 24,000 publications annually. Indeed, infectious diseases, the viral haemorrhagic as we shall show, while a little is known of fevers and Lassa fevers add to the already the ecology of wild rats in farmscapes and a lengthy list of blights which can be few cities in a smattering of developed transmitted by rodents. The 200,000 cases of countries, they are perversely unstudied haemorrhagic fever with renal syndrome where they impact the most. Most startling

50 The Behaviour and Ecology of Rattus norvegicus

of all, effectively nothing is known of the hedgerows at his study site in Berkshire biology of the sewer-dwelling rat. (United Kingdom) were either short-lived or Our objective in this chapter is to review were associated with rat colonies in corn­ the behavioural ecology of wild rats, largely ricks or field-barns. He suggested that within the context of our own team's scattered field colonies were themselves findings. Our contention is that while rat ephemeral, but were probably the main control is manifestly possible in the absence reservoirs from which infestation of farm of much knowledge of rat biology, it is likely buildings occurred in the autumn and to be much more effective if woven into a winter. robust framework of understanding. This Colonists tend to be rats that are proposition rests on the oft-proven wisdom approaching, or have recently achieved, of the maxim: 'know thyn enemy'. In sexual maturity (ZapletaI1964). Telle (1966) particular, our aim is to reveal that found that most colonists weighed between seemingly disjunct, and perhaps even 160-250 g, while Farhang-Azad and rarefied, research topics, such as dispersal, Southwick (1979) reported a mean weight of social status, feeding patterns and disease 190 g for 26 rats collected from newly transmission are actually inextricably linked recolonised burrows. Both concluded that in formulating a biological basis for rat emigrants are mainly young animals, but management. neither reported the sex of new colonists. However, Bishop and Hartley (1976) found

POPULATIONS, DEMOGRAPHY approximately twice as many 'new' adult AND DISPERSAL males as females entering their hedgerow population. Similarly, Calhoun (1962) Questions about the population biology of reported that more males than females were Norway rats were at the forefront of ejected, or at least departed, from more mammalian ecology in post-war years, socially stable colonies. Kendall (1984) and thanks to the pioneering work by Elton and Leslie et al. (1952) found that the sex ratio of Chitty (Chitty 1954) and Davies (1949). rats in environments where they breed Considering the enormity of the rat's tended to be biased towards females. agronomic and public health impact, it is Rat population dynamics, and thus the remarkable that the momentum of these success of control operations, are intimately early investigations was soon dissipated. linked with the availability of food supplies. Numerous studies on farmland In the simplest case, bait uptake is most (Errington 1935; Aisenstadt 1945; Emlen et likely when other sources of food are al. 1948; Zap le tal 1964; Hartley and Bishop unavailable. However, we have found that 1979; Brodie 1981; Huson and Rennison food supply, and other environmental 1981; Homolka 1983) in differing temperate factors, also produce concomitant changes in climates indicate that hedges and fields are behavioural and reproductive ecology (D.W. generally a marginal habitat for rats, except Macdonald and M.G.P. Fenn, unpublished when crops are available as food. Middleton data). These changes in turn may be of (1954) noted that all rat infestations in fundamental importance to rat population

51 Ecologically-based Rodent Management

size and to control efforts. We live-trapped changes in breeding activity-pregnant and radio-tracked rats in three contrasting females were generally captured from United Kingdom farmland habitats, all of March until October, and peak numbers of which were surrounded by winter wheat: juveniles were found between November (i) a resource-rich agricultural tip; (ii) a and December (see also Davies and Hall woodland where grain was intermittently 1951; Farhang-Azad and Southwick 1979, provided for pheasants; and (iii) an adjacent, who report a bimodal pregnancy rate, with resource-poor stream bank. Several salient highs in spring and late summer). There is findings emerge. First, and unsurprisingly, also evidence that reproduction ceases in more rats occurred at the farm rubbish tip, cold winters (Leslie et a1. 1952; Andrews et where food was most abundant, and fewest a1. 1972; Lattanzio and Chapman 1980). along a stream where it was most scarce However, in our study (D.W. Macdonald (Figure 1). Second, numbers varied at each and M.G.P. Fenn, unpublished data) site: in general, there was a cycle in rat breeding activity was not simply a function abundance corresponding to seasonal of season but also depended on food

• tip 100 .A. woodland • stream

E Cl ::::J tll 0

20

Jun Dec Jun Dec Jun 1985 1986 1987

Figure 1. Variation in rat abundance across time in three habitats with different food resources. The figure Illustrates that more rats were captured in the resource-rich environment of the tip than in the woodland (moderate food availability) or stream (poor availability of resources). Cyclical fluctuations in abundance were also more marked in the resource-rich environment (D.W. Macdonald and M.G.P. Fenn, unpublished data).

52 The Behaviour and Ecology of Rattus norvegicus

availability. In the woodland site, winter category and therefore were wllikely to have breeding was stimulated by the provision of access to bait points positioned outside their grain in January for the pheasants, with peak home ranges. Within the home range, rats numbers of juvenile rats occurring in the regularly retreat to rest sites (Orians and population approximately three months Pearson 1979; Galef 1988), which in arable later, in March and April. areas tend to be located in hedge bottoms Fertility in both sexes was affected by and banks (Brodie 1981). season. Using perforation as a measure of attairunent of sexual maturity, the median 360 weight of females at perforation at the § rubbish-tip site was higher in the summer ro 0 sample than the winter one. Fertility in U 280 If) If) males was also modulated by season and Q) UJ food supply, with evidence for delayed ~ 200 onset of sexual maturity and facultative E 'mCl cessation of spermatogenesis where food 5: c 120 ro was scarce. For example, males achieved a '6 Q) greater weight before their testes became ~ scrotal in winter than was the case in 40 summer. Similarly, those animals living in the relatively poor environment of the Tip Wood Stream stream delayed sexual maturity until they Figure 2. had achieved a greater weight than their Median weight at which testes became scrotal in counterparts in more productive habitats winter and in summer at sites which differed in (Figure 2) (D.w. Macdonald and M.G.P. resource availability (tip = resource rich, wood = Fenn, lU1published data). Indeed, it was not moderate, stream = poor). The figure illustrates lU1usual for males weighing more than 300 g that males achieved sexual maturity at lower weights in summer than in winter, and also in to have abdominal testes [the median weight resource-rich environments (p < 0.05 for seasonal of rats with scrotal testes reported elsewhere differences, p < 0.001 for resource differences) was 136 g in rural rats (Davies 1949) and 145 (D. W. Macdonald and M.G.P Fenn, unpublished g in rats living around Baltimore zoo data). (Farhang-Azad and Southwick 1979)]. Clearly, the control of food availability may We radio-tracked rats in and around have an important role in maintaining rat farms (Ferm et a1. 1987; Macdonald and Felm populations at manageable levels. 1995). Males ranged widely through the fields when crop cover was available to Movements provide protection from predators [mean Farmland rats may either occupy stable linear home range = 678 111, standard home ranges or travel widely as transients. deviation (SD) = 535]. However, their ranges Hartley and Bishop (1979) estimated that contracted after harvest (90 m, SD = 28.2). three-quarters of rats fell in the former This effect appeared not to apply to females,

53 Ecologically-based Rodent Management

which generally had smaller home ranges. In 1987; Fenn and Macdonald 1987). In addition to farming activity, the absolute summary, where resources were abundant availability of food also influenced home and clumped, rats formed multi-male, multi­ range size. female groups which we suspect defended a Females at the Wytham tip, where food clan territory. In areas with scattered or was plentiful, had linear ranges averaging sparse resources, male movements were only 85 m whereas those based in the consistent with exclusive male ranges with relatively poor environment of the stream access to several females. Insofar as any had a mean home range of 428 m. Similar spatial exclusivity would affect access to results were observed for males (see also baiting stations, the spatial organisation of Taylor 1978; Hardy and Taylor 1979). rat populations is clearly important to Clearly, home range is likely to vary greatly poisoning operations. On one farm we found with circumstances. that almost all radio-tracked rats visited a particular grain mill at some stage; when Social system poison was placed there an estimated 95% of The seminal study of rat society was the population was killed (Fenn et al. 1987). undertaken by Calhoun (1962) working with The sex ratio of the populations along the rats in an outdoor enclosure. He concluded stream was constant, and equal, throughout that social pressures were important in the the year. In contrast, in the wood (around the movement of rats and, specifically, that pheasant hoppers) the sex ratio was subordinate males were forced to migrate significantly skewed: only approximately into less favourable sites, leading to an one fifth of rats captured between January unbalanced sex ratio (as low as 0.38) in good and June were male [X2 = 5.828, degrees of habitats. Similar reports of unbalanced sex freedon (dJ.) = 1, P = 0.016 from January­ ratios in areas suitable for breeding have also March; X2 = 11.765, dJ. = 1, P = 0.0006 from been made by others (e.g. Leslie et al. 1952). April-June]. We conclude that where groups This socially-induced migration away from developed around reliable food supplies, good sites may explain the transient resident males excluded transient incomers, infestation of fields and corn-ricks often whereas these were numerous in passage reported during the summer. Social through the poorly resourced stream habitat. dominance confers feeding priority (Smith et In order to examine further the al. 1991a), greater reproductive access and consequences of ecological variation on success (Gartner et al. 1981; McClintok et al. social structure, we observed several 1982; Adams and Boice 1983, 1989) and colonies of wild Norway rats housed in large reduces susceptibility to adverse conditions outdoor enclosures (c. 266 m 2). In an effort to (Barnett 1955, 1958a; Christian and Davies bring the field into the laboratory, we 1964; Boice 1969). provided rats with problems which they We radio-tracked rats at our three would encounter in the wild, including farmland study sites (D.W. Macdonald and sufficient space, a diverse and multi­ M.G.P. Fenn, unpublished data), and generational social environment and a various other farm situations (Fenn et al. dispersed food supply. Nocturnal

54 The Behaviour and Ecology of Rattus norvegicus

observations showed that rat colonies were resource. Whilst adult male rats were organised into steady, near-linear obviously in competition for food and mates, dominance hierarchies where male social even the lowest subordinates could achieve status tended to be age-related (Berdoy et a1. access to feeding sites by adapting their 1995a). Larger rats stood a better chance of feeding patterns accordingly (Berdoy and winning contests, particularly when Macdonald 1991; Berdoy 1994). Moreover, interacting with unfamiliar individuals, dominant males could not monopolise (Figure 3a). But social status within colonies access to oestrous females (Berdoy et a1. became fixed: the results of earlier 1995b). encounters appeared to determine the In one colony, observations showed that outcome of future ones, and dominant whilst the alpha male enjoyed the highest individuals thus maintained their social number of copulations, there was no status long after initial body weight straightforward correlation between social asymmetries with younger individuals had status and mating success, with some disappeared or even been reversed (Figure subordinates achieving more copulations 3b). In stable groups, therefore, age is often a than individuals far higher in the dominance better predictor of social status than is hierarchy. In another colony, the dominant with the alpha male being smaller than male actually had less mating success than many of its subordinates (see also Calhoun his two immediate subordinates. 1962). Such 'settled dominance' (Berdoy et This state of affairs is likely to be a a1. 1995a) may be found in a variety of other consequence of the rat's mating system and species (e.g. American bison, Rutberg 1983, may even be encouraged by the female's but see Wolff 1988; red deer, Thouless and behaviour. Observations in the naturalistic Guiness 1986; blue-footed booby chicks, environment of our enclosure colonies Drummond and Osorno 1992; see also showed that mating was achieved by a type Huntingford and Turner 1987, for discussion of scramble competition. Males pursued the of endocrine consequences of fighting). In oestrous female wherever she moved rats it may explain why, despite outside her burrow. Females were typically considerable attention, the evidence that in oestrus for one night only, during which dominance is correlated to body weight has they were assiduously followed by a string been conflicting-e.g. Barnett (1958a), of two to three males (up to seven), and Boreman and Price (1972), Nott (1988) and mated repeatedly with several of them. Smith et al. (1994) found a positive Importantly, males had little time to interact relationship whilst Baenninger (1966, 1970), with each other during the pursuit of Boice (1972), Price et al. (1976) and Sridhara oestrous females because they would lose a et al. (1980) did not. mating opportunity, and as a consequence Why do large subordinates seem to even the most dominant males could not accept the status quo rather than challenging monopolise access to the female. smaller dominant individuals? We suspect The scramble amongst males to mate that the costs of escalated aggression are with a female was so intense that it was hard great relative to the value of the contested to detect whether females displayed any

55 Ecologically-based Rodent Management

Figure 3. (a) 40 The effect of body weight • Heavier rat won asymmetry on social • Heavier rat lost dominance in 132 pairs of ns adult male rats. There was a Ul * ** significantly increasing ~ 30

Figure 3.(b) 40 Older rat won The effect of age asymmetry • Older rat lost on social dominance in 132 • pairs of adult male rats. There Ul was a significantly increasing * * *** *** *** ~ 30 effect of age on the chance of

56 The Behaviour and Ecology of Rattus norvegicus

mate selection or whether they mated information to rats (Natynczuk and promiscuously from choice. Macdonald 1994a,b). To test these possibilities we devised an In order to receive an olfactory signal, apparatus which exploited the sexual rats must smell the encoding odour. We dimorphism in size amongst rats; male rats have investigated 'sniffing behaviour' in a were housed in cubicles around a central group of 62 adult rats (Natynczuk and arena in which a female was placed. A Macdonald 1994a,b). Male rats sniffed circular passage permitted the female access frequently at the various body zones of to each male's cubicle, but was too narrow females but there were significant for the male to pass (M. Berdoy et al., differences in the proportions of sniffs unpublished data; C. Rolland et al., directed to the various body zones unpublished data). Observations in thls (F = 38.21, 32, 28 d.f., P = 0.005). The highest 'inverta-brothel' enabled us to see that proportion of sniffs (23%) were to the females clearly exercised mate choice. females' haunches, and this behaviour was Liberated from the constraints of male-male seen whether or not the female rat was competitive behaviour, females formed related or in oestrus. However, the genital enduring bonds with a single male, but region of non-related oestrous females was nevertheless selected to mate promiscuously investigated significantly more frequently (although to a lesser extent) with a small (29% of all sniffs) than the genital region of number of the males available to them. any other group (X2 = 4.642, 1 d.f., P = 0.031 for difference in proportions of sniffs for Social odours non-related oestrous and non-oestrous There is a huge literature on olfactory females). Males tended to sniff the haunch communication amongst rats (e.g. see after sniffing the forequarters, as part of a reviews in Brown and Macdonald 1985). sequence of sniffing along the female's body Following observations of the males' from forequarters to hindquarters. Histology assiduous sniffing of females in our of the skin sebaceous glands indicated that enclosures, and their pursuit of those in the secretory activity of glands in the oestrus, we began to question the significance haunch, but not those in the forequarters, of haunch odour. The scent of rat haunches changed during oestrus (Natynczuk and had at least 22 volatile components, the Macdonald 1994a,b; Natynczuk et al. 1995). proportions of which varied greatly between A male rat will therefore smell a individuals. Although no single compound discontinuity or gradient in scent along the emerged as diagnostic, principal component body of an oestrous female but not a analysis revealed exclusive categories in the dioestrous female. Rats can thus judge a odour profiles of oestrous females and female's reproductive status by calibrating dioestrous females, with the first axis the odour of her haunch against that of her explaining 80% of the variation. Haunch forequarters. odours could, therefore, be separated along The self-calibration model has four biologically meaningful lines, suggesting that advantages: (a) it obviates the need for they had the potential to signal useful learning or inheriting responses to a

57 Ecologically-based Rodent Management

pharmacopoeia of scents; (b) it minimises problems. First, there is significant seasonal the difficulty posed to the recipient by variation in the period for which they must variation, in quality and quantity, between fast during daylight hours. Second, and the odours of different signallers; (c) social correspondingly, they must satisfy their odours are inevitably mixed with variable energy requirements during nights of and copious background smells, and even variable duration. The shorter the night, the one individual's scent may vary over only a more likely there is to be a conflict of interest few days; and (d) it could work not only between feeding and mating, which is also at with complex mixes of chemicals, but also its peak during the shortest summer nights. with single compounds. Self-calibration We attempted to determine how these relies on assessment of the degree of conflicts are resolved. difference between odours for the Long-term monitoring of feeding activity transmission of a signal and therefore might in our colony of wild rats, using a purpose­ apply to a variety of phenomena detailed in built, continuously recording telemetric the literature (Natynczuk et al. 1995). It is device (Berdoy and Evans 1990) showed that currently unclear whether a strategy the adjustment in feeding intensity to employing pheromones could be used to maintain nocturnality (which rose by 65% disrupt rats mating systems and hence between December and June as nights grew control population size. shorter) was not uniform (Berdoy 1994). Rats mainly compensated for the seasonal FEEDING BEHAVIOUR reduction in feeding time by increasing feeding activity during the last quarter of the Foraging decisions must be carried out night (Figure 4). As a result, the distribution against a background of dominance of feeding activity through the night hierarchies and competition for mates. A gradually changed from being roughly foraging rat must make decisions about constant in winter (and comparable to that when to feed, how to structure foraging obtained in the laboratory) to being clearly bouts within its period of activity, and what skewed in summer, with a sharp peak of to eat. Clearly an understanding of foraging activity before sunrise. Feeding during the behaviour is crucial to the development of earlier part of the night remained at the same more effective baiting systems: neophobia, intensity as in winter. Since food availability food preferences and conditioned aversions was kept constant throughout the year why associated with illness may all limit bait did the timing of feeding activity change so uptakes. As Quy et a1. (1992a,b) and Cowan drastically between winter and summer? et a1. (1994) point out, rat control operations First, during the first half of the night, the often fail because of poor bait uptake. rats were generally busy exploring the enclosure and engaging in social activities. Feeding decisions In males, the disruption of feeding was Most wild rat populations are essentially related to the intensity of mating effort nocturnal (Calhoun 1962; Taylor et a1. 1991; which could result in little or no feeding at Berdoy 1994) and therefore face two related the beginning of the night. Such disturbance

58 The Behaviour and Ecology of Rattus norveg;cus

Sunset Sunrise 16

14

12 ?:- ·Ui c 10 QJ C Ol 8 c '6 QJ QJ 6 LL 4

2

Time of day (quarters)

Figure 4. Non·uniform increase in feeding activity in response to shorter summer nights. To control for the 50% reduction in night length between summer and winter, the data for day and night periods have been divided into quarters (Oay =01-04 ; Night =N1-N4) . The significantly greater increase in feeding intensity during the last quarter of the night ( N4, thick arrow) causes an increasingly skewed feeding distribution during short summer nights. Note also the greater proportion of dawn feeding (01) during summer.

was greatest during the summer when disrupted by social living than were males, oestrous females were most n umerous. could be explained in terms of seasonal Whereas the feeding activity of an oestrous variation in night length. female was principally disrupted for that night only, the presence of an oestrous Predator-altered behaviour female affected the feeding activity of each courting male in th.e colony. Whilst radio-tracking wild rats on farms Second, ra ts may have foraged mainly around Oxfordshire, we identified an. during the last portion of the night to time intriguing pop ulation of diurnal rats (FetUl their feeding activity in anti cipation of and Macdonald 1995). The rats occupied a subsequent energy needs (Le Magnen 1985). rnidden on one of five study fa rms. Preswl1ably rats needed to gather reserves Coincidentally, a particularly large number that allowed them to last until the following of signs of the red fox (Vulpes vulpes ) were night, particularly during periods of long also discovered in the vicinity of the midden, daylight hours. Analyses showed that 90% but were more or less absent from the other of the monthly changes in the timing of four sites, at which rats were typically activity in females, which were less nocturnal. We had previously fOLmd that

59 Ecologically-based Rodent Management

wild-caught rats kept in enclosures modified and traffic activity at night, does not appear their foraging behaviour in order to avoid to interrupt the foraging activities of urban areas scented with fox urine, whereas their rats (Takahashi and Lore 1980). activities were unaffected by rabbit urine Interestingly, foxes visited the midden (Berdoy and Macdonald 1991; see Vernet­ primarily to scavenge on farm waste rather Maury et a1. 1968, 1984 for studies on than to feed on rats. Thus the presence of one odorants inducing stress in laboratory prey type (scavenge) increased the mortality rats-some found in fox faeces). We risk to another prey type (rats). therefore hypothesised that the rats at the midden were diurnally active in order to Meal patterns avoid fox predation. Establishing a direct Rats feed in bouts, so the adjustment of food effect of predation, however, required intake to calorific expenditure must be careful study to eliminate two other equally achieved through variation in the size and plausible explanations. First, the activity the frequency of meals. For example, females observed could have been that of low­ forage in many short visits, whereas males ranking animals, forced to be diurnal to use fewer, longer ones (Inglis et a1. 1996). We escape competition with dominants (a therefore examined how the structure of phenomenon observed in our enclosures - feeding itself is influenced by variable night Berdoy 1994). Second, diurnal behaviour length and social pressures (8erdoy 1991, might have been facilitated by the lack of 1994). The feeding of rats in the human disturbance at the site (see Taylor laboratory tend to show a positive 1975). relationship between the size of a meal and Infra-red photo-electric cells revealed the following inter-meal interval (referred to that the rats were active only when the foxes as a 'post-prandial correlation'), but not were absent. Seasonal use of the midden by between the size of the meal and the interval foxes meant that the risk of predation to rats separating it from the previous one (a 'pre­ was greatest in summer, and corres­ prandial correlation') (Figure 5) (see Le pondingly, the rats were most strictly Magnen 1985 for a review). diurnal in summer. The next step was to go Colloquially, this means that rats decide beyond the correlational nature of the on the size of a meal on the basis of how existing data. A fox-free enclosure was built hungry they expect to be, rather than how near the midden and stocked with rats from hungry they are (Snowdon and Wampler the diurnal population. Rats in the enclosure 1974; Le Magnen 1985). A post-prandial should have been able to detect the absence correlation in an individual's feeding pattern of foxes though the lack of odour from fox is generally thought to indicate that the urine and faeces. If rats were diurnally active individual has good control of the onset and to avoid fox predation, then in the absence of termination of its meals. On the other hand, foxes we expected them to revert to an animal that is less able to control the onset nocturnal behaviour. This was exactly what of feeding than its termination is more likely happened (Fenn and Macdonald 1995). In to exhibit pre-prandial correlations. These contrast, disturbance alone, such as human principles have been useful in elucidating the

60 The Behaviour and Ecology of Rattus norvegicus

physiology of feeding in the laboratory, but (post-prandial correlation). Thus, knowledge they also provided a tool for our investigation of the length of time for which a ra t had not of the complex feeding patterns of rats wIder eaten was, counter-inhLitively, a poor natural circumstances. Following Slater predictor of the size of the next meal. Meal (1981), we tested the hypothesis that in size appeared instead to be a refl ection of the predictable environments (s uch as in our rat's anticipated subsequent energy need. enclosure) individuals would be m ore likely Second, the consequences of agonistic and to exhibit post-prandial than pre-prandial mating behaviour were also reflected in the correlations. Subordinates, on the other hand, values of these relationships. As predicted, which may be less likely to control the onset dominant males, 'who benefi ted from a of feeding due to disturbances by dOlll.inant grea ter freedom of access to the feeding sites, individuals, would effectively be Living in an and females (who were less disrupted by lUlcertain environment and should be more agonistic behaviour and matings than males), likely to exhibit pre-prandial correlations tended to regulate their feed in g more closely than would dominants. If so, subordina te and than their subordinates or male cOlmterparts dominant rats might respond differently to (see also Slater 1981 ). Moreover, post­ baiting programs. p randial correlations were more apparent in winter than in Slim mer, supporting the idea that they were less able to regulate theiT meals Meal Pau se Post-prandial when mating was at its peak an d activity was correlation skewed towards a pre-dawn peak. I The extent to which d ietary decisions depend upon the fine structure of feeding, and the consequences of in divid ual

Pause Pre-prandial varia hon - let alone seasonal varia ti on - on correlation d iet selection are rarely considered in the literature on rat nutrition. Ye t these time d ifferences not only constihlte the basis on Figure 5 . which natural selection operates, but they Types of feeding pattern wh ich reflect a food may also relate to the way in which dietary intake regulated from meal to meal. The upper decisions are made (Tempel et a!. 1985; part of the figure illustrates a positive correlation Hayne et al. 1986). They therefore affect the between the size of meal and the foll owing pause. capacity for d iet selection in general, and for The lower part of the figure shows a positive correlation between size of meal and the aversion learning in particular. preceding pause. Neophobia We analysed the feed ing patterns of 12 Thom pson's (1948) early work clearly adult rats (Berdoy 1991, 1993, 1994; Brunton demonstrated neophobia in wild ra ts in 1995). First, the intervals between meals in the response to both new food and to lighting colony of rats appeared, on the whole, to be used to observe his experimental site (see dependant on the size of the preceding meal also Barnett 1958a; Cm,van 1977; Miller and

61 Ecologically-based Rodent Management

Holzmann 1981; Beck et al. 1988 and review been fed ad libitum for two years) in a in Royet 1983). To overcome neophobia, pre­ familiar feeding box when the grain was baiting is now an integral part of most rat­ scented with natural oils. This reaction was poisoning operations. The function of still significant after 40 days. EVt-'!l more neophobia remains unproven, and it may extreme neophobia was noted when a novel have more to do with a general timidity than food was presented. Inglis et al. (1996) with food selection. However, while undertook a similar study, but his rats were neophobia is likely to incur the cost of housed in concrete arenas and did not have avoiding potentially harmless foods, it may lower intakes of novel foods, or of unfamiliar facilitate the rat's ability to associate eating a foods (foods which had previously been novel food with adverse effects sometime familiar, but had not been offered to the rats later (Rozin and Kalat 1972; Nachman and since they were caught). However, the rats Hartley 1975; Rescorla 1980: ability to did make more visits to the new foods, associate illness with toxic food). Given the consuming less per trip. In contrast, the wide range of food qualities which a rat may introduction of a novel food bowl, even encounter, and the intensity of poisoning though it contained familiar food, elicited pressure to which it is subjected, neophobia strong neophobic responses, reducing food is generally assumed to be of adaptive intake to 5% of its previous level. This significance (Rozin 1976). Indeed, neophobia neophobia, while diminished, was still was found to be absent amongst rats of the evident after five days (Cowan 1976 reports Hawea and Breaksea Islands, New Zealand similar results for the black rat, Rattus rattus, (Taylor and Thomas 1993) which were see also Galef and Heiber 1976; Galef 1988). historically uninhabited. In general, non­ We investigated whether rats of different commensal rodent species also only show provenance displayed different levels of weak neophobia (Cow an 1977; Brammer et neophobia. In particular, we compared the al. 1988). The transition from feeding from behaviour of rats which had recently familiar to novel food after a period of survived intensive poisoning on a Welsh neophobia is usually a gradual process farm with those which had been in the (Chitty 1954; Barnett 1975). Wild rats may protected milieu of our enclosure for two initially only sample a small amount of the years (Brunton and Macdonald 1996). The food with amounts taken gradually enclosure rats were descended from the increasing (Thompson 1948; Shepard and survivors of a poisoning treatment in Inglis 1987; but see Beck et al. 1988). Hampshire two years previously. It is difficult to quantify neophobia in rats Hampshire rats had proven notoriously in the field, because of the large number of difficult to poison (Richards 1981; Greaves et potential confounding variables. We al. 1982a,b; Quy et al. 1992b), prompting the therefore designed a series of experiments to hypothesis that they might be unusually measure neophobic responses in wild-caught neophobic. We designed three trials to test rats. The first of these housed rats in large this. First we tested the effect of an outdoor colonies (Berdoy 1994). The rats unfamiliar odour on a familiar object (this avoided familiar foods (on which they had involved handling the food container

62 The Behaviour and Ecology of Rattus norvegicus

without gloves). Next, we tested the effect of 35 replacing a familiar food container with a • Enclosure rats • Wild farm rats novel container while food and odour 30 remained constant. Finally, we tested the

(j) 25 effect of placing a novel food in a familiar 0. E container. In each case a familiar bowl, co Ul 20 .r: containing fa miliar food, was present u co throughout. The latency to feed, when (j) 15 0 confronted with each form of novelty, was ~ 0 10 allocated an ordinal score to indicate the degree of neophobia. The swnmed results 5 from the three experiments were then used to create a 'neophobia index'. A score of 0 0 0 2 3 4 5 6 indicated no neophobia and 6 indicated Neophobia index extreme neophobia. The survivors from the readily controlled Figure 6. Welsh populations were significantly more Percentage of wild farm rats (from populations considered normal to control; n = 30) and neophobic than enclosure rats descended enclosure rats (descended from Hampshire rats; from the problematic Hampsh.ire n = 30) at each index of neophobia, where a score population. Nonetheless, within both the of 0 indicated no neophobia and 6 extreme Hampshire and the Welsh groups were neophobia. Overall, the farm rats were some individ uals that showed no neophobia significantly more neophobic (Mann Whitney U (8% and 10%, respectively), and others that test Z = - 3 .0; p = 0.009). showed extreme neophobia (an index of 6: Hampshire is therefore not explicable by a 4% and 10%, respectively) (Figure 6). fundamental difference in the inh erited level Perh.aps the Welsh farm rats were a of neophobia. In fact, like Quy et al. (1992a), sample of the m ost neophobic individuals we concluded that the difficulty in from the original population, the less controlling the Hampshire ra ts was most neophobic rats having been selected out by likely due to the stable and abwldant source poisoning. The rats born in the enclosure, of food. Various studi.es suggest that the although descended from the survivors of a strongest neophobic reaction in wild rats is poison treatment, had not themselves been to new objects in a fan"liliar environment subject to selection by poisoning and we (Shorten 1954; Covvan and Barnett 1975; hypothesise that they contained the full CmNan 1976, 1977; WaUace and Barnett range of neophobic phenotypes. Thus, the 1990); evidence is acclllmlating that differences in neophobia between the two neophobia is related to the stability of the groups is likely to be due to the presence of a environment (e. g. little neophobia in land­ higher proportion of strongly neophobic rats fill site rats-Boice and Boice 1968) although in the wild-caught population (Richter 1953; unfamiliar areas with new objects are readily Barnett 1958b; MitcheU 1976; Cowan 1977). explored (Barnett and Spencer 1951; Cowan The failure of poison trea tments in and Barnett 1975; Cowan 1977).

63 Ecologically-based Rodent Management

The interplay of conditioned aversion the olfactory information emanating from . and innate neophobia is extremely complex. another rat which has eaten at the novel food Indeed, neophobia may actually assist in the types (the 'demonstrator effect' -Ludvigson development of conditioned aversion, by et a1. 1985; Galef 1988, 1994). However, the making it more likely that a rat will response of the rats receiving these cues remember eating a novel food, and thereby differs according to the state of the associate it with any adverse consequences. 'demonstrator', with a dead animal In the experiments with rats from Wales and producing no effects on food selection. The Hampshire, the temporal patterns of feeding position of the cues is also important: during the night were related to the rat's residues on the anterior of the rat, but not the degree of neophobia (Berdoy 1994; Brunton posterior, will elicit a response in the 1995). Individuals that displayed no 'observer'. These results make functional neophobia were more inclined than most to sense since the contextual clues which restrict their feeding to the end of the night. induce preference are those which These associations are still largely corroborate the circumstantial evidence of mysterious. We can conclude, however, that what the' demonstrators' have eaten. subordinates may be constrained to eating We investigated the demonstrator effect shortly before dawn (Berdoy and in naturalistic circumstances by Macdonald 1991) and may be more likely to manipulating the olfactory information try new foods than dominant individuals emanating from some individuals in one of (Nott 1988). There is also evidence that the two enclosure colonies and evaluating the strength of taste aversions may be consequences on the diet selection of other modulated by circadian rhythms (e.g. wild colony members (Berdoy 1994). In Infurna et a1. 1979). order to produce individuals that exhibited the characteristics of having eaten Social factors in food avoidance cinnamon-scented food, about a dozen Field studies have shown that rat colonies drops of cinnamon oil in suspension in a living in the same area can show substantial sugary solution were deposited on the neck, differences in food preferences not shoulders and near the mouth of 11 adult explicable by availability (Gandolfi and rats (informants) in one colony but not in the Parisi 1973). Subsequent laboratory studies other. In both colonies, the rats were have demonstrated that information about presented with two novel food types: both the toxicity (the 'poisoned partner peppermint and cinnamon-scented wheat effect'-Bond 1984) and palatability of food grain, presented in two pairs of familiar can be transferred from mother to offspring, feeding boxes. Each pair of boxes thus including via the mother's milk (Galef and provided the rats with a choice between the Clark 1972; Hepper 1990). Diet preference two food types (which previous experiments can also be socially induced in adult had shown to be equally palatable to rats). laboratory rats (Galef and Wigmore 1983; To eliminate the possibility that food Posadas-Andrews and Roper 1983). Thus, selection might be caused by neophobia to a rats faced with novel foods are influenced by new site rather than to the new food, the

64 The Behaviour and Ecology of Rattus norvegicus

scented grain was placed in four familiar colony, was recorded continuously using an feeding boxes, previously containing non­ automatic recording system (Berdoy and scented wheat grain. In addition, rats could Evans 1990). feed on non-scented grain in four other Before the trea tment of the informants, familiar feeding boxes distributed rats in both colonies were highly and equally throughout the enclosure. The tin1ing of neophobic to both types of scented grain visits to all feeding sites, as well as the (Figure 7). identity of selected individuals within the

100

Experimental colony c • Control colony roQl 80 • Ql c .~ Cl 60 "0 Ql C Ql U (/) c 0 40 E co c c ·0 20 ~0

0 en C\I en 0 en I'- en C\I en 'I >. >. >. >. C') >. co .8 co co co co .8 "0 "0 .8 "0 .8 "0 .8 "0 C') co (/) C\I co I !:::- >. ~ (/) !:::- ~ C\I !:!2. (/) co >. (/) (/) >. 0 co >. >. co 0 co co 0 0 0

Before experiment After start of experimental feeding

Figure 7. Change in preference for feeding sites in two colonies of wild rats, as expressed by the proportion of cinnamon-scented grain eaten. In the control colony, the introduction of cinnamon and peppermint-scented grain was associated with no change in relative use of feeding sites. However, in the experimental colony which had 'informants' (cinnamon-scented animals) introduced to the colony before the introduction of the scented grain, there was a preference for the cinnamon over peppermint flavoured feeds. This remained statistically significant for two weeks (p = 0.004, permutation test).

65 Ecologically-based Rodent Management

However, following the tainting of the RAT-BORNE DISEASE informants in one colony, their companions showed a significant preference for cinnamon Parasite-altered behaviour over peppermint, whereas no such effect was The problems of controlling rats, many of observed in the control enclosure. The which revolve around neophobia, might informants themselves were equally reluctant seem largely separate from their role as to eat both types of grain at first. disease vectors. However, we have revealed Subsequently, however, the informants too an intimate link between the two, at least began to show a preference for cinnamon, with regard to infection wi th the protozoan perhaps as they in turn were influenced by Toxoplasma gondii (Webster 1994a; Webster et the odours on the rats they had beguiled into al. 1994, 1995; Berdoy et al. 1995b,c; Webster eating cinnamon. It is noteworthy that, and Berdoy 1997). Infection with Toxoplasma although the informants reduced neophobia alters rat behaviour to increase their towards cinnamon, nonetheless both scented susceptibility to predation by domestic cats, grains were largely eschewed by the colonies the parasite's definitive host (Hutchison et which showed a neophobic response that was al. 1969). These behavioural changes also significant for at least 40 days. Indeed, some incidentally increase the likelihood of individuals avoided the scented grains poisoning. Toxoplasma infection of rats is completely. Furthermore, the switch to eating widespread. In a study of English farms, we novel foods did not always occur gradually. found a mean prevalence of 35% among For example, one dominant male, after rural rats (Webster 1994a). Earlier studies avoiding the novel foods for the first five had, by contrast, indicated low prevalence nights, ate the cinnamon-scented grain levels of between 0-10% (Lainson 1957; almost exclusively (90%) on the sixth night. Jackson et al. 1986). The disease is of medical This new diet selection was associated with a and economic importance: human night of intense mating effort from the male, toxoplasmosis in the United States of with no feeding during the first half of the America reputedly accounts for more night, and a characteristic pre-dawn peak of congenital abnormalities than rubella, feeding activity. syphilis and herpes combined (Schmidt and These results draw attention to a number Roberts 1989). In sheep, the annual loss of of other parameters which are likely to lambs due to the infection is an estimated influence diet selection in the wild: 100,000 in England alone (Berverley 1976). neophobia, the level of information, site Yet despite the importance of rats in the diet preference, competition and the timing of of cats, and hence the subsequent feeding (Berdoy 1994). Thus while much opportunities for direct and indirect remains to be discovered, our experiments transmission of Toxoplasma to humans, wild point to the costs and benefits of sociality in rats have until recently been dismissed as decision making. And for a mammal under unimportant to the dissemination of this such heavy poisoning pressure as the rat, disease. The discovery by Webster (1994a) these decisions are of immediate practical that the infection can be perpetuated even in relevance. the absence of cats (the final hosts) (d.

66 The Behaviour and Ecology of Rattus norvegicus

Wallace 1981) by congenital transmission, show an innate avoidance of ca t odom means that rats represent an important (Vernet-Maury et a1. 1984; Blanchard et a1. wildlife intermediate-host reservoir for 1990; Berdoy and Macdonald 1991; Klein et toxoplasmosis. a1. 1994). In our outdoor enclosures, we In evolutionary terms, a parasite's goal is presented adult rats with. areas containing to increase the chances of infective stages one of four distinct odours: the rat's own meeting their host species. One adaptive smell (own straw bedding), neutral smell route to this goal is host-behaviour (water), rabbit odour (rabbit mine) and cat manipulation. An obvious way of facili tating odour (ca t mine). As expected, non-infected Toxoplasma transmission from an inJected rat rats showed a healthy avoidance of ca t­ to a cat is to enhance the rat's acti vity levels: scented areas, visiting them significantl y less cats are attracted to moving objects and than other sites. However, ill accord ance show little interest in stationary ones (Hubel with the manipulation hypothesis, infected and Weisel1962; Leyhausen 1979). A study rats however were Significantly less averse of the activities of 140 rats revealed that and showed no overall avoidance of areas those infected with Toxoplasma were with signs of cat presence. A proportion significantly more active than uninfected even appeared to show a significan t rats (consistent with findings in lab rnice­ preference for the areas scen ted with odoms Hutchison et a1. 1980; H ay et a1. 1983a,b). of predators (M. Berdoy et aI., unpublished This was true both for ra ts that had acquired data). Toxop la sma as adults and for those which 80 had acquired it congenitally. In contrast, rats 70 harbouring parasites with direct life cycles, such as Cryptosporidium parvurn, d id not 60 exhibit any altered activity (Webster 1994b; "0 50 Ql Webster et a1. 1994). To xoplas ma-infec ted U Ql 40 wild rats were also generally less neophobic ~ ~0 of novel foods (see also Stretch et al. 1960a,b) 30 (Figure 8) and, at farmsteads where the 20 majority of the rat population could be 10 sampled, were trapped more quickly than 0 uninfected rats. Furthermore, they were o 2 3 4 5 6 more curious: when one of us stood in the Neophobia index enclosure it turned out that rats infected Figure 8. with approached m ore closely Toxop lasma Prevalence of Toxoplasma-positive rats in each than non-infected animals (Berdoy et al. neophobia index category, where a score of 0 1995b). We further investigated whether indicated no neophobia and 6 extreme neophobia Toxoplasma-inJected and non-infected rats (n = 36). The figure illustrates t hat infected rats differed in their reaction to potential were less neophobic t han non·infected individuals (F • 5.0, P 0.03). predation by cats. It is widely recognised 1 34 = = that rats, including naive laboratory animals,

67 Ecologically-based Rodent Management

Alterations induced by T. gondii infection enhanced by the intensity of the interaction were confined to the predator's odour, as between rats and domestic cats during the both types of rats behaved similarly with last 4,000 years of shared peridomestic respect to areas containing other odours. existence? Is the same behavioural These kamikaze rats were seemingly neither modification found in other murine debilitated nor deranged in other respects. rodents? For example, in scramble competition for mates they secured just as many copulations Rural rat diseases as did lminfected rats, and were of equal social status (Berdoy et a1. 1995b) (cf. Rau We investigated the prevalence of zoonoses 1983,1984; Freeland 1981: infection with in approximately 600 wild Norway rats Trichinella spiralis and Heligmosomoides captured on farms in southern England polygyrus, respectively, prevent dominance (Table 1). Thirteen zoonotic and ten non­ in mice). It seems, therefore, that Toxoplasma zoonotic species of parasite were identified, affects specific behavioural traits likely to many of which had never previously been make rats more susceptible to predation by recorded, or even investigated, in the United the feUd definitive host. According to the Kingdom (Webster and Macdonald 1995a). saying, curiosity mayor may not kill the cat In addition to Toxoplasma gondii, another ... but it is likely to kill the rat! protozoan, Cryptosporidium parVUnl, which This kamikaze tendency raises intriguing causes enteritis and enterocolitis in humans evolutionary questions. Diminished caution and other mammals (Perryman 1990) was of infected rats, a well known for found to be widespread (Webster and their fearfulness of novel stimuli, could Macdonald 1995b; previously reported in arguably enhance the likelihood of their Japan-Iseki 1986). The link between being preyed on by cats. However, domestic cats and wild rats in the diminished neophobia also seems certain to transmission of human disease was make wild rats more prone to poisoning by continued by the discovery of the rickettsian man. If a poisoned rat were more easily parasite, Coxiella bumettii, the causative caught by cats, the parasite would be agent for Q-fever (Webster et a1. 1995b). disadvantaged if the cats then succumbed to Q-fever outbreaks occur sporadically secondary poisoning. Although (Marrie 1990a,b) and no common source has comprehensive vermin control programs been identified. However, cases in humans are a very recent development in are often linked with infection in domestic evolutionary terms, it is reasonable to cats. In contrast, dogs, which occupy a assume that they have already begun to similar peri-domestic niche, are rarely affect the ecology of Toxoplasma carriers of the parasite (Marrie et a1. 1985; transmission. It is also interesting to Baldelli et a1. 1992). An obvious difference consider the antiquity of this parasite­ between the two, which might contribute to altered behaviour; does it have its origins in their radically different likelihood of the predator-prey arms race between wild acquiring C. burnctti, is the much more felids and rats? Has the adaptation been active predatory behaviour of cats.

68 The Beh aviour and Eco logy of Rattus norvegicus

Perhaps the most dramatic find of our unintended) billion-pound experimental surveys was the p resence, for the first tim e in demonstration of evolution in action. Ra ts Europe, of hantavirus antibodies in wild have two main defences against poisoning animals (Webster and Macdonald 1995a). campaigns: increasingly efficient Hantaan viruses cause a group of illnesses in behavioural adaptations, and physiological humans collectively referred to as hantaan resistance to warfarin (Boyle 1960; Greaves fe ver or haemorrhagic fever with renal 1985) and now, at least incipiently, resistance syndrome. Although a harmless, persistent to second generation anticoagulants infection in rodents, the disease may be (Greaves et a1. 1982a; Gill et a1. 1992). extremely serious in humans. The discovery of hantavirus infection reaffirms the need to Table 1. monitor the disease status of wild rats. Prevalence of zoonoses and zoonotic agents in Hantavirus transmission is strongly approximately 600 wild brown rats from farms in associated with intra specific wounding southern England.

(Glass et a1. 1988). It is therefore possible that Zoonoses/Zoonotic Agents % Infected Rats ill-planned control operations which disrupt Ectoparasites the social hierarchy of rat groups, but fail to Reas 100 achieve eradication, could actually increase Mites 6 7 the prevalence of the disease (see Swinton et Lice 38 Ticks 0 a1. 1997). Our surveys also have Helminths demonstrated the importance of confirming Capillaria spp. 23 rat disease status in different environments: Hymenolepis diminuta 22 Leptospira and Salmonella are usually Toxocara cati 15 considered to be highly prevalent among Hymenolepis nana 11 Taenia taeniaeformis 11 wild rats (e.g. Waitkins 1991; ChomeI1992), Bacteria yet the former was relatively rare (14% Leptospira spp. 14 prevalence) and the latter absent among rats Yersinia enterocolitica 11 studied on British farms (Webster et a1. Listeria spp. 11 1995a,c; see Nakashima et a1. 1978). Other Pasteurella spp. 6 Pseudomonas spp. 4 possible reservoirs of these diseases must Borrelia burgdorferi 0 therefore be investigated. Salmonella spp. 0 Protozoa Cryptosporidillm parvllm 63 RAT CONTROL AND THE EVOLUTION Toxoplasma gondii 35 OF RESISTANCE Babesia spp. 0 Sarcocystis spp. 0 Despite prolonged and intensive efforts to Rickettsia eradicate the Norway ra t, the species Coxiella burnetti 34 remains a major pest. Attempts to control rat Virus Hantavirus 4 populations by poisoning tell a story of Cowpox o attacks and counter-attacks, currently unfolding before our eyes in a (largely

69 Ecologically-based Rodent Management

Behavioural resistance the 'resistant' rats were found, tended to be large and surrounded by fields of cereals, As mentioned above, many rats react to and corn is often stored loose in buildings. novel stimuli with extreme caution. Poison This provides an abundant and relatively avoidance is also enhanced by their ability to predictable alternative food supply. Rats associate the metabolic consequences of a living in this environment can therefore food, long after it was ingested, and their 'afford' to be neophobic. By contrast, in mid­ capacity to interpret cues from other group Wales, where rat control by poisoning is members about the safety of foods. With widely held to be successful, farms tend to these phenomena in mind, and observing be smaller with more livestock and less that some rat populations were stored grain. In these less predictable exceptionally difficult to poison (indeed they environments, rats would need to be more seemed not to eat the poison), the idea arose opportunistic. that they might have evolved enhanced behavioural resistance. A notable instance Physiological resistance was the case of rats in Hampshire (Brunton The introduction of the anticoagulant et a1. 1993, see also Greaves et al. 1982b). To poisons, such as warfarin, marked a confirm that the failure of anticoagulant breakthrough in rat control. Due to their poisons in Hampshire was not attributable slow action, there is a reduced likelihood of to physiological resistance, we organised a aversion learning because the animal has control campaign with a non-anticoagulant already ingested a lethal dose by the time the poison, calciferol, to which there is no symptoms of toxicosis develop physiological resistance. Although some rats (e.g. Nachman and Hartley 1975). succumbed, at least 20-50% survived, Warfarin, the most commonly used despite repeated and intimate access to the rodenticide for the last thirty years, is an poisoned bait. Clearly, they were not eating anticoagulant poison which affects the lethal doses. Three, not necessarily biogenesis of blood clotting factors, exclusive, factors might have explained this: ultimately causing death by many small (a) genetically enhanced neophobia; internal haemorrhages. The production of (b) experience; and (c) the stability of the several blood clotting factors is driven by a environment. Our enclosure trials allowed series of reactions where vitamin K is us to discount the genetic explanation for cyclically oxidised and reduced (Bell and hyper-neophobia: as discussed previously, Caldwell1973; MacNicoll1988). A simple the Hampshire rats were actually less vitamin K deficiency or substances neophobic than were survivors from a disrupting the vitamin K cycle-such as poisoning program in Wales. The evidence warfarin -lead to the production of lower instead suggested that the abundant supply levels of blood clotting factors and therefore of alternative food, and the stable to poor coagulation and an increased risk of environment, were more likely explanations haemorrhage. of the rats' reluctance to eat bait (Brunton et The prompt appearance of resistance to al. 1993). The farms in Hampshire, on which warfarin is a compelling example of the

70

------_...... ------The Behaviour and Ecology of Rattus norvegicus

power of natural selection: by 1972, less than selective advantage of heterozygotes two decades after its introduction in (Greaves et al. 1977). This is consistent with England, warfarin resistance was reported in the interpretation that susceptible rats face 12 areas in the United Kingdom (Greaves reduced fitness due to the effects of the and Rennison 1973). poison, and homozygous resistant rats have reduced fitness due to vitamin K deficiency. The costs of physiological resistance Heterozygotes, on the other hand, enjoy an The new benefits enjoyed by resistant rats efficient compromise: they are more involve new costs. In Welsh populations, resistant to warfarin than susceptible rats, where the mechanisms of resistance have while being less subject to vitamin K been best studied, the altered enzyme deficiency than homozygous resistant rats. present in warfarin-resistant individuals, In practical terms, the lower fitness of whilst less affected by warfarin, is also less resistant genotypes (heterozygotes efficient at producing vitamin K (Greaves included) in the absence of poison (Partridge and Ayres 1969). This results in a natural 1979) advocates a temporary relaxation of vitamin K deficiency (Hermodsen et al. 1969) the use of warfarin to reduce the frequency and ultimately a reduced coagulating of resistant individuals (Smith and Greaves activity in resistant individuals. Resistant 1987). rats are in a constant state of vitamin K deficiency and require a greater than normal A new resistance amount of vitamin K in their diet in order to There may be a new strain of resistance retain a normal clotting activity. amongst rats caught in southern England Homozygous resistant rats need even more (Smith et al. 1993). We found that dietary vitamin K than heterozygous heterozygous resistance to warfarin resistant rats (Hermodsen et al. 1969; see also poisoning was much higher than expected Greaves and Ayres 1973; Martin 1973). The amongst 173 rats taken into captivity from costs of resistance are substantial, two poplations which had resisted particularly in homozygotes, and can lead to poisoning in the wild (71 % and 76% were selective deaths during the first few weeks heterozygous resistant, versus expected after birth (Bishop et al. 1977). Even when values of 50% and 49%; p < 0.001 in both sub-lethal, resistance may also affect other cases) (Gill et al. 1992). Moreover, while components of fitness such as growth, social warfarin-resistant rats normally have lower status and reproduction (Smith et al. 1991b). body weights, these animals had slightly These findings are of particular higher than average weights (Smith et al. theoretical and practical relevance because 1993,1994). These results suggest that these the fitness costs incurred by resistant resistant rats, instead of suffering from the animals may affect the rate of spread and expected costs of resistance, benefited from a maintenance of the resistance allele in wild similar if not higher fitness than the populations. Balanced polymorphism in susceptible genotypes, even in the absence of wild rat populations regularly controlled poison. Apart from its theoretical interest, with warfarin suggests the existence of a these results have profound management

71 Ecologically·based Rodent Management

implications. Resistance could lie dormant, if conditions of high food availability suggests not spread, amongst rat populations living that new strategies are needed to in warfarin-free environments, ready to complement lethal control operations. counteract renewed poisoning efforts Similarly, we have demonstrated that rats (Berdoy and Smith 1993). Nothing is yet may be less important than generally known about the physiological basis of this thought in the transmission of certain potentially fascinating new development in zoonoses (for example Salmonella sp. and the chemical arms race between humans and Leptospira sp.), but that consideration must rats, but our results suggest that rats may now be given to their role in the currently be ahead in that race. transmission of diseases such as Q-fever.

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77 Ecologically-based Rodent Management

Quy, RJ., Cowan, D.P., Haynes, P., Inglis, LR Schmidt, C.D. and Roberts, L.S. 1989. Founda­ and Swinney, T. 1992a. The influence of tions of parasitology, 4th edn. London, Times stored food on the effectiveness of farm rat Mirror /Mosby, College Publishing, 750p. control. In: BCPC Conference-Pests and Shepherd, D.s. and Inglis, LR 1987. Feeding Diseases. Thornton Health, UK, BCPC behaviour, social-interactions and poison bait (British Council of Pest Control) Publications, consumption by a family group of wild rats 291-300. living in semi-natural conditions. In: Lawson, Quy, RJ., Shepard, D.s. and Inglis, LR 1992b. T.J., ed., Stored products pest control. Thorn­ Bait avoidance and effectiveness of anti­ ton Health, UK, BCPC (British Council of Pest coagulant rodenticides against warfarin and Control) Publications, 97-105. difenacoum-resis tant popula tions of Norway Shorten, M. 1954. The reaction of the brown rat rats (Rattus norvegicus). Crop Protection, 11, towards changes in its environment. In: 14-20. Chitty, D., ed., The control of rats and mice, 2. Rau, M.E. 1983. Establishment and maintenance Oxford, Clarendon Press, 307-334. of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology, Singleton, C.R 1997. Integrated management of 86,319-322. rodents: a Southeast Asian and Australian perspective. Belgian Journal of Zoology, 127, Rau, M.E. 1984. Loss of behavioural dominance 157-169. in male mice infected with Trichinella spiralis. Parasitology, 88, 371-373. Slater, P.J.B. 1981. Individual differences in Rescorla, RA 1980. Pavlovian second-order animal behaviour. Perspectives in Ethology, conditioning: studies in associative learning. 4,35-49. Hillside, Lawrence Earlbaum Associates. Smith, P., Berdoy, M., Smith, RH. and Macdon­ Richards, C.C.J. 1981. Field trials ofbromadi­ aId, D.W. 1993. A new aspect of resistance in olone against infestations of warfarin-resist­ wild rats: benefits in the absence of poison. ant Rattus norvegicus. Journal of Hygiene, 86, Functional Ecology, 7, 190-194. 363-367. Smith, P., Berdoy, M. and Smith, RH. 1994. Richter, c.P. 1953. Experimentally produced Body-weight and social dominance in antico­ behaviour reactions to food poisoning in wild agulant-resistant rats. Crop Protection, 13, and domesticated rats. Annals of the New 311-316. York Academy of Science, 56, 225-239. Smith, P., Smith, RH. and Sibly, RM. 1991a. Robertson, H.A, Hay, H.J., Saul, E.K. and Pulsed baiting: laboratory evidence for McCormack, C.V. 1994. Recovery of the behavioural exclusion in wild rats. In: kakeroi: an endangered forest bird of the Fleurat-Lessard, F. and Ducom, P, ed., Cook Islands. Conservation Biology, 8, 1078- Proceedings of the 5th International Confer­ 1086. ence on Stored Product Protection, Bordeaux, Rozin, P. 1976. The selection of food by rats, France, September 1990, 1517-1526. humans and other animals. Advances in the Smith, P., Townsend, M.C. and Smith, RH. Study of Behaviour, 6, 21-76. 1991b. A cost of resistance in the brown rat: Rozin, P. and Kala t, J. 1972. Specific hungers and reduced growth rate in warfarin-resistant poison avoidance as adaptive specializations lines. Functional Ecology, 5, 441-447. of learning. Psychology Review, 78,459-486. Smith, RH. and Creaves, J.H. 1987. Resistance to Royet, J.P. 1983. Les aspects comportementaux anticoagulant rodenticides: the problem and de l'aversion conitionee et de la neophobia. its management. In: Donahaye, E. and L'annee Biologique, 22, 113-167. Navarro, S., ed., Proceedings of the 4th Inter­ Rutberg, AT. 1983. Factors influencing national Conference on Stored-Product dominance status in American bison cows Protection, Tel Aviv, Israel, September 1986. (Bison bison). Zeitschrift Tierpsychologie, 63, Bet Dagon, Israel, Agricultural Research 206-212. Organisation, 302-315.

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Snowdon, CT. and Wampler, RS. 1974. Effects Telle, H.J. 1966. Beitrag zur Kenntis der of lateral hypothalmic lesions and vagotomy Verhaltensweise von Ratten, vergleichen on meal patterns in rats. Journal of Compara­ dargestelt bei Rattus l10rvegicus und Rattus tive and Physiological Psychology, 87, 399- rattus. Angewandte Zoologie, 53, 129-196 409. (MAFF Tolworth translation, Rodent Sridhara, S., Narasimham, AV. and Krishna­ Research reprint 4489). moorthy, RV. 1980. Aggressive interactions Tempel, D.L., Shor-Posner, G., Dwyer, D. and among wild and domestic rodents. Proceed­ Leibowitz, S.F. 1985. Nocturnal patterns of ings of the Indian Academy of Science macronutrient intake in freely feeding and (Animal Science), 89, 351-357. food deprived rats. American Journal of Physiology, 256, R541-R548. Stretch, RG.A., Leytham, G.W.H. and Kershaw, W.E. 1960a. The effect of acute schistosomia­ Thompson, H.V.1948. Studies of the behaviour sis upon discrimination learning and activity of the common brown rat: 1. Watching in mice. Annals of Tropical Yledicine and marked rats taking plain and poisoned bait. Parasitology, 54, 476-486. Bulletin of Animal Behaviour, 6, 2-40. Stretch, RG.A, Leytham, G.W.H. and Kershaw, Thouless, CR and Guiness, F.E.1986. Conflict W.E. 1960b. The effect of acute schistosomia­ between red deer hinds: the winner always sis upon learning in rats under different levels wins. Animal Behaviour, 34, 1166-1171. of motivation. Annals of Tropical Medicine Vernet-Maury, R, Le Magnen, J. and Chanel, J. and Parasitology, 54, 487-492. 1968. Comportement emotif chez le rat: influ­ SwintonJ., Tuyttens, F., Macdonald, D.W., ence de l'odeur d'tm predateur et d' un non­ Nokes, D.T., Cheeseman, CL. and Clifton predateur. Paris, CR Acadamie Scientifique, Hadley, R1997. A comparisonoffertility and 267,331-334, lethal control on bovine tuberculosis in Vernet-Maury, E., Polak, E.H. and Demael, A. badgers: the impact of pertubation. Transac­ 1984. Structure-activity relationship of stress­ tions of the Royal Philosophical Society Series inducing odomants in the rat. Journal of B, 352, 619-631. Chemical Ecology, 10, 1007-1017. Takahashi, L.K. and Lore, RV. 1980. Foraging Waitkins, S.A. 1991. Rats as a source of and food hoarding of wild Rattus l10rvegicus in leptospirosis-Weil's disease. Sorex Techni­ an urban environment. Behavioural and cal Paper No. 4. Cheshire, Sorex Ltd. Neural Biology, 29, 527-531. Wallace, G.D. 1981. Re: 'association of cats and Taylor, K.D. 1975. An automatic device for toxoplasmOSiS'. American Journal of Epide­ monitoring small mammal traffic on miology, 113, 198-201. runways. Journal of Zoology (London), 176, Wallace, RJ. and Barnett, S.A. 1990. Avoidance of 274-277. new objects by the black rat, Rattus rattus, Taylor, K.D. 1978. Range of movement and activ­ after object presentation and change. Interna­ ity of common rats (Rattus norvegicus) on tional Journal of Comparative Psychology, 3, agricultural land. Journal of Applied 253-265. Ecology, 15, 663-677. Webster,J.P. 1994a. Prevalence and transmission Taylor, K.D., Fenn, M.P.G. and Macdonald, D.W. of Toxoplasmagondii in wild brown rats, Rattus 1991. Common rat. In: Corbett, G.B. and norvegicus. Parasitology, 108,407-411. Harris, S.H., ed., Handbook of British Webster, J.P.1994b. The effect of Toxoplasma mammals. Oxford, Blackwell Scientific Publi­ gondii and other parasites on activity levels in cations, 248-255. wild and hybrid Rattus norvegicu5. Parasitol­ Taylor, RH. and Thomas, B.W. 1993. Rats eradi­ ogy, 110, 583-589. cated from Breaksea Island (170HA), Fiord­ Webster J. and Berdoy, M. 1997. Toxoplasma land, New Zealand. Biological Conservation, gondii in Rattus nomegicus: characteristics and 65,191-198. evolution of parasite-altered behaviour. In:

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Holland, S., ed., Modern perspectives on Webster, lP. and Macdonald, D.W. 1995a. zoonoses. Dublin, Royal Irish Academy, 115- Parasites of wild brown rats (Rattus norvegi­ 121. cus) on UK farms. Parasitology, 111, 247-255. Webster, J.P., Brunton, c.P.A. and Macdonald, Webster, J.P. and Macdonald, D.W. 1995b. D.W. 1994. Effect of Toxoplasma gondii on Cryptosporidiosis reservoir in wild brown neophobic behaviour in wild brown rats, rats (Rattus norvegicus); first report in the UK. Rattus Parasitology, 109, 37-43. Epidemiology and Infection, 115,207-209. Webster, J.P., Ellis, W.A. and Macdonald, D.W. Wolff, J,O. 1988. Maternal investment and sex­ 1995a. Prevalence of Leptospira in wild brown ratio adjustment in American bison calves. rat (Rattus norvegicus) populations in the UK. Behavioural Ecology and Sociobiology, 23, Epidemiology and Infection, 114, 195-201. 127-133 Webster, J.P., Ellis, W.A. and Macdonald, D.W. Zapletal, M. 1964. On the occurrence of the 1995b. Prevalence of Leptospira and other brown rat (Rattus nOIVegicus, Berk.) under zoonoses in wild brown rats on UK farms. natural conditions in Czechoslovakia. Zool. Mammalia, 59, 615-622. Listy, 13, 125-134. Webster, J.P., Uoyd, G. and Macdonald, D.W. 1995c. Q-fever (Coxiella humetti) reservoir in wild brown rat (Rattus norvegicus) popula­ tions in the UK. Parasitology, 110,31-35.

80 Roger P. Pech, Greg M. Hood, Grant R. Singleton, Elizabeth Salmon, Robert I. Forrester and Peter R. Brown

Abstract

In this chapter, the main features of current models for predicting the dynamics of house mice (Mus domesticus) populations are reviewed and an assessment made of their data requirements and their ability to contribute to the effective management of mice in Australia. In addition , recent progress with quantifying aspects of the dynamics of mouse populations in the MalJee region of Victoria is described. Robust predictive models are required for the effective management of mice because plagues (massive eruptions of mice) occur at irregular intervals and farmers require early warning to implement control techniques and prevent economic losses. Nine published models have been produced for the plague-prone regions of southern and eastern Australia. Two of these aim to predict the occurrence of plagues at a regional level and five predict changes in the abundance of mice at a district, or local, scale. However, none of the current models for southern Australia include estimates of the numerical response of mouse populations. This limits their value for assessing the relative merits of control programs and new control techniques. A model of the numerical response of mice was developed using observations of the abundance of mice over a 15-year period in the Victorian Mallee region. Rates of increase per 40 days were calculated from the smoothed abundance data and related to (i) estimates of food availability from cereal crops and grazed pasture and (ii) a density-dependent factor representing the effects of predation, disease and intrinsic regulatory processes such as dispersal and social organisation. Although the model represents reasonably welJ the main features of plagues, the strong seasonal variation in the modelled food supply is not matched by changes in the abundance, or rate of increase of mice, in non-plague years. These seasonal effects are likely to be more important in future models for survival and fecundity rates.

Keywords

Mus domesticus, population dynamics, predictive models, rate of increase, density­ dependence, predator-regulation , disease, management

81 Ecologically-based Rodent Management

INTRODUCTION The different dynamics imply that the major regulating factors are not lmiform between regions. HE INTRODUCE D house mouse There are at least nine models, with T (Mus domes ticus ) is a major pest in varying degrees of predicti ve ability, which the grain-growing regions of describe the development of mouse plagues southern and eastern Australia. A wide in Australia (Figure 1, Box 1). They include range of climate, soils and farming regimes two broad-scale, regional models that rely results in regional differences in the on environmental or production data, five population dynamics of mice and in the district and small-scale models that describe opportunities for their management. For in detail the processes of plague formation, example, the Darling Downs in Queensland and two simplified 'process' models experiences relatively frequent outbreaks in focusing on one or more mechanisms tha t contrast to the wheat belt of New South might influence the ra te of change of mouse Wales, Victoria and South Australia where ablmdance. The main fea tures of these occasional severe eruptions are interspersed models are reviewed and their usefulness for with long periods of low abw1dance of mke. predicting mouse plagues is compared.

Northern Territory

Queensland

Western 1. Darling Downs ,~------~---, , Australia , 2. Macquarie Valley South Australia 3. Murrumbidgee Irrigation Area (MIA) 30°8 4. Mallee 5. Turretfield

Grain production areas prone to • mouse plagues o \:, Tasmania\] 40°8

1400E I 1500E I

Figure 1. Grai n production areas of Australia that are prone to mouse plagues. The numbered locations correspond to the 'district' models listed in Box 1.

82 Models for Predicting Plagues in Australia

The model for predicting the onset, Depending on time lags in the responses of magnitude and duration of eruptions of mice predator populations, the suggested in the cereal production areas of the mechanism of a drought-induced reduction Victorian Mallee is based on a IS-year data in predation appears to be the converse of set that has tracked four major outbreaks of the predation-regulation model (below) and mice. In this paper we assess the usefulness the explanation offered by Newsome and of simple food-resource models for Corbett (1975) for a delayed response of predicting the numerical response of mice mice to favourable conditions in central during the period from 1983 to 1997. Australia. The emphasis on drought as a Potential areas for future development of the causal factor also has been criticised by model for the Victorian Mallee are discussed, Redhead (1982) on the grounds that it is particularly in relation to assessing confounded with the effects of drought­ management options including the use of breaking winter-spring rainfalL fertility controL In its present form, the NSW and Victoria regional model is probably too vague to REVIEW OF CURRENT MODELS FOR provide a prediction which can be the basis MOUSE PLAGUES of management actions. The rainfall data on which the model is based are readily Broad-scale models available but the most appropriate definition New South Wales (NSW) and of a severe drought may require some Victoria regional model clarification. Saunders (1986) did not specify Saunders and Ciles (1977) reviewed the when mouse populations should be historical records of mouse plagues from monitored to verify the long-term prediction 1900 to 1970 for northern NSW, southern from the modeL If coupled with additional NSW and northern Victoria. Despite the surveys, the model's predictions, in the form difficulties in using consistent definitions of conditional probabilities suggested by for plagues and droughts, they found a Hone (1980), might constitute the first stage strong positive correlation between of a plague warning system. eruptions of mice and the occurrence of a South Australia regional model severe drought one or two years earlier. The Mutze (1989) documented the distribution model was not tested statistically but it can and frequency of mouse plagues in South provide very early warning of a potential Australia from 1900 to 1984. These data were mouse plague. Predictions could be verified used first by Veitch and Anderson (1985), later by monitoring mouse populations and then Mutze et al. (1990), to examine the (Saunders 1986). Saunders and Giles relationships between the occurrence of suggested several processes that might be mouse plagues and a range of independent responsible for the observed correlation. variables including monthly rainfall, soil Few data are available to test their type, temperature indices and grain 'pathogen' hypothesis (see Singleton 1985). production.

83 Ecologically-based Rodent Management

Box 1. Summary of the main features of the current models for mouse plagues. The events leading to a plague are listed In approximate chronological order for each category of model. However, not all models include each of the steps. The locations of the regional and district models are shown in Figure 1.

(a) Regional models to predict the occurrence of plagues for:

• New South Wales and Victoria (NSW & V) (Saunders and Giles 1977) • South Australia (SA ) (Mutze et al. 1990) Sequence of events:

1. A low-yield crop (~ drought) two years prior to the plague. (SA ) 2. A severe drought (leading to a reduced regulatory effect of disease and/or predation) followed by one or two years with good winter-spring rain. (NSW &V) 3. A special sequence of ra infall events in the 12 months preceding the plague. (SA) 4 . High-yield crop in the summer prior to a plague in autumn. (SA, NSW & V) (b) District models used to predict of the abundance of mice for:

• Turretfield (T) (Newsome 1969a) • Murrumbidgee Irrigation Area (MIA) (Redhead 1982) • Victorian Mallee (VM) (Singleton 1989) • Darling Downs (DD) (Cantrill 1992) • Macquarie Valley (MqV) (Tw igg and Kay 1994) Sequence of events: 1. Good autumn rain two years prior to plague to extend the breeding season into winter. (MIA) 2. Mice disperse from refuges to other favourable areas during t he summer breeding season on e year prior to the pl ague. (MIA) 3. High autumn-winter rainfa ll in the year preceding the pl ague. (VM) 4. High abundance of female mice in a wide range of habitats in the spring prior to t he plague year. (MIA) 5. Correct sequen ce of rainfall eve nts to provide bu rro win g and nesting sites in cracking soils. (T, MqV, DD) 6 . Favoura ble climatic conditions over the summer (a high-yield summer crop) in the pl ague year. (T, MIA , VM. MqV. DD) (c) Process models for the regulation of mouse populations:

• Predator-regulation (P-R) (Sinclair et al. 1990) • Regulation by disease (R-O) (McCallum and Singleton 1989; Shellam 1994) Conditions that prevent a plague: 1. Aggregation of predators in habitats with hi gh mouse nu mbers (e.g. irrigated crops) due to low abundance of mice in surrounding areas. (P-R) 2. Density-dependent increase in the prevalence of lethal or sterilising pathogens. (R-O) Conditions that all ow a pl ague: 1. Wi despread favourable cli matic conditions re su lting in dispersed populations of prey and predators. (P-R) 2. A long delay in a density-dependent increase in the prevalen ce of pathogens or the prevalence is independent of density. (R-O)

84 Models for Predicting Plagues in Australia

The probability of a plague in the (following) total (over-winter) rainfall during the autumn was found to depend on (i) the growing season [Cornish et al. (1980), as difference between grain production in the reported in Mutze et al. (1990), found that current year and that two years earlier, (ii) total rainfall from April to October accounts the difference between the November and for 80% of variation in crop yield], and (iii) the October rainfall for the current year, and the amount of rainfall in September and (iii) the autumn rainfall in the current year. October to 'finish-off' crops. The model can The model accounts for 41 % of the variation be used to predict plague probabilities for in plague occurrence. A plausible each locality and a high probability is taken mechanism by which each of these factors as an indicator that additional evidence, could affect mouse populations has been such as more detailed crop and rainfall suggested. The requirement in the Turretfield records, should be examined. model (see below) for mid-summer rains was The model's predictions were compared not supported even when the data set was with the results of an intensive trapping restricted to sites with predominantly red­ program from 1980 to 1990 (Mutze 1991). brown earths. However, there was a Plagues were predicted for 1980,1984 and significant contribution from autumn rain in 1985 but not in other years. The only plagues the year immediately preceding a plague that occurred in South Australia during this which matches, to some extent, the revised period were in 1980 and 1984; the failure of model for the Victorian Mallee (below). In mice to respond to generally favourable contrast to the MIA model (below), autumn conditions in 1984-85 was due probably to a rains from earlier years appeared to have no late break in a period of low rainfall during effect. the winter of 1985. If projected estimates of crop yield are available, the South Australia regional model District and small-scale models can be used towards the end of winter to Turretfield model predict the likelihood of a mouse plague in Newsome (1969a,b, 1970, 1971) conducted the following autumn. This may provide the first extensive Australian study of the adequate time for preventative control dynamics of wild mouse populations at measures to be implemented if, for example, Turretfield in South Australia (Figure 1). farmers have access to registered in-crop Mice were permanent residents of small rodenticides. The data requirements are the patches of favourable habitat in the autumn (March, April and May) rainfall, the landscape; reedbeds in the case of this study average November-October rainfall, the area. Mice colonised crops in early summer harvest yield from two years before and the but could not over-winter there due to preliminary estimate for the current year. waterlogging of the clayey soils. According These data provide the three variables for to the modeL a plague of mice occurs as a the model. The preliminary harvest direct result of an unusual sequence of estimates are subjective judgements made events: (i) good winter rains to provide an by district agronomists based on (i) autumn adequate food supply through to the rainfall which determines sowing time, (ii)

85 Ecologically-based Rodent Management

following autumn and to keep the sub-soil burrow in sandy soils, plagues do not moist over summer; (ii) a hot summer to appear to develop immediately in areas with crack the soil allowing mice access to nesting these soil types whenever good winter rains sites in the moist sub-soil; and (iii) mid­ are followed by mid-summer rains. summer rain to allow mice to burrow and The apparent ability of mice at breed throughout summer. The data suggest Turretfield to reach plague densities within it is possible for mice to increase to plague five months implies little prospect for long­ numbers in three to five months. This term forecasting of outbreaks. However, the conclusion was supported by an experiment model demonstrated the role of reedbeds as in which free-fed mice reached densities the source of mice that colonise crops, and well in excess of those observed in plagues. for these land systems, the strategy of The model was later modified by selectively targeting minor refuge habitats Newsome and Corbett (1975) to take into may be effective if control was conducted account the effects of predation. In the routinely. revised version, predators can delay by one Murrumbidgee Irrigation Area (MIA) year the build-up of mouse populations model generated by a pulse of favourable conditions. This is consistent with the A 'triphasic' model of mouse plagues was predation-regulation model (below) proposed developed by Redhead (1982) during an by Sinclair et al. (1990). However the intensive four-year study in the MIA in New suggestion by Newsome and Corbett that South Wales (Figure 1). The model is predators may be responsible for the failure complex and includes both intrinsic (e.g. of mouse plagues to persist under spacing behaviour) and extrinsic (e.g. food favourable conditions is contrary to the quality) factors that influence mouse predation-regulation model. population dynamics (Redhead et al. 1985; Two features distinguish this model from Redhead and Singleton 1988a). According to some of the later models. Firstly, the this model, the plague trigger (phase 1) is relationship between the availability of above average autumn rains two years prior breeding sites for mice and soil moisture to the outbreak, which extends the breeding over summer restricts the applicability of the season into winter in refuge habitats by results to areas of red-brown earths providing high quality food. The effect of interspersed with patches of heavy cracking food quality was experimentally soils. Mutze et al. (1990) argued that the demonstrated by Bomford (1987a,b,c) and TurretJield model was relevant to only these Bomford and Redhead (1987). There is high fairly restricted parts of the South Australian productivity of mice in the following wheatlands. Secondly, there is an apparent summer (phase 2) and mice disperse from anomaly in the lead-time (the time from the the refuges into other areas made favourable first events triggering a plague to the plague by the earlier autumn rains. At the start of itself): less than six months for the area the breeding season immediately prior to the characterised by Turretfield and up to two outbreak (phase 3), there is an abnormally years elsewhere. Despite the ease for mice to high abundance of females in a wide range

86 Models for Predicting Plagues in Australia

of habitat types ('induced-donor' habitats). densities in one season. The difference may Provided no unusual factors intervene to lie in the need for mice to colonise 'induced­ impede breeding, a plague will develop over donor' habitats in phase 2, which depends summer. ultimately on the mix of crops and year­ Redhead (1982, 1987) used a numerical round refuge habitats in the landscape. In simulation model (SIMAD) to show that both the preckltion-regulation model and the between-year differences in the mean litter MIA model, mice are held in a low-density size and the observed size of the initial state by spatial, density-dependent population could explain the variation in the processes. However in the predation­ increase period for each of the three phases. regulation model, phases 1 and 2 were simply However the data set for litter sizes is classed as the predator-regulated state and limited and the model does not allow for not necessarily as essential precursors to changes in litter size during a breeding phase 3, the outbreak state. season. The results of the model emphasise In 1983-84, Boonstra and Redhead (1994) the importance of between-year variability tested the hypotheses relating to phases 1 and in breeding performance in the MIA 2 in the triphasic model. Specifically, these compared to the Darling Downs model were that a tight social structure during the (below) where the population is assumed to extended breeding season in phase 1 should increase at the same rate each year. result in high dispersal rates for mice, In the MIA model, the plague trigger presumably into the 'induced-donor' habitats occurs in the autumn two years prior to a outside refuge areas, and that there should be plague. In comparing this to the NSW and a disproportionate abundance of female mice Victoria regional model, Redhead (1982) at the end of phase 2. The weather conditions observed that there appeared to be a prior to this study included a severe drought relationship between the residual mass [the in 1982 and above-average rainfall in the accumulated difference between the long­ autumn of 1983, both of which have been term average and the actual monthly rainfall considered important precursors to a plague (Poley 1957) 1increasing through winter and (Saunders and Giles 1977; Redhead 1982). The spring and a plague two years later. Neither data on fecundity rates, dispersal rates, sex this relationship nor the prior-drought ratios and testosterone levels showed that (i) hypothesis of Saunders and Giles (1977) was it was unlikely that social organisation had tested statistically, but if the relationship modified dispersal, (ii) the expected changes suggested by Redhead is true, then the in breeding performance in phase 2 did not importance of a prior drought is occur, and (Hi) there was no bias towards questionable. The residual mass will females in the sex ratio at the end of phase 2. increase with above average rains breaking a The conclusions were that, for irrigated rice drought (invariably in winter) or if there are crops, plagues could develop much faster simply above average winter-spring rains. than previously envisaged by Redhead (1982) The extended build-up period (phases 1 and the <12-month time frame for the and 2) prior to the plague year is in contrast increase in mouse abundance in 1984 was to other models where mice can reach plague similar to that suggested in other models.

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However, the reasons for the lack of a Victorian Mallee model subsequent plague are not clear and several A long-term demographic study of mice hypotheses were proposed by Boonstra and beginning in 1983 in northwest Victoria Redhead (1994). The most likely explanations (Figure 1) has restructured the MIA model for appear to be associated with the drought that the Mallee wheatlands (Singleton 1989). In affected the surrounding dryland farms in the Victorian MalIee, the development of a 1984. Non-irrigated areas may have acted as a mouse plague may occur in the breeding sink for dispersing mice. Alternatively, season immediately following high autumn mouse populations may have been regulated or winter rainfall, potentially more rapidly by predation, Le. by highly mobile raptors after a 'trigger' than in the MIA, but because moving away from dryer areas to concentrate of the different soil characteristics (Singleton around irrigated crops, as in the predation­ 1989; Singleton and Redhead 1989) plague regulation model proposed by Sinclair et al. development may be more sensitive to the (1990). During an earlier mouse plague in this sequence of rainfall events. For example, a area in 1979-80, Davey and Fullagar (1986) plague in 1988 was less severe than expected noted a large increase in the abundance of despite an increase in mouse numbers three species of mouse-eating raptors, the following initial favourable conditions. As in Australian kestrel (Faleo cenchroides), the the Turretfield and MIA models, landscape brown falcon (Fa lea berigora) and the black­ heterogeneity and the role of refuge habitats shouldered kite (Elanus notatus). appears to be important in the population The relationship between the dynamics of mice in the Victorian MalIee. development of mouse plagues and the For example, Singleton (1989) reported timing of management actions has been significant temporal differences between examined in detail by Redhead and habitats in the increase phase of the 1984 Singleton (1988b) and Singleton and plague. Redhead (1989) and lead to their PICA The time taken for mice to reach plague (Predict, Inform, Control, Assess) strategy. proportions in the Victorian Mallee in 1984 Their analysis demonstrated that the current was similar to that observed by Newsome lack of registered in-crop rodenticides has (1969a) at Turretfield. Although the 1984 forced a series of time delays into the ability plague occurred 15 months after a drought, in of farmers to respond to plague warnings. accordance with the NSW and Victoria regional The delays result from the processes model, no data were collected to validate the necessary to obtain permission to use suggestion of Saunders and Giles (1977) that rodenticides. However, if suitable control predator regulation was the process techniques can be developed and be ready responsible for this time However, the on demand, predictions with a time frame of prevalence of macroparasites was less than 12 months may be sufficient for independent of mouse densities over a 2.5 farmers to control mice effectively. year study prior to, and during, the plague (Singleton 1987). The data suggest that the macroparasites recorded by Singleton were unlikely to regulate mouse numbers.

88 Models for Predicting Plagues in Australia

Based on the Victorian Mallee model, a The application of the PICA management series of trapping surveys following high strategy (Singleton and Redhead 1989) is autumn or winter rainfall could be used to similar in the Mallee and the MIA, except verify a prediction of conditions conducive that plague development may be more rapid for a mouse plague. A suitable protocol in the former. The timing of control would be as follows. operations may be more constrained in the Mallee than the MIA and this may be a Ill- (i) Trap in the second week in September to problem with future applications of a determine Ca) the start of breeding, (b) litter biocontrol agent such as Capillaria hepatica size [litters are larger in the build up to (see below). plagues (Singleton and Redhead 1990a)], and (c) the size of the breeding popula tion. Darling Downs model The data should be collected from The model is based on demographic data i 'donor I refuge' (e.g. fenceIines) and crop collected over 12 years from a standard set of habitats. If the data from September show trapping sites in the central Darling Downs no breeding and low populations, then in Queensland (Figure 1) (Cantrill 1992). there is a low probability of a plague and no Pooled data from all major habitat types further monitoring is required until the (crops, verges, fallow etc.) show a regular following September. Conversely, an early annual cycle in mouse abundance with no start to breeding, large litters and a large clear separation into plague and non-plague breeding population are conditions years. There are minimal between-year favouring a plague and further monitoring differences in (1) the rate of increase of the is required (step ii). mouse population over summer and Ill- (ii) Trap in November to determine the autumn, (1i) the onset of the main breeding percentage of females breeding and the season, and (iii) the months of maximum litter size. High numbers at this time population denSity. The most important indicate a high chance of a plague next factor that can interrupt the cycle of autumn; moderate numbers may be a abundance and affect the peak density of precursor to a plague 18 months away. mice in May and June is the duration of the low abundance phase (defined as less than Ill- (iii) If data from November confirm that a 1% trapping success) the previous spring. In plague is expected in the next six months, a one year, a sequence of flooding rains, third trapping session may be required to probably increasing nestling mortality, detect the rapid build-up in mouse delayed the annual build-up in mouse numbers over the January - February numbers. A second source of between-year March period. variation is a density-dependent decline in Ill- (iv) Moderate numbers in November (and the over-wintering population. no plague within six months) indicate that Trapping data are required from fixed trapping the following September is trapping sites for two, preferably three, important. periods of the year to generate predictions with the Darling Downs model. These are (i) in

89 Ecologically-based Rodent Management

Mayor June-to test the prediction from the sorghum, cotton and maize, in the previous year and to predict the size of the Macquarie valley of New South Wales mouse population at the onset of the main (Figure 1). Soil types in the irrigation area are breeding season in spring, (ii) in self-mulching clays to deep red clays that September-to determine the size of the crack on drying to produce refuge sites for initial spring breeding population, and (Hi) mice similar to those in patches of black in the period from October to December-to cracking soils at the Turretfield site studied determine the starting time for the increase by Newsome (l969a). phase in mouse abundance. Rainfall data Data were collected over three years that from spring and early summer can be used if included two floods. The best models data from the third trapping period are not explained 68% of the variance in the index of available. The model is based on an mouse abundance and 53% of the variance in established trapping protocol and its the abundance with seasonal trends applicability to data collected elsewhere, or removed. Significant coefficients were found for a different mix of land uses, is unknown. for the mean daily range in temperature for The model can provide forecasts 12, 8 and each month, the mean minimum 5 months in advance of the peak mouse temperature, the mean maximum abundance in May. This translates into temperature and the total monthly rainfall in warning of high mouse numbers 9,5 and 2 the one or two months prior to trapping. months in advance of the time when damage Twigg and Kay (1994) also estimated the size due to mice is usually reported. The model of the seed bank, soil moisture and soil also suggests that any farming practices, hardness, the number of crack." in the soil such as minimum tillage, that enhance over­ and their size distribution, and indices of the winter survival of mice may lead to a structure and biomass of the vegetation. relatively large population at the onset of They found that the component of the seed breeding the following spring. This would bank from barnyard grass (Echinochloa crus­ generate a forecast for high mouse numbers galli), rye grass (Lolium rigidum) and wild the following year with the result that oats (Avena jatua) explained 70% of the farmers could be locked into annual mouse variance in mouse abundance with small control. additional improvements contributed by indices of soil cracking and vegetation. Macquarie Valley model However, the regression based on total seed In contrast to the 12-24 month warning-time bank was less satisfactory. The vegetation recommended by Redhead and Singleton data provided a link between climatic (1988a), Twigg and Kay (1994) suggested variables and mouse abundance but a direct that decisions by fanners for managing pests effect of rainfall and temperature on would be based on relatively short-term recruitment was not supported by the predictions of the order of three months. models. In the model for recruitment, the They developed a series of models, based on proportion of adult females lactating or linear multiple regression analysis, for pregnant depended on the seed bank and irrigated summer crops such as soybeans, the distance to the closest summer crop.

90 Models for Predicting Plagues in Australia

The model for the abundance of mice in although the data are extremely limited. In irrigated summer crops provides a useful, the one year when a plague occurred on the short-term predictive tool based on readily farm, mice were abundant over a wide accessible climatic data. Twigg and Kay region due to exceptionally favourable (1994) suggested that it is desirable to use conditions over the preceding months, and routine surveys of mouse abundance to the limited number of predators on the support their model's predictions, however study area failed to regulate mice. Sinclair et a survey protocol suitable for use by farmers al. (1990) suggested that the plague on the was not specified. The data from this study study farm was caused by a combination of support the conclusions from elsewhere in wide dispersal of predators and enhanced Australia that the management of mice, or breeding performance of mice which their food supply, in refuge habitats such as together allowed mice to escape predator­ roadside verges and fencelines should help regulation. to reduce the damage caused by mice. The analysis of Sinclair et al. (1990) can be generalised to the following multi-state Simplified process models model, which is analogous to a model for rabbit plagues in semi-arid Australia (Pech et Predation-regulation model aL 1992,PechetaL 1995,Pechand Hood 1998) The model proposed by Sinclair et al. (1990) and is relevant to regions where predation focuses on the third of the major extrinsic can be a major mortality factor for mice. mechanisms-food supply, shelter, predation and disease - which may be ... (i) There is a plague trigger (a period of responsible for regulating mouse high rainfall) which provides a finite populations. It is based on data collected amount of food that ultimately is over two years on a summer-irrigated cereal exhausted by mice. The time to depletion of farm in the MIA (Figure 1). Although mice the pulse of food is a function of the size of increased in abundance each year over the the trigger, i.e. the duration of the spring-summer period, years were divided favourable conditions. A large pulse could into plague or non-plague categories. In extend over two years, a moderate pulse non-plague years, raptors-primarily might last only one year, and a smaller one black-shouldered kites, Australian kestrels, still should not result in an outbreak, brown falcons and brown goshawks merely a small seasonal increase in the (Accipter fasciatus) and possibly abundance of mice. It should be possible to mammalian predators (foxes - Vulpes vulpes predict the occurrence of the pulses of food and feral cats - Felis catus) could have been as accurately as the long-range weather responsible for regulating mice at low forecasts. densities despite the apparently favourable ... (ii) The triggerresults in high reproduction environmental conditions for mice on the by mice that can result in an escape from farm. Also a second density-dependent predator-regulation. If there are many factor, the effects of a pathogen thought to be predators in an area and no trigger or only Actinobacillus moniliformis was implicated a small trigger, then only a minor increase

91 Ecologically-based Rodent Management

in mice should occur. If there are few toward a search for organisms which could predators, then an outbreak occurs be introduced into mouse populations either immediately following a trigger. The as conventional biological control agents model predicts that if a trigger is not (Singleton and Spratt 1990) or as vectors followed by an outbreak, then predators engineered to induce infertility in infected should have been present in large mice (Singleton and Redhead 1990b; Shellam numbers. 1994). Although the conditions for a candidate biocontrol agent are exacting ~ (iii) The trigger generates a finite amount of (Spratt 1990), pathogens have considerable food in excess of that normally present. If, appeal because of their likely host­ and only if, mice escape predator­ specificity, the absence of toxic residues, regulation can they reach a high density potential economic advantages and their state determined by the new food supply. possible compatibility with current The abundant food eventually disappears, management practices and land use. In or a drought arrives, which resets food to a addition, Australia has the advantage that low level and the system collapses back to a local populations of M. domesticus lack some situation where predators can take over of the mouse-specific parasites found again. overseas (Singleton and Redhead 1990a). The predation-regulation model is based on Following a major review, Barker and a very limited data set and is best viewed as Singleton (1987) concluded that the liver an hypothesis for more extensive testing. nematode Capillaria hepatica showed promise Although the model has little to offer for as a biological control agent for mice. predicting the likelihood of a plague, it does Laboratory studies had established the identify a key process that can be affected by conditions for successful transmission management. No action should be taken between mice (Spratt and Singleton 1986, which would deplete raptor populations, 1987) and had shown that infection and mouse control techniques should be depressed the productivity of female mice to used to ensure that winter populations of a level that may be sufficient to prevent mice stay low, i.e. within the range where plagues (Singleton and Spratt 1986). As well, regulation by predators is possible. surveys demonstrated that mice in plague­ Pathogen-regulation model prone areas had no prior exposure to the Information on the prevalence and parasite despite it being recorded at a range distribution of pathogens in wild mouse of sites in coastal south-eastern Australia populations in south-eastern Australia is (Singleton et al. 1991). McCallum and summarised in Redhead (1982), Singleton Singleton (1989) and Singleton and (1987), Singleton et al. (1991), Singleton et al. McCallum (1990) modelled the likely impact (1993) and Smith et al. (1993). There is some of C. hepatica on mouse population dynamics field-based evidence that endemic and concluded that it had the potential to pathogens may be responsible for regulating significantly reduce the density of mice mouse populations (Sinclair et al. 1990), below infection-free levels. However, it was however most effort has been directed not clear whether time delays in the host-

92 Models for Predicting Plagues in Australia

pathogen cycle might negate its use for periods of low densities of mice, poor tactical release (time- and area-limited and survival rates for mice, little fidelity in the with 'rapid' effect) (McCallum 1993). The use of burrows and loss of access by mice to effectiveness of C hepatica as a biocontrol eggs deposited in the cracking clay soils. agent was tested in pen experiments (Barker Four treated and three untreated et al. 1991) and two large-scale, replicated cereal! sheep farms were used for the field experiments-the first in the Darling experiment in the Victorian Mallee Downs in 1992-93 and the second in the (Singleton and Chambers 1996). The parasite Victorian Mallee in 1993-94 (Figure 1). The was released in September 1993, two months field sites were chosen to be representative prior to a period of sustained increase in the of the farming systems in each region. abundance of mice. About 60,000 mice, or Three releases were conducted in the 10% of the populations on the treated sites, Darling Downs: (i) low density, non­ were dosed with embryonated and breeding mouse populations in winter, (H) unembryonated eggs. The results from the low density, breeding mouse populations in increase phase in mouse density (November summer, and (Hi) high density, non­ 1993 to mid-1994) showed that C hepatica breeding mouse populations in winter persisted for approximately eight months (Singleton et al. 1995). Embryonated and but with little or no effect on the 28-day unembryonated eggs were released on four survival rate and the fecundity or the sites using a combination of baits and direct abundance of mice, but the treatment infection of mice (oral). The treated sites appeared to temporarily delay the increase were interspersed with three control sites. in mouse density during the early part of the The parasite appeared to persist for <5 breeding season. The causes for the poor months after the first release in winter of performance of C hepatica as a biocontrol 1992, for at least 2-4 months with low agent are uncertain but probably include prevalence after the release in the summer of low survival of eggs during hot, dry weather 1993, and persistence was uncertain after the and delays in the life cycle of the parasite winter release in 1993 because the that prevent it from regulating rapidly abundance of mice declined to levels where increasing mouse populations. it was not possible to trap adequate samples. A pathogen-regulation model based on Following all three releases, little or no C. hepatica is still in the early stages of significant difference between treated and development despite intensive efforts to untreated sites was detected in the age collect epidemiological data in laboratory, structure of mouse populations or their pen and field experiments. To be abundance, breeding performance or implemented, the timing and conditions for survivaL An intensive trapping protocol release of the parasite will need to be failed to detect any transfer of the parasite specified, along with the information beyond the experimentally infected areas. required to determine those conditions. This The minimal impact of C hepatica was will determine the extent to which other attributed to inadequate dosage rates and control techniques might be needed to form adverse climatic conditions leading to an integrated control strategy for mice. In

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addition, the model should specify when reason the recent trend to conservation and what information is required to monitor farming, with emphasis on stubble retention the performance of the technique. and minimum tillage, may exacerbate Although the early promise ofbiocontrol problems with mice (Brown et a1. 1998; using C. hepatica has not been realised, a Singleton and Brown 1998). recent feasibility study suggests that virally­ Predation and disease, two factors that vectored immunocontraception may are likely to be density-dependent, have provide a viable alternative (Chambers et a1. been measured directly or their influence 1997). The fertility of laboratory mice has inferred as a possible explanation of mouse been impaired successfully using ectromelia population dynamics. However the virus as a model (Jackson et a1. 1998) for the predation-regulation model (Sinclair et a1. 1990) development of a genetically engineered is the only example where data on predation irnmunocontraceptive strain of mouse have been analysed within the framework of cytomegalovirus (Shellam 1994). predator-prey theory. Supporting evidence from Davey and Fullagar (1986), Kay et a1. Comparison of current models (1994) and Twigg and Kay (1994) reinforce There is a wealth of data, expert knowledge the need for field experiments to determine and experience, published and unpublished, the circumstances under which predation relating to the formation of mouse plagues in can regulate mouse populations. For Australia. The resulting models, example, Sinclair et a1. (1990) hypothesised summarised in Box 1, contain elements of that predator-regulation may be effective the key extrinsic factors likely to affect mice: only when predation pressure is food availability, access to shelter and nest concentrated on localised patches of the sites, predation, disease and landscape landscape. heterogeneity. In most cases food Although Smith et a1. (1993) and availability is estimated from climatic data Singleton et at. (1993) identified many although the South Australian regional model endemic diseases of mice in south-eastern can include agronomic estimates of crop Australia there is little evidence that any of yields if they are available. No model these play a significant role in regulating includes a protocol for collecting direct mouse populations, with the possible estimates of the amount of food accessible to exception of a mouse parvovirus. The effects mice. The models for areas with heavy soils, of a disease, attributed to Actinobacillus by Turretfield, Darling Downs and Macquarie SincIair et a1. (1990), was similarly equivocaL Valley, include the effect of rainfall, or lack of The pathogenic agent was probably Strepto­ rain at critical times, on the abundance of bacillus moniliformis which has been recorded nesting and shelter sites in sub-surface at low prevalence in fluctuating mouse cracks. In these and in other areas with populations in the Darling Downs (TayIor et lighter soils, secure access to refuge sites can a1. 1994). With current technology there depend on the frequency of disturbance appears to be little scope for large-scale caused by the prevailing system of crop manipulative experiments to test for any rotations and periods of fallow. For this regulatory effects of an endemic disease. The

94 Models for Predicting Plagues in Australia

alternative strategy of using translocated social system of low-density mouse pathogenic agents, or engineered sterilising populations in the field are unlikely to be agents, offers the prospect of well-designed realised. In the two hypotheses proposed by experimental trials. Krebs et a1. (1995a), social organisation acts The influence of landscape heterogeneity as a filter on the response of mice to extrinsic is inherent in all the published models and factors. All the suggested social differences this factor is thought to interact with most, if appear plausible (docile versus "a,err,'"";;",,, not all, potential regulatory processes. behaviour, weak versus strong territorial Different habitat types provide temporal behaviour, and open versus closed social asynchrony in food supply, refugia during systems) but the causal factors in population drought or when there is disturbance from dynamiCS may be still extrinsic. It is farming activities, and may result in either probably more important to begin by testing concentrated or dispersed prey populations rigorously the most parsimonious for raptors and terrestrial predators. At this hypotheses: Boonstra and Redhead (1994) stage there is very limited information on were unable to find evidence to support dispersal and other movements between aspects of intrinsic regulation in the MIA habitats by mice (see for example, Newsome model (Redhead 1982), and some of the et a1. 1982; Boonstra and Redhead 1994; extrinsic mechanisms underlying the current Krebs et a1. 1995b) on which to base models appear amenable to direct spatially-explicit models for mouse plagues. experimental manipulation. Krebs et a1. (1995a) reviewed the case for the intrinsic regulation of mouse Practical application of populations. They urged an analogy with current models models for the cyclic changes in populations At present three models (the South Australia of some rodent species in the Northern regional model and the models for the Darling Hemisphere and proposed two variants of Downs and Macquarie Valley) and possibly a the Chitty hypothesis, with low, increasing, fourth (the NSW and Victoria regional model) high and declining populations of mice could be used unambiguously by people characterised by differences in the ratio of other than those who produced them. Most aggressive and docile phenotypes. There are models imply that reliable forecasts can be at least two problems with this view, one provided only for the medium (less than 12 practical and the other philosophical. Figure months) or short term (less than 6 months). 2b illustrates the difficulty of obtaining This imposes some constraints on the timing sample sizes sufficient to extract the simplest of effective control options, especially those demographic parameters - abundance and relying on biocontrol agents. All models rate of increase - during periods of low have been developed using location-specific mouse numbers. Even if the two data and, to date, none have directly phenotypes, or their effects, can be addressed the extent of the geographic range distinguished in the laboratory experiments of their predictions. Some models - for suggested by Krebs et a1. (1995a), the example, the two regional models - should resources required to measure aspects of the apply across state boundaries to districts

95 Ecologically-based Rodent Management

with similar soils, climate and agricultural MODIFIED MODEL FOR MOUSE practices. Other models are limited by PLAGUES IN THE VICTORIAN MALLEE attributes such as soil type or cropping regime. With the exception of the Darling Background and data Downs model, none of the existing models The aim of the following analysis is to relate the density of mice, or the effect of construct a quantitative model, based on the controls, to the extent of damage caused by conceptual model of Singleton (1989), to mice. This is an essential requirement for explain the observed rates of increase of future models of mouse plagues. mice over the last two decades in the A prerequisite for the application of a Victorian Mallee. The ultimate purpose is to model is that the data and the methods used use quantitative models to predict when to generate a prediction are clearly specified. mouse plagues will occur and to assess the For most models the protocols for data effectiveness of a range of control collection have not been specified in techniques, including fertility controt for sufficient detaiL In future such protocols will managing mice in the Mallee region. need to be designed and tested for areas Mice were live-trapped at intervals of other than the localities where the models approximately six weeks from 1983 to 1997 were developed. in several habitats either on the Mallee One approach to improving the value of Research Station or on nearby farms in existing models is to include their predictive northwest Victoria (35.08°5, 142.02°E). The capability with other expert knowledge in region has a Mediterranean-type climate 'decision-support systems' (Norton 1988). (Figure 2a) and is used for cropping and An example is the computer-based expert livestock production. Details of the trapping system that can provide short-, medium­ protocol are given in Singleton (1989). and long-term predictions based on the Although most trapping sessions were Darling Downs model (Cantrill1992). A conducted over three nights and all mice decision support system, MOUSER, is under were tagged, the number of recaptures was development for the Victorian Mallee generally <15%. As well, the trapping grids (Brown et al. 1998). This software provides were moved periodically to cater for the advice on how to achieve effective mouse rotation of crops and pasture so that control by modifying farming activities. The capture-mark-recapture techniques did not aim is to include interactive models for provide the best estimates of abundance. plarming mouse-control campaigns in future Instead, the number of captures, adjusted to editions of MOUSER. However, all the take into account trap saturation, was used existing regional and district models focus as an index of abundance. This required on predicting the occurrence of plagues or transforming the proportion, P, of traps the abundance of mice rather than their rates catching mice per night (the frequency of of increase. This means that none of the captures) to the number of animals that models are capable of assessing the impacts would have been caught per trap if the traps of control programs in an interactive way. were capable of multiple captures (an index of the density of mice). Then the adjusted

96 Models for Predicting Plagues in Australia

120 (a)

>,E 80 :cS..... c:= OCll :if: 1: 40 'Cij.... o 1.0 15-0 c: OJ 0= 'tt;:::o (/) 05, Cl. Cl. e~ 0...... 0.0

1.0

Cl. e(.) >< Cil -ll 0,5 OJ c: ..c'- S 0.0

(d) 3000

2000

1000 o 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 Year Rgure2. (a) Monthly rainfall (mm) at the Mallee Research Station (MRS), Victoria. (b) Smoothed abundance of mice (-), indexed by the proportion of traps filled at the MRS and nearby farms. Data for 1983-85 are from Singleton (1989), for 1993-94 from Singleton and Chambers (1996) and for 1993-97 from Singleton and Brown (1998). The data are shown for each night of trapping with the size of the symbols Co) scaled according to the trapping effort (minimum = 10, maximum = 355, median = 242 trap-nights). (c) Modelled food from wheat crops (equation 1). with the mid-summer amplitude proportional to the total rainfall for the winter/spring period. (d) The estimated total seed biomass (kg/ha) from annual grasses and medic using the model GrassGro (Moore et al. 1997). Parameter settings for the GrassGro model are shown in Table 1.

97 Ecologically-based Rodent Management

density, N, is -In(l- p) (Caughley 1977). We During 1984 and 1985, the diet of mice would expect this density to be affected was measured at a cereal farm not far proportionally by various factors and (approximately 25 km) from the Mallee therefore the regression model would be Research Station (Tann et a1. 1991). The additive on In(N) = In[-ln(l- p)]. findings of this study showed that the main The data for the proportion, p, are dietary components were monocotyledon somewhat noisy (Figure 2b) and small seed (primarily wheat-Triticum aestivum fluctuations, particularly during periods of and some grasses such as brome - Bromus very low-density, are unlikely to be spp., barley - Hordeum leporinum, wild important in the overall population oats - Avena fatua and ryegrass - Lolium dynamics. Therefore the data were rigidum) and dicotyledon seed such as smoothed in a generalised linear modelling medic - Medicago spp. and Chenopodaceae framework by fitting a spline in time as an species. The proportion of the major explanatory variable, with the component, monocotyledon seed, showed complementary log-log link function. The strong seasonal variation, rising from a model was fitted in S-PLUS (1997) using a minimum around July in mid-winter to a smoothing spline with 20,30, 50 and 70 peak at harvest six months later. Post­ degrees of freedom (d.f.). The residual harvest, the consumption of monocotyledon deviances (and the residual dJ.) obtained seed declined to a low point in the following were 9067 (515), 5921 (505),4123 (485), and winter. Bomford (1987a) found similar 3276 (465), respectively. There was a changes in the diet of mice occupying a substantial reduction in the residual wheatfield on an irrigated cereal farm in deviance for a model with 30 d.f. compared central New South Wales. In the Mallee, the to 20 d.f. which was reflected in the better exception to this pattern was a brief increase tracking of the mouse plague peaks in the in wheat consumption at the time of sowing data. Fitting splines with more than 30 dJ. in the early winter of 1985, presumably did not lead to a marked improvement in because mice were unearthing the sown the fit to the main peaks and started to grain. No direct measurements of the generate spurious peaks in the periods availability of food items for mice were between major plagues. The inclusion of reported by Tann et a1. (1991) and other data seasonal (sine and cosine) terms did not for the period from 1983 to 1997 are very improve the model which is not surprising limited. Consequently existing models were since mouse plagues do not occur on a used to estimate the relative availability of regular annual cycle. The slope of the monocotyledon and dicotyledon seed. trajectory for In(N) is the instantaneous rate French and Schultz (1984) used data for 61 of increase of the mouse population. Using sites in South Australia from 1964-1975 to S-PLUS, the estimated first derivatives were establish a linear relationship between wheat obtained from the fitted model at 40.55 day yield and the rainfall summed over the period intervals (1/9th of a year). This from April to October, RkO" They found that approximates the mean interval between 65% of the variation in wheat yield was trapping sessions for mice. explained by the rainfall data. Cornish et a1.

98 Models for Predicting Plagues in Australia

(1980), using a similar model, accounted for where the rainfall has been expressed as a 80% of the variation in wheat yield and Seif proportion of the maximum observed value and Pedersen (1978) used spring rainfall to of 348 mm for the winter / spring period. The account for 86% of the variation in yield in values of this index for the years 1983 to 1998 central New South Wales. The data set used are shown in Figure 2c. A transformed by French and Schultz (1984) included areas version of W that helps to distinguish with climate and soils similar to the Victorian between average and bumper crops was used Mallee region and the validity of later for modelling the rate of increase of the extrapolating from their results was tested by mouse population. comparing April to October rainfall with crop vields from the Mallee Research Station for 3 Yield = 0.0087 Rain 0.1648 " Ft = 0.69 the period 1984-1997. The regression • • accounts for 69% of the variance in the

However, some measurements of spilled Rain (mm from April to October) grain have been made immediately post­ Figure 3. harvest and at irregular intervals for up to Comparison of the summer wheat yields four months (G.R. Singleton, unpublished (tonnes/ha) at the Mallee Research Station with data). These data show a steady decline in the total rainfall (mm) over the preceding period from quantity of spilled grain post-harvest with April to October. French and Schultz (1984) little or none remaining on the ground by mid established a linear relationship between April to October rainfall and wheat yield using data from to late autumn. Based on this information, South Australia. and the observed seasonal changes in monocotyledon seed component in the diet of Th.e model, GrassGro (Moore et a1. 1997), mice (Tann et a1. 1991; Bomford 1987a), the was used to estimate the biomass of ripe and within-year variation in the food from wheat unripe seed,S, produced by annual grasses crops was modelled as a sinusoidal function, and medic (Figure 2d). It requires detailed [1 + cos(2:n:(T /9)]/2, where T is the time in information on stocking regimes, soil type ninths of a year (i.e. intervals of 40.55 days) and climate (Table 1). Although areas since the first of January. Then an index of the accessible to mice included grazed pastures amount of food from crops is: and ungrazed grass along fencelines and roadside verges, only the estimates for grazed pasture were used. This is the predominant non-crop habitat in the Victorian Mallee and there are relatively

99 Ecologically-based Rodent Management

minor differences in the modelled total seed Estimates of seed biomass were then biomass for the two types of pasture. The recorded for each lO-year simulation seed biomass data for a grazed pasture, excluding the first two years to reduce the including medic (Paraggio) and barley grass, effect of 'reseeding' the pasture on the seed were estimated for the period from 1st available to mice. Finally, seed biomass, S, January 1980 to 31st May 1998. The 1st for each 40-day time step was determined by January 1980 was used as a starting time to interpolation from the nearest weekly remove any distortion from initial values estimates from the GrassGro model. and runs were made over 10-year intervals to ensure that annual grass seed banks were Modified Victorian Mallee model not exhausted after droughts and to mimic Many of the existing models for predicting pasture sowing after cropping. Each run had mouse plagues invoke a complex set of a two year overlap with the next. fac tors to explain the population dynamics of mice (see, for example, the MIA rnodel). In Table 1. this case, as a first step, we assessed how Data requirements for using the GrassGro much of the variance in the rate of increase model (Moore et a l. 1997) for the Mallee of mice can be explained by the m.ost Research Station (MRS) at Walpeup (35.08°5, 142.02°E) in the northwest of Victoria . obvious factor, food availability. Then we determined whether inclusion of a density­ Attribute Units/description dependent fac tor improved the predictive Rainfall daily rai nfall in mm recorded at ability of the model. This additional factor is MRS a surrogate for several processes that may Temperature daily maximum and minimum modify the rate of increase when the denSity temperature of m ice is high. Examples include disease 1965-95: MRS 1996-97: Ouyen Post Office and changes in mating behaviour, social (35.0rS, 142.32°E)a organisation or dispersal. The approach is Terrain gently sloping similar to the generalised fo rm of the Soil sandy loam, fertility rating of 0.8, predation-regulation model in that the soil moisture budget parameters dynamics of the mouse population are (including thickness of each soil assumed to be driven primarily by annual layer, volumetric water content of each laye r, drainage and pulses of food whose duration and evaporation rates) magnitude is determined by the weather. Pasture barley grass, medic (Parragio) However predator-regulation at low mouse species densities, e.g. through the aggregation of Livestock 2.0 ewes/ ha managed for wool raptors, was assumed to be less important in and meat production the croplands of the Victorian Mallee than in a Temperature data for 1996-97 were extrapolated the localised irrigated areas studied by from records at the Ouyen meteorological station Sinclair et al. (1990). using the 1965-95 records to generate a temperature·difference profile with the MRS . An Ivlev model was used for the relationship between food availability and

100 Models for Predicting Plagues in Australia

the rate of increase, r, for mice. 1his has the variables, food from wheat crops and general form: pasture and the density of mice, were tested singly then in combination. The overall r = -a + exp(-d.F)] (2) q1- goodness of fit of each model was estimated using VENSIM@ (1997) to calculate the sum where F is an index of food biomass which is seed from pasture and / or wheat in the case of of the squared errors between the observed rates of increase (from the smoothed data mice. In equation (2), a is the maximum rate of series) and the predictions of each model for decrease, the maximum rate of increase is the period 1983 to 1989. 1his statistic was rmax = (c - a), and the demographic efficiency, used as a guide in model selection. A second d, is a measure of the ability of the mouse criterion was the ability to predict the rates population to respond to scarce resources. This form for the rate of increase has been of increase and the trajectory of mouse abundance for the later period from 1991 to used to model the response of several species 1994. The optimal values, with 95% to widely fluctuating food supply in confidence limits, were estimated for the climatically-variable parts of Australia; e.g. parameters in equations (2) and (3), although kangaroos-Macropus spp. (Bayliss 1987; Caughley 1987; Cairns and Grigg 1993), feral for some models the maximum rate of increase and the maximum rate of decrease pigs-Sus scrota (Caley 1993; Choquenot and were calculated directly from the smoothed Dexter 1996) and rabbits-Oryctolagus trajectory of mouse abundance and used as cuniculus (Choquenot 1992; Pech and Hood 1998). The model applies when changes in the fixed parameters. The estimates from the wheat model (equation 1, Figure 2c) do not abundance of a population are determined necessarily indicate their relative availability primarily by the availability of food. or value for mice. Comparison of Figures 2b When food is scarce r is negative, i.e. the and 2c suggest that the high wheat yields in population declines, and when food is 1984,1987,1993 and 1996 correspond, with a readily available r is positive but ultimately limited to a maximum value r by the smalllag, to mouse plagues. The outbreaks ! max' appear to be a response to the difference species' reproductive capacity. Density- between normal years, e.g. 1988-92, and the dependence was included as a linear four high-yield years. The sensitivity of the additive factor, in a similar way to that rate of increase to this difference can be suggested by Caughley and Krebs (1983). explored by transforming the amplitude of With the additional factor, the parameters a the wheat yield index to (R /348)U, where and (c a) in equation (2) no longer retain AO the scaling exponent u is estimated by fitting their demographic interpretation so the the models to the data. Then the model of the model was simplified to: food available from wheat crops is: r = a + c.exp( -d.F) + gN (3) where g is a measure of the strength of the density-dependence. Models were developed through an If, for example u» 1, then equation (4) iterative process where the explanatory indicates that mouse population dynamics

101 Ecologically-based Rodent Management

are sensitive to changes in high values of W, Model (iii) was based on the pasture seed whereas u "'" 1 implies no transformation is biomass which showed strong seasonal necessary (Figure 4). variation and, apart from 1984 and 1993, was The results of fitting the models are mostly in the range 0-1000 kg/ha. Since this summarised in Table 2 and illustrated in was also the part of the fitted numerical Figures 5 and 6. It is apparent in Figure 2b response with a positive slope (Figure 6c), that in non-plague years there is too much the predicted r showed a corresponding variability in the field data to detect the pattern that was not reflected in the observed expected seasonal variations in the mouse rates of increase of mice (Figure Sc). A trans­ population, e.g. the annual spring decline formation similar to that for wheat was tried in abundance (Singleton 1989). The absence unsuccessfully with the seed biomass model. of these small seasonal variations carries The best fit to the observed rates of through to the observed rates of increase increase was obtained by combining a (Figures Sa-d). However, in all years, density-dependent effect with the wheat­ seasonal effects are quite pronounced in the based food index [model (iv) in Table 2]. This models for food supply (Figures 2c,d) and also resulted in improvements in predicting it was necessary to suppress much of this the trajectory of mouse abundance. within-year variability in fitting the models However, the upper 95% confidence limit for for the numerical response. The result is the density-dependent parameter, g, could that the models including wheat, (i), (ii) not be estimated and there was only a and (iv) in Table 2, have scaling exponents, relatively small improvement in the sum of u, of 6.6,9.4, and 11.3, respectively; i.e. all squared errors compared to model (ii). these models require a transformation of W The results in Figure 5d show that the similar to that shown in Figure 4b. model matched the high rates of increase The corresponding numerical response that generated the mouse plagues in 1984, functions show a rapid change from negative 1987 and 1993, but not the latter part of the to positive r at low values of the wheat index, period of high r leading to the plague in saturating at rmax above this threshold 1997. The major density-dependent (Figures 6a, b and d). Even with these contributions were during plague years transformations, all of the food-only models (Figure 5d) and, compared to the wheat-only were a poor fit to the observed r in non­ model (ii), produced a slightly better fit plague years. Fixing the maximum rate of during periods of rapid decline in mouse decrease in model (i) resulted in a reasonable numbers. All the models that include wheat fit to the post-plague declines in mouse (i, ii and iv) were optimised with high values abundance (Figure Sa) but an overall poorer of the scaling exponent, u. fit compared to model (ii) where only the In each case this was balanced to some maximum rate of increase, r max' was fixed. extent by high values in the demographic Conversely, model (ii) did not match periods efficiency, d, in the product dW. An with large negative rates of increase but independent estimate of at least one of these provided a clearer distinction between two parameters is required to resolve this plague and non-plague years (Figure 5b). difficulty with the Ivlev model.

102 Models for Predicting Plagues in Australia

(a) u = 1

1.0

0.8 ~ ~ 0.6 ro ~ g 0.4 . u.. 0.2 .

0.0

(b) u= 10

1.0

0.8 ~ ~ 0.6 ~'" ::> to 15 0.4 0 u..

Figure 4. The effect of the parameter, u, In equation (4) in modifying the index of food availability from wheat crops. Time, in units of 1/9th of a year, is measured from the 1st of January each year and rainfall is in mm. (a) U = 1, which Is the same food index used for Figure 2c. (b) U = 10, showing the effect of u» 1 in suppressing the food availability for low rainfall, <200-250 mm, and greatly exaggerating the relative availability above this threshold.

103 Ecologically-based Rodent Management

1

0

-1

1

0

ID fIJ

-1

1

0

-1 o i ~ -0.5 ~ ID ID o 0 c:

Figure 5. (a}-(d) The observed (.) and modelled (-) rates of increase per 40 days. (e) The observed (0) and modelled (-) index of abundance of mice. For (a)-(d) the predicted trajectories correspond to the models (i}-(iv) listed in Table 2. The density-dependent contribution to f(- -) is shown in Cd). For (e), the abundance of mice was predicted using model (iv) from Table 2.

104 Models for Predicting Plagues in Australia

(a) Model i 1.0 '- ID 0.5 (/) ~! C1l ~ 0.0 (.l .£: '0 -0.5 n;

(b) Model 11 1.0 '- ID 0.5 (/) {"(I -/ ~ 0.0 (.l .~ '0 -0.5 - n;

Flgure 6. The estimated numerical response functions corresponding to models (I)-(Iv) In Table 2. Food is from (a) wheat crops, with,max and Sw fixed at the observed values, (b) wheat crops, with only,max fixed, (c) pasture seed In kg/ha, with rmax and Sw fixed, and (d) wheat crops with the density of mice set at 0.001 In the denslty-dependent term in model (Iv).

105 Ecologically-based Rodent Management

Table 2. Results from fitting models for the numerical response of mice. The food biomass, F, in equation (2) was replaced by an index ofthe food available from cereal crops, W, (equation 4) for models (i) and (ii), and seed biomass from grazed pasture,S, in kg/ha (model iii). The models' parameters have corresponding subscripts. In model (iv), the rate of increase is determined by equation (4) for W(replacing Fin equation 3) and the index of mouse abundance, N. Parameters were optimised using VENSIM® (1997) to fit the models to the data for the rate of increase per 40 days for the period from 1983 to 1989. SSE is the sum of the squared errors in fitting each model. For the optimised values, 95% confidence limits are given in square brackets unless they could not be estimated [NE]

(i) Food from wheat crops: r = - aw + cJl - exp(- dw- W)]. with the maximum rate of increase (rmax = Cw - awl and maximum rate of decrease (-aw) fixed at the observed values. aw = 1.34 (fixed) Cw = 2.19 (fixed) dw = 48.0 [NE - 77 .0] u = 6.6 [NE - 7.5] SSE = 34.7 (ii) Food from wheat crops: r = -aw + cJl - exp(-dw- W)]. with the maximum rate of increase (rmax = Cw - awl fixed at the observed value. aw = 0.24 [0.026 - 0.45] Cw = rm ax + aw = 0.84 + aw (fixed) dw= 23.7 [4.8 - 61.3] u = 9.4 [7.3 - 13.6] SSE = 10.3

(iii) Pasture seed biomass: r = - as + cs[l - exp(-ds. Sl]. with the maximum rate of increase (rmax = Cw - awl and maximum rate of decrease (- awl fixed at the observed values. r- as = 1.34 (fixed) Cs = 2.19 (fixedl ds = 0.0039 [NE] SSE = 35.5

(iv) Wheat and density: r = aN + cN exp(-dN. W) + gN aN = 0.22 [0.11 - 0.41] cN = 0.74 [0.37 - 0 .94] dN = 102.5 [19.7 - NE] u = 11.3 [8.8 - 16.7] g = -0.30 [-12.6 - NE] SSE = 9.1 In addition, the estimation procedure is Some of the main demographic features quite sensitive to small changes in the are represented reasonably well. However, constants which, together with the wide the results clearly demonstra te that the post­ confidence limits, suggests that we are plague declines are not well modelled nor is searchi.ng a very fla t parameter space in there an obvious explanation for the 12- attempting to fit the models. month difference between the predicted In Figure Se, the observed densities of plague in 1996 and the observed ou tbreak ill mice for the period for 1983 to 1997 are 1997. compared to the predicted trajectories using model (iv) in Table 2.

106 Models for Predicting Plagues in Australia

Future directions for the Victorian influenced by rainfall events in summer and Mallee model the autumn-winter period (Singleton 1989; Boonstra and Redhead 1994). The modified Victorian Mallee model It is likely that the strong seasonal represents some progress towards a variation in food from wheat crops and quantitative model for assessing the pasture will play an important role in future effectiveness of mouse control operations in age-structured models for both fecundity southern Australia. However, any and survival. Field data are required to assessments will be subject to the proviso validate the pasture and wheat crop models, that the model for the numerical response is especially the relationship between seed and still appropriate after a mouse population crop biomass and the amount of food has been reduced by a control technique. available to mice. In addition, manipulative Alternatively, in the case of immuno­ experiments should be used to confirm the contraception, estimates would be required dependence of the numerical response on of the proportional change in r resulting food supply. Although it may be difficult to from an imposed level of infertility manipulate factors like predation and (Chambers et al. 1997, 1999). disease, there may be opportunities to use An obvious shortcoming of the modified future mouse control campaigns to test the model is the lack of detail on seasonal importance of the density-dependence changes in demographic parameters. implied by the optimal model. Improvements in this area are likely in future models which will treat fecundity and survival rates separately. Examples of this ACKNOWLEDGMENT approach include the density-dependent, Part of this work was included in an stochastic model of Leirs et al. (1997) for the unpublished review prepared by R. Pech for multi-mammate rat Mastomys nataiensis in the Grains Research and Development Africa and the model used by Pech et al. Corporation in 1991. (1997) to assess the value of fertility control for the management of foxes in Australia. REFERENCES There is some evidence that the onset of Barker, S.c. and Singleton, G.R. 1987. Conclu­ breeding by mice depends on seasonal sion. In: Singleton, C.R., ed., Capillaria hepatica environmental triggers (e.g. Olsen 1981; (Nematoda) as a potential control agent of Bomford 1987a,b,c; Bomford and Redhead house mice. Proceedings of a CSIRO 1987; Tann et al. 1991) and the results of workshop,June 1987. Division of Wildlife and Rangelands Research, Technical model (iv) in Table 2 suggest that density­ Memorandum No. 28, Commonwealth Scien­ dependent factors are likely to be important tific and Ind ustiral Research Organisation in terminating plagues, presumably through (CSIRO), Melbourne. decreased survival rates of mice. In addition, Barker, S.c., Singleton, C.R. and Spratt, D.M. other factors could be included to fine-tune 1991. Can the nematode Capillaria hepatica regulate abundance in wild house mice? the model. For example, the ultimate Results of enclosure experiments in south­ abundance of mice in a plague can be strongly eastern Australia. Parasitology, 103,439-449.

107 Ecologically-based Rodent Management

Bayliss, P.1987. Kangaroo dynamics. In: Caugh­ Cantrill, S. 1992. The population dynamicS of the Iey, G., Shepherd, N. and Short, J., ed., house mouse (Mus domesticus) in a dual crop roos: their ecology and management in the agricultural ecosystem. PhD thesis, School of sheep rangelands of Australia. Cambridge, Life Science, Queensland University of Cambridge University Press, 119-134. Technology. Bomford, M. 1987a. Food and reproduction of Caughley, G.c. 1977. Analysis of vertebrate wild house mice. 1. Diet a nd breeding seasons populations. Chicester, John Wiley & Sons. in various habitats on irriga ted cerea1 farms in Caughley, G.C.1987. Ecological relationships. In: New South Wales. Australian Wildlife Caughley, G., Shepherd, N. and Short, J., ed., Research, 14, 183-196. Kangaroos: their ecology and management in Bomford, M. 1987b. Food and reproduction of the sheep rangelands of Australia. wild house mice. n. A field experiment to Cambridge, Cambridge University Press, examine the effect of food availability and 159-187. food quality on breeding in spring. Austral­ Caughley, G.c. and Krebs, c.J. 1983. Are big ian Wildlife Research, 14, 197-206. mammals simply little mammals writ large? Bomford, M. 1987c. Food and reproduction of Oecologia,59,7-17. wild house mice. III. Experiments on the Chambers, L.K., Singleton, G.R. and Hinds, L.A. breeding performance of caged house mice 1999. Fertility control of wild mouse popula­ fed rice-based diets. Australian Wildlife tions: the effects of hormonal competence and Research,14,207-218. an imposed level of sterility. Wildlife Bomford, M. and Redhead, T. 1987. A field exper­ Research, 26, 579-591. iment to examine the effects of food quality Chambers, L.K., Singleton, GR and Hood, G.M. and population density on reproduction of 1997. Immunocontraception as a potential wild house mice. Oikos, 48, 304-311. control method of wild rodent populations. Boonstra, R and Redhead, T.D. 1994. Population Belgian Journal of Zoology, 127, 145-156. dynamics of an outbreak population of house Choquenot, D. 1992. The outsiders: competition mice (Mus domesticus) in the irrigated rice­ between introduced herbivores and domestic growing area of Australia. Wildlife Research, stock in rangeland grazing systems. In: 21,543-598. Australian rangelands in a changing environ­ Brown, PR, Singleton, G.R and Dunn, C. 1998. ment. Proceedings of the ;nh Biennial Confer­ Best farm management practices for mouse ence of the Australian Rangeland SOciety, 5-8 control: testing of recommendations. In: The October 1992, Cobar, NSW. Cobar, Australian future of vertebrate pest direc­ Rangeland Society, 106-116. tion for the third millennium. Proceedings of Choquenot, D. and Dexter, N.1996. Spatial varia­ the 11 th Australian Vertebrate Pest Confer­ tion in food limitation: the effects of foraging ence, 3-8 May, Bunbury, Western Australia, constraints on the distribution and 99-104. abundance of feral pigs in the rangelands. In: Cairns, S.c. and Grigg, G.c. 1993. Population FIoyd, RH., Sheppard, A.W. and De Barro, dynamics of red kangaroos Macropus ru/us in P.J., ed., Frontiers of popUlation ecology. relation to rainfall in the South Australian Melbourne, CSIRO Publishing, 531-546. pastoral zone. Journal of Applied Ecology,30, Cornish, E.A., R.J. and Hill, G.W. 1980. 444-458. Yield trends in the wheat belt of South Caley, P. 1993. Population dynamics of feral pigs Australia from 1896 to 1964. Agricultural (Sus scrota) in a tropica 1riverine habitat Record Ko. 7. Adelaide, Government Printer. complex. Wildlife Research, 20, 625-636. Davey, c.c. and Fullagar, P.J. 1986. Changes in the abundance and distribution of raptors during a house mouse plague. Corella, 10,52- 54.

108 Models for Predicting Plagues in Australia

Foley, lC 1957. Droughts in Australia. Review of growth and soil moisture submodels, and the records from the earliest years of settlement GrassGro DSS. Agricultural Systems, 55, 535- to 1955. Melbourne, Commonwealth Bureau 582. of Meteorology, Bulletin No. 43. Mutze, G.J. 1989. Mouse plagues in South French, RJ. and Schultz,J.E.1984. Water use Australian cereal-growing areas. 1. Occur­ efficiency of wheat in a Mediterranean-type rence and distribution of plagues from 1900 to environment. 1. The relation between yield, 1984. Australian Wildlife Research, 16, 677- water use and climate. Australian Journal of 683. Agricultural Research, 35,743-64. Mutze, G.J. 1991. Mouse plagues in South Hone, J. 1980. Probabilities of house mouse (Mus Australian cereal-growing areas. Ill. Changes musculus) plagues and their use in control. in mouse abundance during plague and non­ Australian Wildlife Research, 7,417-420. plague years, and the role of refugia. Wildlife Jackson, RJ., Maguire, DJ, Hinds, L.A and Research,18,593-604. Ramshaw, LA 1998. Infertility in mice Mutze, G.]., Veitch, L.G. and Miller, RB.1990. ind uced by a recombinant ectromelia virus Mouse plagues in South Australian cereal­ expressing mouse zona pellucida glycopro­ growing areas. n. An empirical model for tein 3. Biology of Reproduction, 58,152-159. prediction of plagues. Australian Wildlife Kay, B.J., Twigg, L.E., Korn, T.J. and Nicol, HJ. Research, 17, 313-324. 1994. The use of artificial perches to increase Newsome, AE. 1969a. A population study of predation on house mice (Mus domesticus) by house-mice temporarily inhabiting a South raptors. Wildlife Research, 21, 95-106. Australian wheatfield. Journal of Animal Krebs, CJ., Chitty, D., Singleton, G. and Ecology, 38, 341-359. Boons tra, R 1995a. Can changes in the social Newsome, AE. 1969b. A population study of behaviour help to explain house mouse house-mice permanently inhabiting a reed­ plagues in Australia? Oikos, 73, 429-434. bed in South Australia. Journal of Animal Krebs, CL Kenney, AI. and Singleton, G.R Ecology, 38, 361-377. 1995b. Movements of feral house mice in Newsome, AE. 1970. An experimental attempt agricultural landscapes. AustralianJournal of to produce a mouse plague. Journal of Zoology, 43, 293-302. Animal Ecology, 39, 299-311. Leirs, H.,Stenseth, N.C, Nichols, J.D., Hines, J.E., Newsome, AE.1971. The ecology of house-mice Verhagen, R. and Verheyen, W. 1997. in cereal haystacks. Journal of Animal Stochastic seasonality and non-linear Ecology, 40, 1-15. density-dependent factors regulate popula­ Newsome, AE. and Corbett, L.K 1975. VI. tion size in an African rodent. Nature, 389, Outbreaks of rodents in semi-arid and arid 176-180. Australia: causes, preventions, and evolu­ McCallum, H.!. 1993. Evaluation of a nematode tionary considerations. In: Prakash, 1. and (Capillaria hepatica Bancroft, 1893) as a control Ghosh, P.K, ed., Rodents in desert environ­ agent for populations of house mice (Mus ments, The Hague, W.Junk,117-153. musculus domestiells Schwartz and Schwartz, Newsome, AE., Cowan, P.E. and Ives, P.M. 1982. 1943). Revue Scientifique et Techique OIE Homing by wild house-mice displaced with (Office International des Epizooties), 12,83- or without the opportunity to see. Australian 94. Wildlife Research, 9, 421-6. McCallum, H.!. and Singleton, G.R 1989. Models Norton, G.A 1988. Philosophy, concepts and to assess the potential of Capillaria hcpatica to techniques. In: Nortol1, G.A and Pech, RP., control population outbreaks of house mice. ed., Vertebrate pest management in Australia: Parasitology, 98,425-437. a decision analysis/ systems analysis Moore, A.D., DonneIly, J.R and Freer, M. 1997. approach. CSIRO Division of Wildlife and GRAZPLAN: decision support systems for Ecology, Project Report No. 5, 1-17. Australia grazing enterprises. m. Pasture

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Olsen, P. 1981. The stimulating effect of a phyto­ decision analysis/ systems analysis approach. hormone, gibberellic acid, on reproduction of CSIRO Division of Wildlife and Ecology, Mus musculus. Australian Wildlife Research, Project Report No. 5, Melbourne, 18-37. 8,321-325. Saunders, G.R 1986. Plagues of the house mouse Pech, RP. and Hood, G.M. 1998. Foxes, rabbits, in south eastern Australia. In: Salmon, T.P., alternative prey and rabbit calicivirus ed., Proceedings of the twelfth vertebrate pest disease: consequences of a new biological conference. Davis, University of California, control agent for an outbreaking species in 173-176. Australia. Journal of Applied Ecology, 35, Saunders, G.R and Giles, J.R 1977. A relation­ 434--453. ship between plagues of the house mouse, Pech, R, Hood, G.M., McIlroy, J. and Saunders, Mus musculus (Rodentia: Muridae) and G. 1997. Can foxes be controlled by reducing prolonged periods of dry weather in south­ their fecundity? Reproduction Fertility and eastern Australia. Australian Wildlife Development, 9, 41-50. Research, 4, 241-7. Pech, RP., Sinclair, AE. and Newsome, AE. SeH, E. and Pedersen, D.G. 1978. Effect of rainfall 1995. Predation models for primary and on the grain yield of spring wheat with an secondary prey. Wildlife Research, 22, 55--64. application to the analysis of adaptation. Pech, RP., Sinclair, A.E., Newsome, A.E. and Australian Journal of Agricultural Research, Catling, P.e. 1992. Limits to predator regula­ 29,1107-1115. tion of rabbits in Australia: evidence from Shell am, G.R 1994. The potential of murine predator-removal experiments. Oecologia, cytomegalovirus as a viral vector for 89,102-112. immunocontraception. Reproduction Fertil­ Redhead, T.D. 1982. Reproduction, growth and ity and Development, 6,401-409. population dynamics of house mice in Sinclair, ARE., Olsen, P.D. and Redhead, T.D. irrigated and non-irrigated cereal farms in 1990. Can predators regulate small mammal New South Wales. PhD thesis, Department of poplIlations? Evidence from house mouse Zoology, Australian National University, outbreaks in Australia. Oikos, 59, 382-392. Canberra. Singleton, G.R 1985. Population dynamics of Redhead, T.D. 1987. Computer simulations of Mus musculus and its parasites in mallee mouse plagues: plague formation and wheatlands in Victoria during and after a prevention. In: Working Papers of the 8th drought. Australian Wildlife Research, 12, Australian Vertebrate Pest Control Confer­ 437-445. ence, Coolangatta, Queensland, 186-194. Singleton, G.R. 1987. Parasites of mice in the Redhead, T.D., Enright, N. and Newsome, A.E. Victorian manee wheatlands. In: Singleton, 1985. Causes and predictions of outbreaks of G.R, ed., Capillaria hepatica (Nematoda) as a Mus musculus in irrigated and non-irrigated potential control agent of house mice. CSIRO cereal farms. Acta Zoologica Fennica, 173, Division of Wildlife and Rangelands 123-127. Research, Technical Memorandum No. 28, Redhead, T.D. and Singleton, G.R 1988a. The Melbourne, 12-14. PICA Strategy for the prevention of losses Singleton, G.R 1989. Population dynamics of an caused by plagues of Mus domesticus in rural outbreak of house mOllse (Mus domesticus) in Australia. EPPO Bulletin, 18,237-248. the mallee wheatlands of Australia­ Redhead, T.D., and Singleton, G.R. 1988b. An hypothesis of plague formation. Journal of examination of the "PICA" strategy for the Zoology (London), 219, 495-515. prevention oflosses caused by plagues of the Singleton, G.R and Brown, P.R 1998. Manage­ house mouse (Mus domesticus) in rural ment of mouse plagues in Australia: integra­ Australia. In: Korton, G.A. and Pech, RP., ed., tion of population ecology, bio·control and Vertebrate pest management in Australia:

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best farm practice. In: Cowan, D.P. and Feare, Singleton, G.R and Spratt, D.M. 1986. The effects CJ., ed., Advances in vertebrate pest manage­ of Capillaria hepatica (Nematoda) on natality ment. Furth, Filander Verlag, 189-203. and survival to weaning in BALB/ c mice. Singleton, G.R and Chambers, L.K. 1996. A Australian Journal of Zoology, 34, 677-681. manipulative field experiment to examine the Singleton, C.R and Spratt, D.M. 1990. Biological effect of Capillaria hepatiea (Nematoda) on control of mice-the challenge, progress and wild mouse populations in southern prospects. In: Noble, J.C, Joss, P.J. and Tones, Australia. International Journal for Parasitol­ C.K., ed., The mallee lands: a conservation ogy, 26, 383-398. perspective. Proceedings of the National Singleton, G.R, Chambers, L.K. and Spratt, D.M. Mallee Conference, Adelaide, April 1989. 1995. An experimental field study to examine Melbourne, CSIRO, 238-242. whether Capillaria hepatica (Nematoda) can Singleton, G.R., Spratt, D.M., Barker, S.e. and limit house mouse populations in eastern Hodgson, P.F. 1991. The geographic distribu­ Australia. Wildlife Research, 22, 31-53. tion and host range of Capillaria hepatica Singleton, C.R and McCallum, H.!. 1990. The (Bancroft) (Nematoda) in Australia. Interna­ potential of Capillaria hepatiea to control tional Journal of Parasitology, 21, 945-957. mouse plagues. Parasitology Today, 6, 190- Smith, A.L., Singleton, G.R, Hansen, GM. and 193. Shellam, G. 1993. A serologic survey for Singleton, GR, McCallum, H.!. and Spratt, D.M. viruses and Mycoplasma pulmonis among wild 1990. Fertility control of house mice using an house mice (Mus domestieus) in southeastern hepatic nematode. Proceedings of the "Fertil­ Australia. Journal of Wildlife Diseases, 29, ity Control of Wildlife" Conference, 219-229. Melbourne, 21-23 November, 1990. S-PLUS 4 Guide to Statistics. 1997. Seattle, Data Singleton, G.R and Redhead, T. 1989. House Analysis Products Division, Mathsoft. mouse plagues. In: Noble, le. and Bradstock, Spratt, D.M. 1990. The role of helminths in the RA., ed., Mediterranean landscapes in biological control of mammals. International Australia: maliee ecosystems and their Journal for Parasitology, 20, 543-550. management. Melbourne, CSIRO, 418-33. Spratt, D.M. and Singleton, GR. 1986. Studies of Singleton, G.R. and Redhead, T.D. 1990a. Struc­ the life cycle, infectivity and clinical effects of ture and biology of house mouse populations Capillaria hepatica (Bancroft, 1893) that plague irregularly; an evolutionary (Nematoda) in mice (Mus musculus). Austral­ perspective. Biological Journal of the Linnean ian Journal of Zoology, 34, 663-675. Society, 41, 285-300. Spratt, D.M. and Singleton, G.R 1987. Experi­ Singleton, G.R and Redhead, T.o. 1990b. Future mental embryonation and survival of eggs of prospects for biological control of rodents Capillaria hepatica (Nematoda) under mouse using micro- and macro-parasites. In: Quick, burrow conditions in cereal-growing soils. C.R, ed., Rodents and rice. Report and Australian Journal of Zoology, 35, 337-341. proceedings of an expert panel on rice rodent Tann, CR., Singleton, G.R and Coman, B. C 1991. control, Los Banos, Sept. 10-14,1990, IRRI, Diet of the house mouse (Mus domestieus) in the Philippines, 75-82. malIee wheatlands of north-western Australia. Singleton, GR, Smith, A.L, Shell am, G.R, Wildlife Research, 18, 1-12. Fitzgerald, N. and Muller, W.J. 1993. Preva­ Taylor, J.D., Stephens, CP., Duncan, RG. and lence of viral antibodies and helminths in Singleton, C.R. 1994. Polyarthritis in wild field populations of house mice (Mus domesti­ mice (Mus musculus) caused by Streptobacillus eus) in southeastern Australia. Epidemiology moniliformis. Australian Veterinary Journal, and Infection, 110,399-417. 71,143-145.

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Twigg, L.E. and Kay, B.J. 1994. The effects of Veitch, L.G. and Anderson, R.B. 1985, Mouse microhabitat and weather on house mouse plagues in South Australia. CSIRO, Division (Mus domesticus) numbers and the implica­ of Mathematics and Statistics, Consulting tions for management. Journal of Applied Report No. SAC 85/17. Ecology 31, 651-663. VENSIM@DSSReferenceSupplementVersion 3.0.1997. Ventana Systems, Inc., USA.

112 Chris R. Dickman

Abstract

Because of their ability to use agricultural production and their role in spreading disease in humans, rodents are often viewed as having negative impacts in modified and natural ecosystems. Some species, such as the black rat, have been further implicated in the extinctions of many species of insular land birds, small mammals and invertebrates. In this review, I focus on the interactions of rodents with chemical and structural attributes of the environment, using the concept of 'ecosystem engineering' as a framework. I also discuss the direct and indirect impacts of rodents on food resources. Many rodents alter the structure of their environment by surface tunnelling, construction of leaf or stick nests, arranging pebbles around burrow entrances, or stripping bark from trees. These activities provide living space or resource opportunities for other organisms, and represent examples of simple allogenic engineering. In more complex examples, digging, nest-building and other activities modify the environment more extensively and modulate resource flows to other organisms. Burrowing rodents such as pocket gophers, prairie dogs and mole-rats alter soil structure and microtopography, nutrient cycling and water flows over local or regional areas, and have dramatic effects on the growth and species composition of plant communities. Nest structures that divert resource flows also represent complex allogenic engineering. For example, beaver impoundments affect nutrient cycles and water flow, and consequently the species richness of aquatic invertebrates, fish and riparian vegetation at local and catchment scales. Rodents also engineer local environments biotically by dispersing seeds and the storage organs of geophytes, as well as the spores of hypogeal fungi that form mycorrhizal associations with plants. Some species probably also play a minor role as pollinators. Rodents, finally, have diverse and often pervasive effects on their food resources; there is much evidence of positive and negative effects on growth form, standing crop and the species composition and physical structure of plant communities Rodents therefore contribute importantly to ecosystem function, and may have value as indicators of environmental change. Management of rodent pests will need to move away from the broadly destructive current approach of chemical warfare toward ecologically-based solutions that sustainably control only the target species.

Keywords

Ecosystem engineering, environment, rodent, facilitation, predation, nests, burrows

113 Ecologically-based Rodent Management

INTRODUCTION pollinators or vectors of fungal spores (Tory et al. 1997). Both microtine and sciurid rodents have been used as indicators of LTHOUGH SOME 1,800 species of industrial pollution (Kostelecka-Myrcha et modem rodents have been al. 1981; Lepage and Parker 1988), while A described (Corbet and Hill 1991), some murids have been used to indicate the few have been well-studied and the majority severity of impact wrought by defoliants remains poorly known. Not surprisingly, used in chemical warfare (Sokolov et al. most knowledge has been obtained on 1994; Evgenjeva and Fadeeva 1996). Several that impact on humans by exploiting further species also may be sensitive agricultural production or by spreading barometers of climatic change (Frey 1992; diseases (Chitty and Southern 1954; Twigg Bright and Morris 1996). 1978), or are useful in laboratory research The range of interactions of rodents with (Barnett 1975). Different species of rodents, the environment is not well appreciated, especially Rattus spp., have been implicated perhaps because the interactions are also in the demise of island vertebrate faunas diverse, often complex, or not apparent in (Atkinson 1985, 1996), and have often been studies carried out in small study areas or subject to intensive control to achieve for short periods. However, such an conservation objectives. Effective appreciation is likely to be important for management of rodent pests remains an successful management of rodent elusive but important goal in many parts of and essential if management is to be the world, and for different reasons. As ecologically-based. discussed by various authors in this book, In the present paper, I present a selective solutions may lie more with ecologically­ review of rodent-ecosystem relationships, based management than with simple one­ focusing on the impacts of rodents on the factor approaches that have been used physical, chemical and biotic environments previously. and the consequences of these impacts for Despite the often negative effects of other biota. Little attention is given to rodents in natural and modified competitive relationships among rodents or ecosystems, many species have been shown to rodents as prey, because reviews of these to contribute to ecosystem function and to topics are available elsewhere (Sinclair have value as indicators of environmental 1989; Brown and Harney 1993; Dickman change. For example, microtine rodents are and Doncaster, submitted for publication). important at times in the cycling of carbon, Where possible, studies that demonstrate nitrogen and other elements (Inouye et al. interactions experimentally have been 1987a, Huntly 1991), while beavers cause emphasised, because these are most likely alteration of hydrological regimes (Naiman to identify the nature and magnitude of any et al. 1988). Such species have been termed interactions that occur. The concept of 'ecosystem engineers' (Jones et al. 1994). 'ecosystem engineering' is used to provide Other species may be important as a framework for much of the review.

114 Rodent Ecosystem Relationships

ECOSYSTEM ENGINEERING given in Figure 1; this approach also provides consistency in this review. Trophic The term'ecosystem engineering' was interactions do not fit an engineering introduced by Jones et a1. (1994) and refined paradigm, and the effects of rodents on plant by Jones et a1. (1997). It may be defined as and invertebrate prey species are discussed follows: "Physical ecosystem engineers are separately below. organisms that directly or indirectly control the availability of resources to other ALLOGENIC ENGINEERING organisms by causing physical state changes in biotic or abiotic materials. Physical Simple cases: changes in physical ecosystem engineering by organisms is the state (Figure 1a) physical modification, maintenance or creation of habitats. The ecological effects of Rodent burrows are obvious and widespread engineering on other species occur because examples of allogenic engineering. Simple the physical state changes directly or burrows are made by most species at some indirectly control resources used by these time in their life cycle, and vary in size, other species" (Jones et al. 1997, p. 1947). orientation, depth and substrate Engineers were divided into two broad characteristics. Among Australian desert groups by Jones et a1. (1994, 1997). Autogenic rodents, Pseudomys hermannsburgensis and engineers change the environment by their Notomys alexis dig deep, vertical burrows in own physical structures; an example would be summer to avoid high daily temperatures, but the shed limbs of trees that modulate occupy shallow surface burrows in other microclimate and microhabitat for other seasons when temperatures, and daily organisms on the forest floor. In contrast, variations in temperature, are less extreme allogenic engineers change the environment by (CR. Dickman, personal observation). Other transforming living or abiotic materials from species, such as Rattus colletti, barely modify one state to another by mechanical or other cracks in the soil (Madsen and Shine 1999) Of, means. An example would be the construction like Rattus villosissimus, may construct of burrows by one species that could be used complex networks of tunnels under by others. Rodents could be expected to be favourable conditions (Predavec and allogenic engineers. Dickman 1994). The burrows of many species In both their papers, Jones et a1. (1994, have been described in the literature (e.g. 1997) drew a distinction between physical Kemper 1981; Bronner 1992), with overviews ecosystem engineering and other ecological provided by Reichman and Smith (1990), processes such as pollination, dispersal, Meadows and Meadows (1991) and Hansell competitive and trophic interactions, (1993). including the utilisation of living or dead The major resource created by burrows is tissue by consumers or decomposers. In the living space for other organisms. Other present paper, however, I include the former rodents, lizards, snakes and many species of two of these processes under the term 'biotic invertebrates make opportunistic use of engineering'. Justification for this approach is burrows (Kiviat 1978; Skinner and Smithers 1990). In arid Australia, several species of

115 Ecologically-based Rodent Management

dasyurid marsupials make extensive use of nesting, roosting and shelter sites for several abandoned rodent burrows, being unable to species of birds, bats and other arboreal dig burrows themselves (Dickman and Read mammals (Corbet and Harris 1991; 1992; Dickman 1996). In one study, the MacKinnon et al. 1996). It is likely that burrowing activity itself, in reducing rodent-induced damage to plants provides compaction of soil, was shown to have the opportunities for exploitation by a broad additional effect of promoting germination range of organisms, but few relevant studies of seeds of an iridaceous geophyte have been carried out to confirm this (for a (Contreras and Gutierrez 1991). general discussion, see Karban and Myers Nests provide another example of 1989). allogenic engineering. Simple constructs, such as the cup-shaped grass nests of Complex cases: state changes that Micromys minutus, may take hours or days to modulate resource flow (Figure 1b) build and last for the duration of one Continual and intensive burrowing activity breeding season (Harris and Trout 1991); by rodents may provide temporary living more complex structures of sticks and other space for other organisms, but it also affects detritus, engineered by Leporillus spp. and nutrient cycling, water flow, soil structure Neotoma spp., often last for generations and microtopography. Such effects have been (Copley 1988). Nests are made from a variety studied in detail in several species of fossorial of living and non-living materials, and are and terrestrial rodents, especially North sometimes decorated with pebbles or other American geomyids, or pocket gophers, materials (Anstee et al. 1997) for reasons that prairie dogs and Old World mole-rats. remain unclear. As with burrows, nests The digging activities of pocket gophers provide living space for other species of (70-350 g) produce small piles of fresh surface vertebrates and invertebrates. Such soil that may, over extended periods, exploitation is usually opportunistic. accumulate into large mounds termed mima However, blind, wingless earwigs of the mounds (Inouye et al. 1997). In some habitats, genus Hemimerus are found primarily in the digging activity can cast over 15,000 kg of nests of Cricetomys gambianus, and may be soil/ha/year onto the surface, and mima obligatelyassociated (Knight 1984). mounds of 25-50 m in diameter and 2 m in Two, more subtle examples of allogenic height may be common (Beuchner 1942; Ross engineering may be cited. The first involves et al. 1968). Some 50-100 mima mounds have shallow scrapes created in surface soil by been recorded per hectare in some areas, with foraging rodents that provide sites for higher densities occurring usually in accumulation of seeds (McNaught 1994, see disturbed prairie and agricultural landscapes also below). The second involves bark­ (Mielke 1977). The mounds may consist stripping of trees by Sciurus spp., entirely of topsoil, or soil with gravel and Sundasciurus spp.and other squirrels pebbles 50-60 mm diameter; in some (Med way 1983). De-barking facilitates access locations the presence of soil horizons within of fungal pathogens to vascular tissues mounds suggests a long period of (Abbott et al. 1977), while dead trees provide stabilisation (Cox and Gakahu 1986).

116 Rodent Ecosystem Relationships

Comparisons of soils from mow1ds and conditions (Hobbs and Mooney 1991 ); the lmdisturbed inter-mound areas have shown timing and intensity of soil disturbance may differences in texture, organic content, also be important (Moloney et aJ. 1992). water-holding capacity and nutrient status Fin ally, in tallgrass prairie, the mOlmds of (Mielke 1977; Hobbs and Hobbs 1987; Geornys bursarius have complex effects on Inouye et a l. 1987b; H untly and Inouye both vegetation and faw1a. MOlmds break 1988). These differences in turn promote the prairie canopy and provide recruitmen t heterogeneity in plant species composition sites for d icot seedlings, often increasing an d growth responses. In shortgrass prairie, local plant diversity (Hartnett and Keeler the burrowing activities of Thomornys bottae 1995). MOlmds also attrac t some herbivores may kill standing vegetation but provide such as grasshoppers, but may eitl1er attract opportunities for establishm ent of or repel mammalian herbivores sllch as the herbaceolls perennial dicots (Martinsen et al. meadow vole Micro tus pennsylvanicus 1990). In serpentine grassland, moun ds of (Whittaker et al. 1991; cf. Klaas et aJ. 1998) . If T. bottae are invaded by different species of mounds alter local patterns of herbivory, plants depending on preva il i.ng rainfall this is likely to produce further effects on

Allogenic or biotic engineering Resource Flows 1 (a) (b) t State 1 ! State 1 State 2 • State 2 = Resource • J i 1 Organism Organism

Figure 1. Conceptual models of allogenic and biotic engineering, as applied to rodents (after Jones et al. 1994, 1997). In the simplest case, (a), living or non-living raw materials are transformed by animal activity from state 1 to state 2. The point of modulation is shown by opposing arrow heads. In allogenic engineering, state 2 is a new engineered resource such as a burrow that usually can be used immediately. In biotic engineering, state 2 is an activated but incipient resource such as a pollinated flower or dispersed seed or spore that may be structurally no different from the state 1 condition. In the more complex case, (b), the product s of state 2 modulate the flow of one or more resources to other species. Such modulation may be rapid if state 2 resources have been engineered allogenically, but slow if engineering has been biotic and is cont ingent on growth of plant or fungal tissue. Jones et al. (1994, 1997) discussed additional types of allogenic and autogenic engineering, but these do not appear relevant to rodents. 'Biotic engineering' is used for the first time here.

117 Ecologically-based Rodent Management

plant community structure and large volumes of soil and often result in the heterogeneity, perhaps promoting species creation of surface mounds. These surficial richness over time (Klaas et al. 1998). structures resemble the mounds of pocket Like their smaller counterparts, prairie gophers and prairie dogs in size and dogs (1 kg) also modulate resource flows to composition, and have usually similar other species by digging. Research on the effects on nutrient status, water flow and best-studied species, Cynomys ludovicianus, organic content (Jarvis and Sale 1971; Cox shows that colonies develop on deep, and Gakahu 1985; Cox et al. 1987). Cox and productive soils where flooding is unlikely, Gakahu (1985) showed that coverage of and range in size from tens to hundreds of forbs and shrubs on mima mounds of hectares (Dahlsted et al. 1981; Hoogland Tachyoryctes splendens was more than double 1994). Up to 300 burrows may occur per that on inter-mound plots, whereas coverage hectare, with soil mounds 1-2 m diameter of grass and Acacia trees was much reduced. surrounding each burrow entrance (Whicker These authors also noted a correlation and Detling 1988). Digging affects soil between the activity areas of mole-rats and a structure and compaction, increases fungus-gardening termite-Odontotermes drainage and, with grazing by prairie dogs, sp., and suggested that termites the cycling of nitrogen and other nutrients preferentially use the rich organic deposits (Coppock et al. 1983). Although grazing and in mole-rat nest chambers to establish engineering effects have not been fungus gardens. A wide range of disentangled in studies of C. ludovicianus, invertebrates has been documented using both probably contribute to extensive the nest mounds of the blind mole-rat Spalax patteming of plant communities within ehrenbergi (Heth 1991). However, it is not prairie dog colonies. In mixed-grass prairie, clear here whether mound use represents a Coppock et al. (1983) showed that grasses simple case of allogenic engineering, or a decreased in biomass with colony age more complex case where mounds modulate whereas forbs and dwarf shrubs increased; food or other resources that sustain the nitrogen in graminoid shoots also peaked in invertebrate communities. Further examples long-established colonies. The modified of fossorial or semi-fossorial rodents habitats produced by prairie dog modulating resource flow for other species excavations favour increased local by their burrowing activities occur within abundances and diversity of open-plain the Microtinae, Octodontidae and birds but decreased species richness of small Heteromyidae Chew and Whitford mammals (Agnew et al. 1986). Interestingly, 1992; Contreras and Gutierrez 1991; G6mez­ colony sites also contain higher densities of Garcia et a1. 1995; Borghi and Giannoni soil nematodes than undisturbed areas 1997). A useful review is provided by (Ingham and Detling 1984), perhaps Huntly and Reichman (1994). reflecting greater ease of establishment in Nest structures that divert resource flow loosened soiL represent a further class of examples of Burrowing and tunnelling activities by complex allogenic engineering. Beaver dams fossorial rodents such as mole-rats displace are the most conspicuous examples of such

118 Rodent Ecosystem Relationships

structures; similar but less extensive nests and, to a lesser extent, for the related Castor are made by muskrats Ondatra zibethicus and fiber in Europe (Cirmo and Driscoll1993; occasionally by Myocastor coypus (Ebenhard Macdonald et al. 1995). 1988). The physical structure of beaver dams, Beaver dams are constructed of young and particularly the effects of dams on and mature trees that the animals cut resource flows, have important themselves, as well as sediments and other consequences for aquatic and terrestrial debris. The North American beaver, Castor animals and riparian vegetation. In the short canadensis, builds some 2-16 dams per term (years) impoundments may kill kilometre of stream, with small dams streamside trees and provide nest or roost containing 4-18 m3 and larger dams> 100 m3 sites for volant vertebrates following of wood (Naiman et al. 1986,1988). The formation of hollows. In the longer term major effect of dams is to alter the stream (decades to millenia), impoundments are channel by impounding water, creating likely to be colonised by wetland plants and patch bodies (sensu Johnston and Naiman follow successional pathways that may lead 1987) of water, sediment, aerobic soil to meadows, bogs or wetlands (Figure 2). beneath the pond and anaerobic soil in The relative roles of beaver engineering and deeper strata. The surrounding riparian other physical processes such as erosion, zone is also affected by damming, with sedimentation and fire in directing stream widths sometimes increased by an particular pathways remain unclear, but order of magnitude from their original likely differ between regions (Naiman et al. condition (Naiman et al. 1988). Because of 1988,1994; Johnston 1995). the changed hydrological regime and the Damming produces a shift from lotic (fast additional effects of beaver herbivory, patch flowing) to more lentic (still-water) bodies show dramatically different fluxes of conditions, especially in higher order carbon, nitrogen and energy compared with streams. Among aquatic invertebrates, this unaltered streams. Impoundments usually shift favours collector and predator species have relatively low inputs of carbon, but such as tubificid worms, clams and high standing stocks and outputs (Naiman dragonflies over shredder and scraper et al. 1986); significant fluxes arise from species such as blackflies, scraping mayflies release of methane (Naiman et al. 1991; and net-spinning caddisflies (McDowell and Yavitt et al. 1992). Impoundments have been Naiman 1986). However, lotic taxa may still shown further to enhance accumulation of be represented highly on the dam walls, nitrogen in sediment by 9-44 fold compared perhaps because the dam acts as a net that with undisturbed streams (Francis et aL traps drifting lotic fauna (Clifford et al. 1985). The effects of impoundment on pH, 1993). Among fishes, lotic taxa give way dissolved oxygen, fluxes of energy, other similarly to still-water specialists in beaver nutrients and ions have been much studied impoundments. Species richness and for C. canadensis in many parts of its range composition differ in dammed headwater Wilde et aL 1950; Hodkinson 1975; and lower-order streams and vary also with and Naiman 1991; Naiman et al. 1994) age of the impoundment (Keast and Fox

119 Ecologically-based Rodent Management

Beaver activity Sedimentation, erosion, hydrology

Emergent Po~ O wetland ~o/0 - 0 / ~ o \ o Bog t 0ldpoo St"am " / 0 , ! f":\ Fi ~ 0 Forested \.V wetland Meadow

1-100 years 50-200 years 200-2000 years

Reversible Irreversible succession succession

Figure 2. Potential effects of beaver ( Castor canadensis) on vegetation and landscape patterns, based on work by R.J. Naiman and colleagues in the boreal forests of northern Minnesota (after Naiman et a!. 1988).

1990; Hagglund and Sjoberg 1999; Snodgrass Chrysomela confluens. The beetles sequester and Meffe 1998). phenolic glycosides from the cottonwood Descriptive and experimental studies leaves and use them as a means of predator have suggested further that beaver ponds defense. Martinsen et a1. (1998) asserted act as reproductive source populations for further that habitat mosaics created by fish whereas adjacent streams act as sinks beaver activity increase the diversity of (Schlosser 1995). If so, beaver dams may be arthropods and perhaps higher vertebrates seen as important components of fish as well, but provided no evidence in support metapopulations at catchment or larger of this claim. spatial scales. A final class of examples of complex The engineering activities of beavers allogenic engineering is the surface digging may, finally, have subtle indirect effects on activity of rodents that results in terrestrial invertebrates. Martinsen et a1. accumulation of organic material and (1998) have shown recently that resprout diversion of water flow. Gutterman (1982) growth from beaver-cut cotton wood trees showed that the diggings of Indian crested (Populus fremontii and Populus angustifolia) is porcupines, Hystrix indica, accumulate seeds attractive to a specialist leaf beetle, and other organic matter, and provide

120 Rodent Ecosystem Relationships

microhabitats favourable for the germinate and become established (Vander germination and establishment of certain Wall 1990), but the role of rodents as species of plants. Diggings are more suitable dispersal agents remains poorly known. In for germination in protected than exposed one particularly instructive recent study, habitats, apparently because they allow run­ Vander Wall (1997) showed that some 80% off of rainfall for longer periods (Gutterman of pifion pine (PilIUS monophylla) seeds, and Herr 1981; see also Yair and Rutin 1981). placed experimentally on the ground Steinberger and Whitford (1983) presented beneath trees, were gathered by rodents. similar findings from their work on the Radioactively labelled seeds were mostly surface digging activities of desert cached, either in scatter-hoards or larders, at heteromyids. distances up to 38.6 m from the source. Over Studies of larger mammals such as brush­ a third of caches occurred beneath shrubs; tailed bettongs (Bettongia penicillata) and these appeared to favour establishment, and grizzly bears (Ursus arctos horribilis) indicate served as nurse plants for young pines. that surface digging activity can Vander Wall (1997) demonstrated seed dramatically decrease soil water repellency caching by four species of rodents in and enhance levels of mineral nitrogen captivity-Peromyscus maniculatus, (Garkaklis et al. 1998; Tardiff and Stanford Peromyscus truei, Perognathus parous and 1998). Such effects might be predicted also Dipodomys panamintinus-and inferred that from the digging activity of larger rodents, these were the main seed dispersers in his but do not appear yet to have been field site too. documented. Fossorial rodents have also been demonstrated to move the storage organs of BIOTIC ENGINEERING geophytic plants, often concentrating them Dispersal of seeds and spores within mounds or burrow systems (Galil 1967; G6mez-Garcia et al. 1995). Sprouting of Although movements of seeds or spores storage organs at their new locations from one place to another constitute biotic suggests that rodent-induced dispersal can engineering as defined here, the be effective (Borghi and Giannoni 1997). phenomenon is ecologically more relevant Dispersal of fungal spores by rodents has after growth of the embryonic tissue has received relatively little attention. Many become sufficient to modulate resource flow species eat the fruiting bodies of fungi (e.g. to other organisms. Movement of seeds by Maser et al. 1978; Claridge and May 1994; rodents is well established. In some species, Tory et aL 1997), but it has not always been such as tropical squirrels, seeds are ingested and later excreted elsewhere in the animals' shown that ingested spores remain viable. However, spores usually remain structurally home ranges (Em mons 1992; MacKinnon et intact following passage through rodent al. 1996). In many other species, seeds are collected and cached, or hoarded, for later guts, and Claridge et al. (1992) showed that spores recovered from faeces of another consumption (GumeIl1983; Reichman and mammal, Potorous tridactylus, developed Price 1993). Seeds often survive caching to ectomycorrhizae on the roots of two species

121 Ecologically-based Rodent Management

of Eucalyptus. Importantly, the fungi TROPHIC IMPACTS OF RODENTS ingested by many species of rodents are Rodents take a very broad range of plant and hypogeal and form mycorrhizal associations animal foods, so their potential effects on with the roots of trees and other vascular prey species and communities could be plants, thus potentially assisting plant pervasive. Some species of rodents specialise growth. Future research should seek to in taking only one or two prey taxa (e.g. the clarify the extent to which rodents disperse heteromyid Liomys salvini specialises viable spores, and also quantify their seasonally on seeds of Enterolobium contribution to regeneration and cyclocarpum, a Central American leguminous development of forest environments tree; Janzen 1981), whereas others are (Reddell et al. 1997; Tory et aL 1997). broadly omnivorous (e.g. many species of Australian desert rodents; Murray et al. Pollination 1999). The direct impacts of rodent predation Bats and primates that visit flowers for food have a long history of study, especially with are often effective pollinators, especially in respect to effects on crops and other tropical and arid habitats (Fleming and Sosa vegetation, but indirect impacts have been 1994). The effectiveness of rodents as recognised increaSingly in recent work. This pollinators, however, is less clear. Many is a vast topic that can only be treated species visit flowers and could transfer superficially here. pollen that has lodged in the fur (Recher The best estimates of rodent impact on 1981). Examples include arboreal food resources are from agro-ecosystems in such as dormice-Mllscardinus avellanarius different parts of the world (e.g. Buckle and (Bright and Morris 1996), tree-rats-Solomys Smith 1994; Singleton and Petch 1994; other spp. (D. Fisher, pers. comm.) and desert chapters in this book). In these simplified rodents in the genus Pseudomys environments, rodents can reach (CR. Dickman, persona] observation). Few extraordinary densities (e.g. >3,OOO/ha for studies have shown that rodents carry Mus domesticus; Caughley et aL 1998) by significant loads of pollen between flowers eating one or a very few types of food, and (Lumer 1980; Wiens et al. 1983; Van Tets cause great damage to crops. Both native 1997) and none has yet distinguished the and introduced species of rodents can relative importance of rodents as pollinators become pests, and achieve higher densities compared with other taxa (Carthew and in crop systems than in the natural Goldingay 1997). As Flerning and Sosa environment. Very high densities may be (1994) point out, the genetic effects of even achieved transiently by rodents in the more conspicuous mammalian unmodified environments, often following pollinators and frugivores on plant drought-breaking rains (e.g. 1,200/ha for populations have been rarely investigated; R. villosissimus; Palmer 1886), but impacts on there is much scope for new research. food resources under these conditions have been little-studied (Batzli and Pitelka 1970; Noy-Meir 1988).

122 Rodent Ecosystem Relationships

In natural or little modified environ­ Perhaps because the impacts of rodents ments, rodents may have local or broad­ on vegetation are often obvious and scale effects on vegetation. Below ground, economically relevant, the effects of rodents herbivory often modifies plant community on other food groups have been seldom structure, reducing the standing crop but studied. However, limited experimental increasing local species richness (Andersen evidence suggests that high density 1987; Huntly and Reichman 1994). Selective populations of omnivorous species may foraging on individual plant species may deplete the local richness of epigeal benefit certain life-history stages such as invertebrates (Figure 3). On Boullanger seeds or small bulbs by reducing Island, Western Australia, invertebrate intraspecific competition (Contreras and species richness increased on average by 3% Gutierrez 1991), but can also depress plant on plots from which M. domestic us had been biomass and flower production (Reichman removed, in contrast to a decrease of 18% on and Smith 1991) or even result in local plant control plots (Figure 3a). Increases occurred extinction (Cantor and Whitham 1989). primarily in beetle and spider species, which Above ground, rodent herbivory (including the mice ingested (CR. Dickman, personal frugivory and granivory) has even more observation). In urban woodland in the dramatic effects on vegetation. Selective United Kingdom, invertebrate species foraging may again deplete favoured species richness increased similarly by 83% on plots in local areas, and alter trajectories of plant from which Apodemus sylvaticus had been succession Uohnston and Naiman 1990). removed, compared with only a 32% increase Generalist foraging has been shown to have on control plots (Figure 3b). Increases pervasive effects on life form, growth, occurred in species of beetles, spiders and allocation of nutrients and energy stores snails-taxa found commonly in the diet of within plants, as well as on the physical urbanA. sylvaticlIs (CR. Dickman, personal structure and species composition of plant observation). Primarily insectivorous communities (Batzli and Pitelka 1970; Brown rodents such as grasshopper mice et a1. 1979; Brown and Heske 1990; Holland (Onychomys spp.) likely affect individual et a1. 1992; Jefferies et a1. 1994; but d. Gibson species and communities of invertebrates at et a1. 1990). Although this topic is too broad times also, but evidence is lacking. to discuss fully here, the effects and In circumstances when omnivorous mechanisms by which herbivores affect rodents have been introduced to new plant communities have been reviewed by environments, they have sometimes had Crawley (1983) and Huntly (1991), and the dramatic effects on populations of induction of plant defenses has been invertebrates and small vertebrates. On Lord reviewed by Karban and Myers (1989). Howe Island, for example, an endemic Short-term feed backs and longer-term phasmid, Dryococelus austraIis, disappeared coevolution between herbivorous rodents following establishment of Rattus rattus, and plants also have been discussed in detail while numbers of two species of island snails elsewhere (Crawley 1983; Coley and Barone were severely depressed (Smithers et aL 1996; Pastor et a1. 1997). 1977).

123 Ecologically-based Rodent Management

60

(/) (/) 50 Cl> c .<:: u .'" 40 (/) Cl> ·0 ~ 30 (/) Cl> . ~ Bi 20 :::J E :::J 0 10

0 Apri l May June July August

Figure 3. Effects of rodent removal on species richness of invertebrates. (a) Mus domesticus was removed from trapping plots on Boullanger Island, Western Australia, and invertebrates sampled by pitfall trapping before and after removal in both t he removal and control sites ( n = 3 control, 3 removal plots, means shown ± standard error (SE); mean before/after ratios of species richness differed significantly bet ween control and removal treatments, P < 0.0 5).

50

Control (/) (/) 40 • Removal Cl> c .<:: u • .'" (/) . ~ 30 u Cl> 0- (/) Cl> > 20 ~ :::J E :::J 0 10

0 May June July August

(b) Apodemus sylvaticus was removed from trapping plots in urban woodland in Oxford, United Kingdom, and invertebrates sampled in the same manner as in (a) (n = 3 control, 3 removal plots, means shown ± SE; mean before/after ratios of species richness differed significantly between control and removal treatments, P <0.01). Methodological details are given in Dickman (1988), Dickman and Doncaster (1989; also unpublished data).

124 Rodent Ecosystem Relationships

Extinctions and range contractions of Finally, while most research has many other species of large invertebrates evaluated the direct trophic impacts of and small vertebrates, including seabirds rodents, some recent work indicates that and flightless birds, have occurred on rodent foraging may have far-reaching islands off the coast of New Zealand and indirect effects. In Californian grassland, throughout the Pacific following Batzli and Pitelka (1970) showed that forb introductions of R. rattus, Rattus exulans and and grass cover increased in plots that Rattus norvegicus (Steadman 1989; King excluded the herbivorous meadow vole, 1990). Although rats appear to have been the Microtus californicus, as compared with cover only obvious threat introduced to some levels in control plots. An indirect effect of islands, in many cases their impact is the vole exclusion was a dramatically difficult to distinguish from the effects increased abundance of the pillbug wrought by other introduced species and by (Annadillidium vulgm'e) within two years; this habitat change. species was apparently favoured by the It remains equivocal also whether rat denser vegetation or increased food impacts were caused by predation, resources that it contained. In analogous competition, introduction of diseases or experiments, removal of M. dom esticus from other processes, although direct predation plots on Boullanger Island resulted in a 24% has been implicated by most authors i.ncrease in li tter depth within just three (Smithers et al. 1977; King 1990; Atkinson months, compared with a 16% decrease in 1996). litter depth on control plots over the same period (Figure 4).

2.5

• Control T 2 • Removal E ~ .c Cl. 1.5 Ql - .!!1 ~ :.:J 05

0 April May June July August

Figure 4. Effects of removal of Mus domesticus on depth of the leaf litter layer on Boullanger Island, Western Australia (n = 3 control, 3 removal plots, means shown ± standard error; before/after ratios of mean litter depth differed significantly between control and removal treatments, P < 0.01). Further details are given in Dickman (1988).

125 Ecologically-based Rodent Management

Capture rates of the skinks (Ctenotus fallens ubiquity of rodents in terrestrial and Morethia lineoocellata) increased in the environments. Mus-removal plots by up to 35% (CR. With respect to the management of Dickman, personal observation), presumably rodent pests, the review also allows the because of the increased shelter afforded by conclusion to be drawn that we must be the deep leaf litter or the more diverse food more clever and more focused in our resources that were available (Figure 3a). approaches to rodent control. In many Over larger periods, rodent foraging can regions, broad-scale application of poison indirectly facilitate other taxa. In the remains the favoured control method Chihuahuan Desert, Thompson et al. (1991) (Buckle and Smith 1994; Singleton and Petch demonstrated that the foraging activities and 1994). In the 1993 mouse plague in south­ abundance of granivorous birds declined eastern Australia, for example, some 350,000 markedly in rodent exclusion plots over a ha of cropland in South AQstralia alone were period of 10 years. In the absence of rodents, baited with the poison strychnine (Caughley especially kangaroo rats (Dipodomys spp.), et al. 1994). Such broad-scale campaigns may litter accumulated and concealed seeds on the reduce the numbers of the target pest, but soil surface from the view of the visually very likely decimate populations of non­ foraging birds. In control plots by contrast, target species (Dickman 1993), including rodent foraging activities created areas of those with potentially positive effects on the bare soil and trails, hence exposing seeds and physical and biotic environment. In the facilitating access by birds. Brown and Heske wheat-growing areas of New South Wales, (1990) considered kangaroo rats in the native rodents have been virtually Chihuahuan Desert to be a keystone guild in eliminated by introduced species, changes in recognition of their major direct and indirect land use, and perhaps also by agrochemicals effects on biological diversity and that are used to maintain the biogeochernical processes. More complex (Dickman 1993). It is clear that management webs of direct and indirect effects of rodent of rodent pests will need to eschew its foraging are suspected (e.g. Klaas et al. 1998), damaging reliance on chemical warfare and and will require much ingenuity to study and embrace sustainable, ecologically-based understand. solutions. Heartening moves in this direction include fertility control (Chambers CONCLUSIONS et al., Chapter 10), mortality control via This review shows that rodents interact predators or parasites that target pest taxa extensively with their physical, chemical (Buckle and Smith 1994), and physical and biotic environments, and that their barrier methods that limit access of pests to activities have complex but often beneficial crop areas (Singleton et al., Chapter 8). effects on other organisms across a broad range of spatial and temporal scales. This ACKNOWLEDGMENTS should not be surprising, because of the I thank G. Singleton and L. Hinds for the great species richness, abundance and opportunity to prepare this review, and

126 Rodent Ecosystem Relationships

Z. Zhang and other members of the Beijing Atkinson, LAE. 1996. Introductions of wildlife as organising committee for hosting the a cause of species extinctions. Wildlife Biology, 2, 135-141. conference on rodent biology and Barnett, S.A 1975. The rat. Chicago, U.5.A, management. R. Baxter, c.-L. Beh, R. Shine, University of Chicago Presst 318p. N. Shchipanov and G. Sjoberg helped to find Batzli, G.O. and Pitelka, F.A 1970. Influence of elusive references or kindly provided reprints meadow mouse populations on California of the manuscripts, E. Gerzabek and G. grassland. Ecology, 51, 1027-1039. McNaught assisted with preparation of this Beuchner, H.K. 1942. Interrelationships between the pocket gopher and land use. Journal of manuscript, and P. Brown, C. McKechnie and Mammalogy, 23, 346-348. G. Singleton provided critical comments. I am Borghi, c.E. and Giannoni, S.M. 1997. Dispersal grateful also to the Australian Research of geophytes by mole-voles in the Spanish Council for funding my work on rodents, and Pyrenees. Journal of Mammalogy, 78, 550- to Commonwealth Scientific and Industrial 555. Research Organisation (CSIRO) Wildlife and Bright, P.W. and Morris, P.A 1996. Why are dormice rare? A case study in conservation Ecology for funding my attendance at the biology. Mammal Review, 26, 157-187. Beijing conference. This paper has benefited Bronner, GN.1992. Burrow system characteris­ from discussions with numerous conference tics of seven small mammal species (Mamma­ participants. lia: Insectivora; Rodentia; Carnivora). Koedoe,35,125-128. Brown, J.H. and Harney, B.A 1993. Population REFERENCES and community ecology of heteromyid Abbott, RJ., Bevercombe, C.P. and Rayner, rodents in temperate habitats. In: Cenoways, AD.M. 1977. Sooty bark disease of sycamore H.H. and Brown, J.H., ed., Biology of the and the grey squirrel. Transactions of the Heteromyidae. Provo, U.5.A., The American British Mycological Society, 69, 507-508. Society of Mammalogists, 618-651. Agnew, W., Uresk, O.W. and Hansen, RM.1986. Brown, J .H. and Heske, KJ. 1990. Control of a Flora and fauna associated with prairie dog desert-grassland transition by a keystone colonies and adjacent ungrazed mixed-grass rodent guild. Science, 250,1705-1707.

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Holland, E.A., Parton, W.]., Detling, J.K and Jefferies, RL., Klein, D.R. and Shaver, G.R 1994. Coppock, D.L. 1992. Physiological responses Vertebrate herbivores and northern plant of plant populations to herbivory and their communities: reciprocal influences and consequences for ecosystem nutrient flow. responses. Oikos, 71, 193-206. American Naturalist, 140,685-706. Johnston, CA. 1995. Effects of animals on Hoogland, J.L. 1994. The black-tailed prairie landscape pattern. In: Hansson, L., ed., dog: social life of a burrowing mammal. Mosaic landscapes and ecological processes. Chicago, U.S.A., University of Chicago Press, London, U.K., Chapman and Hall, 57-80. 576p. Johnston, CA. and Naiman, RI. 1987. Boundary Huntly,N.1991. Herbivores and the dynamics of dynamiCS at the aquatic -terrestrial interface: communities and ecosystems. Annual the influence of beaver and geomorphology. Review of Ecology and Systematics, 22, 477- Landscape Ecology, 1, 47-57. 503. Johnston, CA. and Naiman, RJ. 1990. Browse Huntly, N. and Inouye, R 1988. Pocket gophers selection by beaver: effects on riparian forest in ecosystems: patterns and mechanisms. composition. Canadian Journal of Forest Bioscience, 38, 786-793. Research, 20,1036-1043. Huntly, N. and Reichman, O.J. 1994. Effects of Jones, CG., Lawton, J.H. and Shachak, M. 1994. subterranean mammalian herbivores on Organisms as ecosystem engineers. Oikos, 69, vegetation. Journal of Mammalogy, 75, 852- 373-386. 859. lones, CG., Lawton, J.H. and Shachak, M. 1997. Ingham, RE. and Detling, J.K. 1984. Plant­ Positive and negative effects of organisms as herbivore interactions in a North American physical ecosystem engineers. Ecology, 78, mixed-grass prairie Ill. Soil nematode 1946-1957. populations and root biomass on Cynomys Karban, Rand Myers, J.H. 1989. Induced plant ludovicianus colonies and adjacent uncolo­ responses to herbivory. Annual Review of nized areas. Oecologia, 63, 307-313. Ecology and Systematics, 20, 331-348. Inouye, RS., Buntly, N.J. and Tilman, D.1987a. Keast, A. and Fox, M.G. 1990. Fish community Response of Microtus pennsylvanicus to structure, spatial distribution and feeding vegetation fertilized with various nutrients, ecology in a beaver pond. Environmental with particular emphasis on sodium and Biology of Fishes, 27, 201-214. nitrogen concentrations in plant tissues. Kemper, C1981. Description of Pseudomys novae­ Holarctic Ecology, 10, 110--113. hollandiae burrows located with radioiso­ Inouye, RS., Huntly, N.J., Tilman, D. and Tester, topes. Australian Mammalogy, 4, 141-143. J.R 1987b. Pocket gophers (Geomys bursarius), King, CM. (ed.) 1990. The handbook of New vegetation, and soil nitrogen along a succes­ Zealand mammals. Auckland, New Zealand, sional sere in east central Minnesota. Oecolo- Oxford University Press, 600p. 72,178-184. Kiviat, E. 1978. Vertebrate use of muskrat lodges Inouye, RS., Huntly, N. and Wasley, G.A.1997. and burrows. Estuaries, 1, 196-200. Effects of pocket gophers (Geomys bursarius) Klaas, B.A., Danielson, B.J. and Moloney, KA. on microtopographic variation. Journal of 1998. Influence of pocket gophers on meadow Mammalogy, 78, 1144-1148. voles in a tallgrass prairie. Journal of Janzen, D.H. 1981. Patterns of herbivory in a Mammalogy, 79, 942-952. tropical decid uous forest. Biotropica, 13, 271- Knight, M.H. 1984. The ecophysiology of the 282. African giant rat Cricetomys gambianus Jarvis, J.U.M. and Sale, J.B. 1971. Burrowing and (Waterhouse). Pretoria, South Africa, Univer­ burrow patterns of East African mole-rats sity of Pretoria, unpublished MSc. disserta­ Tachyoryctes, Heliophobius, and Heterocephalus. tion. Journal of Zoology, London, 163, 451-479.

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Kostelecka-Myrcha, A., Myrcha, A. and Meadows, P.S. and Meadows, A. (ed.) 1991. The Gutkowska, H.E. 1981. Hematological and environmental impact of burrowing animals morphophysiological indices of some and animal burrows. Oxford, U.K, Claren­ rodents under conditions of varying indus­ don Press. trial pressure. Polish Ecological Studies, 7, Medway, Lord 1983. The wild mammals of 145-153. Malaya (Peninsular Malaysia) and Singapore. Lepage,P. and Parker, G.H.1988. Copper, nickel, Kuala Lumpur, Malaysia, Oxford University and iron levels in peIage of red squirrels Press, 128p. living near the ore smelters at Sudbury, Mielke, H.W. 1977. Mound building by pocket Ontario, Canada. Canadian Journal of gophers (Geomyidae): their impact on soils Zoology, 66, 1631-1637. and vegetation in North America. Journal of Lumer, C 1980. Rodent pollination of Blakea Biogeography,4,171-180. (Melastomataceae) in a Costa Rican cloud Moloney, KA., Levin, S.A., Chiariello, N.R and forest. Brittonia, 32, 512-517. Butt~l, L. 1992. Pattern and scale in a serpen­ Macdonald, nw., Tattersall, F.H, Brown, E.D. tine grassland. Theoretical Population and Balharry, D. 1995. Reintroducing the Biology, 41, 257-276. European beaver to Britain: nostalgic Murray, B.R, Dickman, CR, Watts, CH.S. and meddling or restoring biodiversity? Mammal Morton, S.H. 1999. Dietary ecology of Austral­ I~eview, 25,161-200. ian desert rodents. Wildlife Research, 26, 421- MacKinnon, K, Hatta, G., Halim, Hand Manga­ 437. lik, A. 1996. The ecology of Kalimantan. Hong Naiman,RJ.,Johnston, CA. and Kelly,J.C1988. Kong Hong Kong, Periplus Editions, Alteration of North American streams by 802p. beaver. Bioscience, 38, 753-762. Madsen, T. and Shine, R 1999. Rainfall and rats: Naiman, RJ., Manning, T. and Johnston, CA. climatically-driven dynamics of a tropical 1991. Beaver population fluctuations and rodent population. Australian Journal of tropospheric methane emissions in boreal Ecology, 24, 80-89. wetlands. Biogeochemistry, 12, 1-15. Martinsen, G.D., Cushman, J.H and Whitham, Naiman, RJ., Melillo, J.M. and Hobbie, J.E. 1986. T.G. 1990. Impact of pocket gopher distur­ Ecosystem alteration of boreal forest streams bance on plant species diversity in a short­ by beaver (Castor canadell"is). Ecology, 67, grass prairie community. Oecoiogia, 83,132- 1254-1269. 138. Naiman, RJ., Pinay, G., Johnston, CA. and Martinsen, G.D., Driebe, E.M. and Whitham, Pastor, J. 1994. Beaver influences on the long­ T.G. 1998. Indirect interactions mediated by term biogeochemical characteristics of boreal changing plant chemistry: beaver browsing forest drainage networks. Ecology, 75, 905- benefits beetles. Ecology, 79, 192-200. 921. Maser, C, Trappe, J.M. and Nassbaum, RA. Noy-Meir, 1.1988. Dominant grasses replaced by 1978. Fungal-small mamma 1 interrelation­ ruderal forbs in a vole year in undergrazed ships with emphasis on Oregon coniferous mediterranean grasslands in Israel. Journal of forests. Ecology, 54, 799-809. Biogeography, 15,579-587. McDowell, D.M. and Naiman, RJ. 1986. Struc­ Palmer, E. 1886. Notes on a great visitation ofrats in ture and function of a benthic invertebrate the north and north-western plain country of stream community as influenced by beaver Queensland, in 1869 and 1870. Proceedings of (Castor canadensis). Oecologia, 68, 481-489. the Royal Society of Queensland, 1885, 193-198. McNaught,G.H 1994. The foraging behaviour of Pastor, J., Moen, Rand Cohen, Y. 1997. Spatial an Australian desert rodent, Notomys alexis heterogeneities, carrying capacity, and (Family Muridae). Sydney, Australia, feedbacks in animal-landscape interactions. University of Sydney, unpublished Honours Journal of Mammalogy, 78, 1040-1052. dissertation.

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Pinay, G. and Naiman, RI. 1991. Short-term Skinner, J.D. and Smithers, R.H.N. 1990. The hydrologic variations and nitrogen dynamics mammals of the southern African subregion. in beaver created meadows. Archiv fur Pretoria, South Africa, University of Pretoria, Hydrobiologie, 123, 187-205. 769p. Predavec, M. and Dickman, C.R 1994. Popula­ Smithers,C., McAlpine, D.,Colman, P. and Gray, tion dynamics and habitat use of the long­ M.1977. Island invertebrates. In: Smith, N., haired rat (Rattus villosissimus) in south­ ed.,. Lord Howe Island. Sydney, Australia, western Queensland. Wildlife Research, 21, The Australian Museum, 23-26. 1-10. Snodgrass, J.W. and Meffe, GK. 1998. Influence Recher, H.F. 1981. Nectar-feeding and its evolu­ of beavers on stream fish assemblages: effects tion among Australian vertebrates. In: Keast, of pond age and watershed position. A., ed., Ecological biogeography of Australia. 79, 928-942. The Hague, Netherlands, Dr W. Junk, 1637- Sokolov, V.E., Shilova, S.A. and Shchipanov, 1648. N.A. 1994. Peculiarities of small mammals Reddell, P., Spain, A.V. and Hopkins, M. 1997. populations as criteria for estimating anthro­ Dispersal of spores of mycorrhizal fungi in pogenic impacts on tropical ecosystems. scats of native mammals in tropical forests of International Journal of Ecology and north eastern Australia. Biotropica, 29, 184- Environmental Sciences, 20, 373-386. 192. Steadman, D. W. 1989. Extinction of birds in Reichman, O.J. and Price, M.V. 1993. Ecological eastern Polynesia: a review of the record, and aspects of heteromyid foraging. In: comparisons with other Pacific Island Genoways, H.H. and Brown, J.H., ed., groups. Journal of Archaeological Science, 16, Biology of the Heteromyidae. Provo, USA., 177-205. The American Society of Mammalogists, 539- Steinberger, Y. and Whitford, W.G. 1983. The 574. contribution of rodents to decomposition Reichman, O.J. and Smith, S.c. 1990. Burrows processes in a desert ecosystem. Journal of and burrowing behavior by mammals. Arid Environments, 6, 177-181. Current Mammalogy, 2, 197-244. Tardiff, S.B. and Stanford, J.A.199B. Grizzly bear Reichman, O.J. and Smith, S.C.1991. Responses digging: effects on subalpine meadow plants to simulated leaf and root herb ivory by a in relation to mineral nitrogen availability. biennial, Tragopogon dubius. Ecology, 72,116- Ecology, 79, 2219-2228. 124. Thompson, D. B., Brown, J.H. and Spencer, W.D. Ross, B.A., Tester, J.R and Breckenridge, W.J. 1991. Indirect facilitation of granivorous birds 1968. Ecology of mima-type mounds in north­ by desert rodents: experimental evidence western Minnesota. Ecology, 49, 172-177. from foraging patterns. Ecology, 72, 852-863. Schlosser, LJ. 1995. Dispersal, boundary Tory, M.K., May, T.W., Keane, P.J. and Bennett, processes, and trophic-level interactions in A.F. 1997. Mycophagy in small mammals: a streams adjacent to beaver ponds. Ecology, comparison of the occurrence and diversity of 76,908-925. hypogeal fungi in the diet of the long-nosed Sinclair, A.R.E. 1989. Population regulation in potoroo PotOtOllS tridactylus and the bush rat animals. In: Cherrett, J.M., ed., Ecological Rattus fuscipes from southwestern Victoria, concepts. Oxford, U.K., Blackwell Scientific Australia. Australian Journal of Ecology, 22, Publications, 197-241. 460--470. Singleton, G.R. and Petch, D.A.1994. A review of Twigg, G.!. 1978. The role of rodents in plague the biology and management of rodent pests dissemination: a worldwide review. in southeast Asia. Canberra, Australia, Mammal Review, 8, 77-110. Australian Centre for International Agricul­ Vander Wall, S.B. 1990. Food hoarding in tural Research, 6Sp. animals. Chicago, USA., University of Chicago Press, 44Sp.

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Vander Wall, S.B. 1997. Dispersal of singleleaf Wilde, S.A, Youngberg, CT. and Hovind, J.H. pifion pine (Pinus monophylla) by seed­ 1950. Changes in composition of ground caching rodents. Journal of Mammalogy, 78, water, soil fertility, and forest growth 181-19l. produced by the construction and removal of Van Tets, LG. 1997. Extraction of nutrients from beaver dams. Journal of Wildlife Manage­ Protea pollen by African rodents. Belgian ment, 14, 123-128. Journal of Zoology, 127, 59-65. Yair, A and Rutin, J. 1981. Some aspects of the Whicker, AD. and Detling, J.K. 1988. Ecological regional variation in the amount of available consequences of dog disturbances. sediment produced by isopods and porcu­ Bioscience, 38, 778-785. pi.nes, northern Negev, Israel. Earth Surface Whittaker,J.C, List, E., Tester,J.R. and Christian, Processes and Landforms,6, 221-234. D.P. 1991. Factors influencing meadow vole, Yavitt, J.B., Angell, L.L., Fahey, n., Cirmo, CP. Microtus pennsylvanicus, distribution in and Driscoll, CT. 1992. Methane fluxes, Minnesota. Canadian Field-Naturalist, lOS, concentrations, and production i.n two 403-405. Adirondack beaver impoundments. Limnol­ Wiens, D., Rourke, J.P., Casper, B.B., Rickard, ogy and Oceanography, 37, 1057-1066. E.A, La Pine, T.R., Peterson, CJ. and Channing, A 1983. Non-flying mammal pollination of southern African proteas; a non-coevolved system. Annals of the Missouri Botanical Gardens, 70, 1-31.

133 6. The Role of Rodents in Emerging Human Disease: Examples from the Hantaviruses and Arenaviruses

James N. Mills

Abstract

Becau se of the severity and the dramatic nature of the diseases they cause, the rodent-borne haemorrhagic fever viruses recently have received considerable attention from ecologi sts and he alth scientists. During the past five years, re searchers have identified at least 25 'new' hantaviruses and aren aviru ses, all associated with murid rodents, and coevolutionary theory suggests that many additional virus-host associations await discovery. Basic research on the ecology of hantavirus and arenavirus reservoir species is providing information of practical importance for reservoir control and disease prevention. Stu di es of reservoir geograph ic distribution and habitat associations help define potential disease­ endemic are as and more prec isely identify the spacial variation in rel ative ri sk to hu mans. Cross-sectional and longitudinal studies of reservoir populations help define mechanisms of viral transmission and identify the rel ationship between environment, rese rvoir popul ations, and human disease. Integrated results from a variety of reservoir studies can be combined with data from satellite images to provide models that can help scientists pred ict specific times and place s of increased ris k to human populations. Biologists and pest co ntrol specialists who work wi th reservoir speci es may be at increased risk of infection with ro dent-borne viruses unless appropriate safety guidelines are followed.

Keywords

Ro dents, infectious disease, rodent-borne disease, zoonoses, haemo rrhagic fever, arenavirus, hantavirus

134 The Role of Rodents in Emerging Human Disease

INTRODUCTION and the prevention of human disease; (4) discuss the implications of our increasing awareness of severe rodent-borne diseases s THE chapters in this volume and the understanding of their transmission amply illustrate, rodents-as patterns in terms of the safety measures A pests -are responsible for recommended for mammalogists and considerable economic loss, through vertebrate pest control specialists working in damage to crops, food stores and human disease-endemic areas; and (5) provide an property. Rodents, as carriers of diseases up-to-date list of the rodent-borne transmitted to humans (rodent-borne haemorrhagic fever viruses, their reservoir zoonoses), are also responsible for hosts, and the host distributions, so that considerable economic loss in terms of rodent biologists can assess their particular decreased worker productivity and health­ risk and take appropriate precautions. care costs. The most important negative impact of rodent-borne diseases, the loss of EMERGING INFECTIOUS DISEASES human health and lives, can be assigned no In 1967 the Surgeon General of the United price tag. States, William H. Stewart, declared that it Although the specific theme of this was time to "close the book on infectious chapter is the application of basic research diseases" and start paying more attention to on rodent biology and ecology toward chronic ailments. In 1998, Surgeon General public health goals, the goals of pest David Satcher, speaking to the United States management personnel and public health Congress, addressed the "continuing threat practitioners are similar. Whether to prevent of emerging infectious diseases", singling economic loss or to prevent disease, we seek out infectious disease as the number one to control rodent popuiations, prevent their killer worldwide. Even in the United States, access to human food and other products, according to Dr. Satcher, the death rate from prevent their access to our dwellings, and infectious diseases, excluding acquired minimise their contact with humans. immune deficiency syndrome (AIDS), rose Accomplishment of these objectives is by 22% between 1980 and 1992. What factors facilitated by a thorough understanding of are responsible for this stark difference in the biology and ecology of the target species. perspective coming from two surgeons In this chapter, I will (1) introduce the extent general? What are emerging infectious and severity of the human disease problem diseases? Why are they suddenly becoming caused by the rodent-borne haemorrhagic important? fever viruses; (2) use examples from the The term'emerging infectious disease' hantaviruses and arena viruses to illustrate applies to two groups of illnesses: those the broad nature and potential for expansion caused by previously unknown agents that of the rodent-borne disease problem; (3) are being recognised at an increasing rate, illustrate how a structured basic research such as AIDS, Lyme disease and hantavirus program can provide data that may assist in pulmonary syndrome, and those that the management of rodent host populations

135 Ecologically-based Rodent Management

represent the re-emergence of previously disease in humans. Nevertheless, the described diseases in drug-resistant or more potential number of agents is vast. The virulent forms, such as tuberculosis, malaria, disease agents that infect the house mouse and the illnesses due to Escherichia coli (Mus musculus) have been relatively well 0157:H7 (Institute of Medicine, 1992). The studied because of its use as a laboratory recent awareness of emerging infectious animaL Although it does not claim to be diseases is due to several factors. The comprehensive, a recent report (Committee development of antibiotic resistance is one. on Infectious Diseases of Mice and Rats, Others include rapid transportation, that 1991) provides a discussion of about 40 quickly brings victims of remotely acquired bacteria, viruses, and parasites that cause diseases into heavily populated cities, disease in M. musculus. These agents are improved diagnosis, and physician described mostly from populations of mice education. Another important factor is our that have not been outside of the relatively rapidly expanding population with the sterile environment of the laboratory for resulting incursion of humans into remote, many generations. Thus, the potential for natural habitats where previously unknown pathogen diversity may be much greater in diseases have existed for many years in populations of sylvatic species. It is certainly cycles involving wild-animal hosts. Some of not unreasonable to suspect that every these diseases of wild animals, the zoonotic species of wild rodent might harbour as diseases, can be transmitted to humans. many, if not more, potential disease agents. Rodents, because of their tremendous In the natural host, coevolution likely has diversity, social behaviour, opportunistic life lead to a relatively benign relationship history, high reproductive potential, between host and pathogen. The death or periodically high population densities, and severe illness of the host is rarely to the peridomestic affinities, are among the most evolutionary benefit of a parasite. When important natural reservoirs for zoonotic other animals (including humans) come into diseases. A review published in 1995 contact with rodents, the possibility of a described approximately 60 zoonotic cross-species infection occurs. The response diseases, or groups of associated diseases, of the human immune system to these novel for which rodents serve as hosts for the agents is unpredictable. In many cases the etiologic agent (Hugh-Jones et aL 1995). The pathogen will be cleared rapidly by the rodent-borne haemorrhagic fevers represent immune response and no disease occurs. one such group. Some pathogens may be pre-adapted to hide Because of our phylogenetic relatedness from the human immune system (e.g. to them, other mammals are the most likely human immunodeficiency virus). Others animals with which humans may be might elicit a strong immune response, but expected to share pathogens. Rodents are the that response might, itself, result in severe most diverse group of mammals, comprising pathology to the host. Such is the case with nearly half of the 4,600 species in the class. It the rodent-borne haemorrhagic fever is likely that only a small proportion of the viruses. organisms infecting rodents would cause

136 The Role of Rodents in Emerging Human Disease

THE RODENT-BoRNE cause the South American hemorrhagic HAEMORRHAGIC FEVERS fevers in the New World, and Lassa fever in the Old World. These diseases are the cause of The magnitude of the potential for human significant morbidity and mortality. There disease involving rodent-borne is may be 200,000 cases of HFRS each year in largely unknown. However, one group for Asia, primarily in China and Korea (McKee et which considerable progress has been made al. 1991). Lassa virus is responsible for as in recent years is the rodent-borne many as 300,000 human infections each year haemorrhagic fever viruses. An awareness in West Africa (McCormick et aL 1987). of the distribution of these viruses and their Secondly, each virus in both families is disease potential is becoming increasingly usually associated with a specific rodent host, important to rodent biologists and of the family Muridae, in which it establishes management personnel. In this chapter I will a chronic, p~rsistent infection that involves provide brief descriptions of the most the sporadic or persistent shedding of large important of the known the quantities of infectious virus into the recognised diseases caused by each, and environment in urine, faeces or saliva. These their general distributions. Additional characteristics of the infection are key to the details concerning their importance for transmission of the virus, both from rodent to wildlife biologists (Childs et al. 1995), rodent, and from rodent to human. Humans identification and distribution of the are believed to be infected most frequently reservoir species (Mills and Childs 1999), via the inhalation of infectiOll..<; aerosols of and epidemiology of the diseases (Peters et rodent excreta or secreta. Other likely but less al. 1996; Peters et al. 1999; Enria et al. 1999) frequent routes of infection include direct can be found in other sources. contact of broken skin or mucous membranes The rodent-borne viral haemorrhagic with contaminated rodent fluids or fomites, fevers are caused by two groups of viruses, ingestion of contaminated food, or the bite of the hantaviruses and the arena viruses. an infected rodent. Transmission within host Although they are both negative-stranded, populations may be by a variety of horizontal enveloped ribonucleic add (RNA) viruses, and vertical mechanisms, but evidence from the two groups are not closely related field studies indicates that horizontal taxonomically. The hantaviruses constitute transmission, and perhaps, specifically the genus Hantavirus, within the family aggressive encounters between adult male Bunyaviridae; the arenaviruses constitute the rodents, may be an important mechanism family Arenaviridae. Nevertheless, these two (Glass et al. 1988; Mills et al. 1992, 1997b). groups of viruses share several important characteristics. Both cause severe haemorrhagic fever in humans. The HAEMORRHAGIC FEVER WITH hantaviruses cause hantavirus pulmonary RENAL SYNDROME syndrome (HPS) in the New World and HFRS is the term applied collectively to a haemorrhagic fever with renal syndrome suite of diseases of varying severity caused (HFRS) in the Old World. The arenaviruses by hantaviruses in Asia and Europe. The

137 Ecologically-based Rodent Management

diseases are characterised by fever, chills, Epidemics are seasonal with an autumn myalgia, and varying degrees of peak, coinciding with the maximum haemorrhage and renal compromise with agricultural activity and probably maximum 1% to 15% mortality. The viruses are carried host population density. Cases occur by rodent hosts of the murid subfamilies predominantly among adult men in rural Murinae (Old World rats and mice) and habitats; many cases are among farmers, Arvicolinae (voles), and the distributions of forest workers and soldiers in the field the diseases generally coincide with the (McKee et a1. 1991; Peters et a1. 1999). distributions of the host species (Mills and Seoul virus, which is found nearly Childs 1999). A summary of the viruses, the worldwide in association with its known diseases, and approximate cosmopolitan host, the Norway rat (Rattus distribution of the reservoirs is provided norvegicus), is responsible for a relatively (Appendix 1). mild form of HFRS (Lee et a1. 1980). The prototype hantavirus, Hantaan Although Seoul virus has been detected in virus, gained worldwide attention during rats throughout most of the range of the the Korean conflict, when over 3,000 United species, most confirmed cases of HFRS Nations troops contracted a severe form of caused by Seoul virus have been restricted to HFRS, then referred to as Korean Korea, Russia, and China. Reasons for the haemorrhagic fever (KHF). However, the apparent lack of disease in other parts of the disease, which has variously been referred world are unknown, but may include to as epidemic hemorrhagic fever, inadeguate case finding. A search in one hemorrhagic nephrosonep hritis, Churilov's United States city revealed three suspected disease, and Songo fever, has been cases (Glass et a1. 1994). recognised for many years in Asia (McKee Dobrava virus, hosted by the yellow­ et a1. 1991; Peters et a1. 1999). A Chinese necked field mouse (Apodemus jlavicollis), is medical text from 960 AD may describe responsible for a severe form of HFRS in the compatible symptoms. The disease was Balkans. Dobrava virus may be associated noted by Soviet scientists as early as 1913, with A. agrarius in the Baltic region (Plyusnin and outbreaks continued to be described by et a1. 1997; Peters et a1. 1999). the Soviets as well as among Japanese Although several hantaviruses are hosted troops in Manchuria during the 1930s. The by arvicoline rodents in Asia and Europe, etiologic agent of KHF was not described only one is known to be associated with until the late 1970s when Ho Wang Lee human disease. Puumala virus, carried by isolated a virus from the lungs of the striped the bank vole (Clethrionomys glareolus), is the field mouse (Apodemus agrarius) captured on etiologic agent for a mild form of HFRS the banks of the Hantaan River near the called nephropathia epidemica (NE). NE is border between North and South Korea (Lee endemic to Scandinavia, western Europe, et a1. 1978). Currently, Hantaan virus is and European Russia. Several additional responsible for perhaps 200,000 cases of hantaviruses, some only recently HFRS each year, in China, Korea, and the discovered, are associated with murine and Russian Far East (McKee et a1. 1991). arvicoline rodents in Asia and Europe

138 The Role of Rodents in Emerging Human Disease

(Appendix 1). These viruses have not been been documented in Argentina, Chile, definitively associated with human disease, Paraguay, Uruguay, Brazil, and Bolivia, and but extensive studies are lacking. hantavirus or hantavirus antibody has been demonstrated in rodents from Peru, HANTAVIRUS PULMONARY SYNDROME Venezuela, Costa Rica and Mexico.

HPS is a New World hantavirus disease THE SOUTH AMERICAN HAEMORRHAGIC characterised by a flu-like prodrome involving FEVERS fever, myalgia, and malaise, which rapidly progresses to cardiopulmonary compromise The South American haemorrhagic fevers that may end in death in about 50% of cases in currently consist of four recognisLu diseases spite of aggressive hospital care. that are clinically similar. 1hey are In early 1993, only a single characterised by an insidious prodrome of autochthonous hantavirus was known from fever, malaise, muscle aches, and retroorbital the New World: Prospect Hill virus (Lee et headache, which may be followed by a1. 1982), which is associated with the hypotension, conjunctival injection, petechiae meadow vole, Microtus pennsylvanicus. It still on the throat, cllest, and axillary area, has not been associated with any human dizziness, and tremors. Severe cases disease. The seemingly sudden appearance demonstrate bleeding from gums and mucous of HPS in the spring of 1993 led to the membranes, shock, coma, and convulsions isolation of Sin Nombre virus (SNV; Elliott et (Enria et a1. 1999). Mortality may be 10% to a1. 1994) and its association with the deer 33%. With a single possible exception, the New mouse (Peromyscus maniculatus; Nichol et al. World arenaviruses for which the reservoir is 1993; Childs et al. 1994). Armed with a known are all associated with sigmodontine specific case definition and the molecular rodents (Appendix 2). and serologic tools and reagents necessary to The first arenaviral haemorrhagic fever to detect SNV, physicians and mammalogists be recognised and, to date, the best studied quickly discovered that HPS was a pan­ is Argentine haemorrhagic fever (AHF). The American disease, and that numerous disease was described in 1953 (Arribalzaga species of New World sigmodontine and 1955) and the etiologic agent, Junin virus, arvicoline rodents serve as hosts for a was described in 1958 (Parodi et al. 1958). plethora of hantaviruses. Currently, Several hundred to over a thousand cases of approximately 20 viruses have been AHF were confirmed each year on the described in association with about as many central Argentine Pampa from the discovery host species occurring from Canada to of the disease until the recent development Patagonia (Appendix 1 and Figure 1). About of a vaccine. half of these viruses are known human Cases are predominantly in adult men pathogens. All of those viruses responsible from rural areas, and epidemics are for HPS are hosted by rodents of the murid seasonal, occurring in the fall-coinciding subfamily Sigmodontinae. In addition to the with the harvest of principal crops (corn and United States and Canada, HPS has now soybeans) and maximum densities of the

139 Ecologically-based Rodent Management

Laguna Negra

Figure 1. Geographic locations of the principal currently recognised New World hantavlruses (after Mills and Chllds 1998).

140 The Role of Rodents in Emerging Human Disease

principal reservoir, the corn mouse (Calomys between November and January (Manzione musculinus). The introduction of an effective et a1. 1998). treatment using immune plasma decreased Finally, an arenaviral haemorrhagic fever the mortality from 15-30% to less than 1 %, caused by Sabia virus is known from a single and the recent use of a highly efficacious naturally acquired case near Sao PauIo, vaccine in the AHF-endemic area has Brazil, in 1990 (Coimbra et a1. 1994). Nothing resulted in a substantial reduction in the is known about the reservoir, or the potential numbers of reported cases (Maiztegui et a1. endemic area. 1998). Bolivian hemorrhagic fever (BHF), OLD WORLD ARENAVIRAL caused by Machupo virus, was described HAEMORRHAGIC FEVERS following several clusters of cases in 1959. Lassa fever, which is endemic to West The 2,000-3,000 cases of naturally acquired Africa, is the only recognised arenaviraI BHF have all been from the Beni Department haemorrhagic fever in the Old World. of north-western Bolivia. Sporadic cases Although the magnitude and geographic predominantly involve adult males from extent of the cases are poorly known, Lassa rural environments (Kilgore et a1. 1995), but virus probably causes 100,000 to 300,000 several large outbreaks have been associated cases and 5,000 deaths annually (McCormick with high densities of the reservoir, Calomys et a1. 1987). The virus has been isolated from callosus, in and around villages. Unlike its humans or rodents in Nigeria, Sierra Leone, congener, C. musculinus (which is strictly Guinea, and Liberia, but serologic surveys associated with grassland and agricultural show that Lassa or Lassa-like viruses are habitats), C. callosus can be found in close present in at least 10 other African countries association with human dwellings. An (Peters et a1. 1996; Appendix 1). Two or more outbreak in the town of San Joaqufn in 1963- species of the Mastomys natalensis species 1964 ended abruptly after two weeks of complex appear to serve as the reservoir for continuous trapping in homes, during which Lassa virus. At least eight species of 3,000 C. callosus were captured (Kuns 1965), Mastomys occur in Africa south of the and an ongoing program of rodent trapping Sahara, and their distribution and in villages in the BHF-endemic area may be, relationships are poorly understood at least in part, responsible for the scarcity of (Robbins and Van Der Straeten 1989). A 32- cases since 1974 (PAHO 1982). chromosome species, Mastomys huberti, has Venezuelan haemorrhagic fever, been described as being found in dwellings, described in 1989 (Salas et a1. 1991), is caused while a 38-chromosome species, Mastomys by Guanarito virus, an arenavirus hosted by erythroleucus, was found in the surrounding the cane mouse, Zygodontomys brevicauda. bush areas; both species were frequently Recognised cases have been restricted to infected with Lassa virus with a prevalence rural areas of southern Portuguesa and of about 30% (McCormick et a1. 1987). northern Barinas states. The highest risk of Lymphocytic choriomeningitis (LCM), disease is among adult male farm workers, caused by the arenavirus lymphocytic and the greatest numbers of cases occur

141 Ecologically-based Rodent Management

choriomeningitis virus (LCMV), is phylogenetic relationships among the associated with the house mouse rodent hosts (Bowen et a1. 1997; Mills et al. (M. musculus) throughout much of its 1997a; Schmaljohn and Hjelle 1997). This worldwide range. LCMV usually produces a pattern suggests that there was an ancestral syndrome of fever and myalgia (sometimes hantavirus and arenavirus associated with complicated by meningitis), which is rarely an ancestral mu rid rodent, before the serious, but infections during pregnancy subfamiliallineages diverged, over 20 have been associated with serious, even fatal million years ago, and that the viruses have complications to neonates (Peters et a1. 1996). been co-speciating and co-evolving along LCM is not considered a viral haemorrhagic with their rodent hosts since that time. fever and will not be discussed further. Implicitly, the maximum potential number Nevertheless the disease may be much more of hantaviruses and arenaviruses would be common than is diagnosed, and biologists one for each of the 143 of and pest control practitioners should be Arvicolinae, 529 species of Murinae, and 423 aware of the risk. Detailed reviews have species of Sigmodontinae (numbers of been published (Jahrling and Peters 1992; species from Musser and Carleton 1993). Peters et al. 1996; Enria et a1. 1999). Indeed, some species (e.g. Sigmodon alstoni, Sigmodon hispidus, Bolomys obscurus; PoTENTIAL VIRUS DIVERSITY Appendix 1) are known to host an arenavirus and a hantavirus. Nevertheless, it The rate of discovery of new haemorrhagic is unlikely that this maximum number of fever viruses has increased almost viral species will be found. Virus extinctions exponentially in recent years. In the are very likely to have occurred in some Americas, for instance, the number of murid lineages. For instance, some well­ known autochthonous hantaviruses has studied species (e.g. M. musculus, and increased from one, in 1993, to over 20 in C. musculinus) appear not to be associated 1998 (Figure 1). The rate of discovery of new with a hantavirus. It is also likely, however, hantaviruses and arenaviruses is not that some trans-species 'host jumping' may slowing, and theoretical considerations have occurred over time (Bowen et al. 1997; suggest that we may recognise only a small Morzunov et al. 1998), thus further proportion of the potential diversity. In increasing the potential diversity of viruses. general, each hantavirus and arenavirus appears to be associated with a single species of murid rodent host. The ECOLOGICAL STUDIES OF hantaviruses are associated with the RESERVOIR SPECIES Murinae, the Sigmodontinae, and the Just as control of pest populations for Arvicolinae; the arena viruses with the economic reasons depends upon an Murinae and the Sigmodontinae. Further­ understanding of the biology and ecology of more, the phylogenetic relationships among pest species, the control or prevention of the viruses (with some exceptions for the rodent-borne disease largely depends upon Arenaviridae) are generally mirrored by the understanding the biology and ecology of

142 The Role of Rodents in Emerging Human Disease

the host. Several basic research studies of the arenaviruses, to illustrate the value of basic ecology of virus reservoir species during the research toward the practical goal of past 12 years have provided information preventing and controlling human disease that potentially can be very useful for risk caused by rodent-borne pathogens. assessment and directed intervention in disease control. Defining disease-endemlc areas In an earlier paper (Mills and Childs One of the most basic pieces of information 1998) we reviewed some of these studies and for designing and directing a prevention outlined a series of directed goals toward the program for any disease is a precise understanding of reservoir ecology as it knowledge of the geographic area where a relates to human disease. After initial disease may occur (the potential endemic identification of the reservoir host, these area). Prevention efforts, such as public goals include (a) determining the potential education and reservoir control, must be disease-endemic area by identifying the directed throughout this area, while efforts geographic distribution of the host, and the outside the area represent wasted time and range of infection by the pathogen within the money. For any rodent-borne disease, the host distribution; (b) more precisely defining geographic distribution of the reservoir relative human risk by determining the defines the maximum potential endemic distribution of the host and pathogen among area of the disease. For many rodent species the distinct habitats on a regional scale; (c) in North America, the distributional ranges investigating potential mechanisms of are precisely known and are available in the transmission of the pathogen within host literature (Hall and Kelson 1959). Following populations; (d) conducting long-term the identification of the deer mouse as the prospective studies to elucidate the temporal reservoir for SNV (Childs et a1. 1994), patterns of infection in host populations; and scientists consulted the published (e) integrating data from reservoir studies distribution of P. maniculatus in North toward the development of a predictive America (Carleton 1989), and realised that model that would allow the early the potential endemic area for HPS caused identification of specific times, places, and by SNV could encompass most of the North conditions that may lead to increased rodent American continent. Education of populations, or increased infection in rodent physicians and increased surveillance soon populations that can cause elevated risk of confirmed that sporadic cases of HPS human disease. Although specifically occurred throughout the range of the deer directed at understanding rodent ecology in mouse in the United States. For other rodent relation to human disease, many of these species, in less extensively studied parts of goals (especially a, b, d, and e) are applicable the world, these distributions are poorly to studies of economic pests. In this section, defined. This is the case with several the above-listed goals are used as a important hantavirus and arenavirus structural basis, while providing examples reservoir species in South America. For from studies and theoretical problems example, the published distribution for specific to the hantaviruses and C. musculinlls, reservoir of Junin virus,

143

------. ------Ecologically-based Rodent Management

includes central and northern Argentina Populations of C. muscuIinus appear to be (Red ford and Eisenberg 1992). Nevertheless, continuous across the boundary of an during recent ecological investigations of expanding AHF-endemic area (Maiztegui et Laguna Negra virus on the Chaco of aL 1986). The spatially restricted but Paraguay (Yahnke et al. 1998), C. musculinus expanding distribution of Junfn virus within was frequently captured. A concerted effort, a continuous host population suggests as well as multi-disciplinary studies that recent introduction of Junfn virus or recent include health scientists, ecologists, and genetic changes in the virus, host, or both systematists, will be essential to define populations. Reasons for the lack of accurately the distributional ranges of coincidence in host and virus distributions important reservoir species. are likely to be diverse and involve host For some host-virus systems (e.g. genetics, geographiC boundaries, and local P. maniculatus and SNV), the host appears to extinctions in subpopulations. The be infected throughout its geographic range. elucidation of these factors, which will In other cases, the distribution of the virus require collaboration among ecologists, may include only a small portion of the virologists, geneticists, and systematists, will range of the host. In those cases, the contribute to our understanding of host­ identification of the geographic area in virus coevolution, the relationships among which the host and the pathogen both occur rodent species, and the properties of host provides a more precise definition of the systems that are required to support long­ potential disease-endemic area. While term maintenance of viral symbionts. On the C. musculinus occurs throughout central and practical side, these studies will allow the northern Argentina (and apparently western precise definition of the geographic areas in Paraguay), the AHF-endemic area occupies which humans are at risk for specific only a very limited region of the central diseases. Argentine Pampa (Maiztegui et al. 1986). Limited searches for Junin virus in Defining habitat associations C. musculinus populations outside the In addition to the large geographic patterns endemic area have been unsuccessful (Mills discussed above, host and pathogen et al. 1991). Calomys laucha also occurs from populations may vary on regional or local central Argentina through south-eastern scales. Many species of rodents demonstrate Bolivia, western Paraguay, and west-central distinct local habitat preferences, which may Brazil (Musser and Carleton 1993), yet have practical implications for disease Laguna Negra virus apparently occurs only transmission as well as reservoir on the Chaco of Paraguay Gohnson et aL management. The risk of human disease 1997, Mills and Childs 1998). Populations of may be more precisely defined by describing C. laucha in Paraguay and central Argentina differences in host distribution, population appear to be disjunct, and it is possible that densities, and prevalence of infection among the populations of C. laucha in Argentina are the distinct habitats represented in a local genetically distinct and will not support area. Even for species that are considered infection with Laguna Negra virus.

144 The Role of Rodents in Emerging Human Disease

opportunists or generalists, habitat studies working, or pursuing recreational activities may yield useful information. in various habitats. The deer mouse is considered a habitat The corn mouse, C. musculinus, has generalist and has been reported as historically been considered a denizen of occurring in nearly every dry-land habitat in corn fields, as its common name implies. North America (Burt and Grossenheider Junin virus has been thought to be 1976). A habitat study conducted in the transmitted to farmers working in those crop south-western United States confirmed that fields during the mechanised harvesting P. maniculatus occupied all of the major process (Carballal et al. 1988). Recently habitats represented (Mills et al. 1997b). however, habitat studies conducted in the Nevertheless, the prevalence of infection AHF-endemic area demonstrated a distinct with SNV varied significantly among preference by C. musculinus for the relatively habitats, being lowest at the altitudinal and stable, weedy border habitats (fence lines climatic extremes (desert and alpine tu.ndra) and roadsides) adjacent to the crop fields and highest at the middle altitude habitats (Figure 2). such as chaparral, grassland, and pmon­ These resul ts suggest a need to reconsider juniper woodland. The last habitat is where the possible places and mechanisms of most H PS cases in the south-western United transmission ofJwlin virus to humans. They States have occurred. Similar results were also suggest a specific intervention demonstrated by a study in Nevada and mechanism for dec reasing the incidence of California (Boone et al. 1998). Results such as AHF: periodically burning or cutting the these can be applied by p ublic health weedy border habitats to eliminate the scientists to define more precisely the preferred habitat for the reservoir host. relative risk of disease to humans living, Habitat studies conducted for other

100 ,------,

(f) 80 ~ :::J li Cll 0 60 a >- u c 40 Q) :::J 0- Q) Lt 20

0 2 3 4 5 6 7 8 9 10 11 12 Row Number Figure 2. Cumulative numbers of captures within each of 12 rows of traps of a 12 by 12 t rapping grid located in crop fields and adjacent roadside habitat in central Argentina, March 1998 to August 1990. Rows 1 and 2 are roadside habitat; rows 3 through 12 are in crop fields.

145 Ecologically-based Rodent Management

reservoir species might suggest similar important for testing predictions based on approaches. laboratory results.

Identifying mechanisms of Long-term studies transmission Perhaps the greatest amount of useful Basic field studies of reservoir demography information about reservoir populations and have provided important clues to the host-virus dynamics is achieved through the specific mechanisms of virus transmission use of longitudinal mark-recapture studies within host populations. Field studies with (Mills et al. 1999b). These studies involve the SNV (Mills et aL 1997b) and Black Creek establishment of multiple pennanent trapping Canal virus (Glass et aL 1998) have shown a plots, which are operated at defined intervals J-shaped curve of antibody prevalence with (usually monthly for disease studies) for host age. This pattern suggests that the several consecutive nights. Captured rodents young of infected females are born with are measured, sampled (e.g. blood and oral maternal antibody, which is lost within a swab), identified with a permanent mark or few weeks. Infection is then acquired by number, and released at the site of capture. In some horizontal mechanism later in life. subsequent trapping events, animals are Field data have also demonstrated a positive repeatedly captured, measured, and sampled. correlation between scars and the prevalence In this way, changes in community structure of infection (Glass et al. 1988). The more and population densities - as well as aggressive males may have a much higher individual growth rates, movement, prevalence of infection than females (Mills et reproductive condition, and infection status aL 1992; Mills et al. 1997b). Thus, an -are measured over time. Simultaneous important, specific mechanism of virus monitoring of environmental variables, such transfer within reservoir populations may be as temperature, rainfall, and growth and aggressive encounters among adult male cover by vegetation, provides clues animals. Laboratory studies have indicated concerning environmental changes that are that lymphocytic choriomeningitis and related to changes in reservoir populations Lassa viruses are maintained by vertical and, subsequently, changes in risk of human transmission mechanisms (Childs and Peters disease. 1993). However preliminary field data have Mark-recapture studies have helped to demonstrated an age-associated acquisition elucidate the temporal population dynamics of antibody in Mastomys populations in of host virus infection for the reservoirs of Guinea (A.R. Dembyand 10 others, Seoul and Prospect Hill viruses (Childs et aL unpublished data). This and similar 1987), Puumala virus (Niklasson et aL 1995), disparities between laboratory and field Junin virus (Mills et al. 1992), and SNV results for Junfn virus (Mills et aL 1992) may (Douglass et al. 1996; Mills et aL 1999a). The indicate that laboratory results may not cited studies and others in progress are always be applicable to natural field helping to elucidate the associations among conditions and that field studies are environmental conditions, rodent population densities, prevalence of infection

146 The Role of Rodents in Emerging Human Disease

in reservoir populations, and human disease Regular population cycles are not known risk. in rodents from the Northern Hemisphere The incidence of several rodent-borne tropics or anywhere in the Southern diseases is related to changes in density of Hemisphere. However, periodic, dramatic reservoir populations. Large year-to-year increases in the density of some rodent fluctuations in population density are populations do occur. These population characteristic of rodent populations of many irruptions are generally associated with species. Northern Hemisphere arvicolines, unusual climatic conditions, which result in such as the reservoir for Puumala virus abundant food supplies and ideal or (c. glareolus), undergo regular population prolonged conditions for reproduction. A cycles with a periodicity of 3-4 years, three-year longitudinal study of although the causes for the cycles are still C. musculinus in Argentina demonstrated a unclear (Krebs and Myers 1974; Niklasson et clear positive association between reservoir al. 1995). The year-to-year incidence of HFRS population density and the magnitude of caused by Puumala virus was shown to be AHF epidemics (Figure 3). correlated with the density of C. glareolus in The associated environmental conditions Russia and Scandinavia (Niklasson et al. were a relatively benign winter, followed by 1995). a wet summer, which apparently resulted in

8~------'200

Corn mouse density ... AHF cases 150 u.. :::c

1988-1990 Figure 3. Mean numbers of captures of Calomys musculinus per 100 trap nights (trap success) and numbers of cases of Argentine haemorrhagic fever (AHF) in central Argentina, March 1998 to August 1990. Reprinted with permission from Mills et a!. (1992).

147 Ecologically-based Rodent Management

unusually lush vegetation and abundant reservoir of Andes virus (Oligoryzomys food supplies (Mills et al. 1992). longicaudatus). Causes for the rodent The outbreak of HPS in the south-western irruption are unclear, but may be related to United States in 1993 was preceded by an El an unusually benign winter or to the Nifio Southern Oscillation (ENSO) event, flowering of a local species of bamboo, an which resulted in unusually warm winters event that may occur only every 40 years and and high rainfall in affected areas. It has been that provides abundant food for the hypothesised that the HPS outbreak was a granivorous 0. longicaudatus (Munia et al. direct result of increases in rodent 1996; Toro et al. 1998). Longitudinal studies populations and increases in prevalence of are currently being planned and initiated in SNV infection among high-density reservoir Chile and Argentina to follow the populations (Parmenter et al. 1993). Although environmental variables associated with intuitively attractive, no longitudinal changes in population density and infection monitoring of rodent populations and status in O. longicaudatus populations and infection status was in place in the area of the the relation of these variables to human outbreak, so this hypothesis cannot be disease. confirmed. Subsequent to the outbreak, An important key to being able to predict however, the Centers for Disease Control and the relative risk of diseases to humans is Prevention, in collaboration with several local understanding the conditions that lead to universities, initiated a series of longitudinal increased virus transmission and increased mark-recapture studies in the south-western prevalence of infection in host populations. United States (Mills et al. 1999b). These Infection appears to be associated with studies were in place to document behavioural events involving the environmental changes and associated interactions of individual rodents. Given the increases in reservoir populations in some pattern of horizontal transmission areas of the south-west in response to an demonstrated for many hantaviruses and ENSO event in 1997/1998 (T.L. Yates, K.D. arenaviruses, it might be predicted that Abbott, CH. Calisher and M.L. Morrison, increasing population densities should unpublished data). These increases in result in increased rodent-to-rodent contact reservoir populations have been associated and a higher prevalence of infection in host with increased numbers of HPS cases in the populations. In fact, however, investigators south-western United States. As of August are frequently unable to show a correlation 1998, there have been about 14 cases in the between rodent population density and four-state area of Arizona, Colorado, New prevalence of infection in rodent Mexico, and Utah, in comparison to 2, 2, and populations (Mills et al. 1992; Douglass et al. 4, for the same time periods in 1995, 1996, and 1996; Bond et al. 1998; Boone et al. 1998). The 1997, respectively (Centers for Disease problem with these approaches may be in Control and Prevention, unpublished data). seeking an instantaneous, linear relationship A recent outbreak of HPS in southern between density and antibody prevalence. Chile was apparently preceded by a In strongly seasonal environments, the dramatic increase in local populations of the effects of seasonal reproduction and

148 The Role of Rodents in Emerging Human Disease

horizontal transmission of virus may result spring (Niklasson et al. 1995; Mills et al. in an alternation of peaks in population 1999a). Research leading to an under­ density and prevalence of infection. In standing of the conditions that lead to Sweden, the population density of increased virus transmission and prevalence C. glareolus was highest in autumn of infection in host populations will improve (Niklasson et al. 1995), while the prevalence the ability of public health scientists and of antibody to Puumala virus in these modellers to predict increases in the risk of populations was highest in the spring, and human disease. correlated with vole population density the Predictive models of disease risk previous fall. A similar pattern of alternating peaks in density and antibody prevalence Perhaps the most important practical was observed for populations of Akodon application of studies of reservoir azarae infected with Pergamino virus in populations is to integrate the data from Argentina-rodent density was highest in these studies into a predictive model that the fall, antibody prevalence was highest in would allow public health practitioners to the spring (Schmidt et al. 1998). This pattern identify specific times and places where has also been observed for P. maniculatus conditions may pose a threat to the public populations infected with SNV in Colorado health. Such a model (Figure 4) assumes that (Calisher et al. 1999), and Peromyscus boylii the risk of human disease is related to rodent infected with a Sin Nombre-like virus in population density and prevalence of Arizona (Abbott et aL 1999). This delayed­ infection; rodent populations are affected by density-dependent prevalence of infection the quality of the biotic environment (e.g. may be typical for viruses transmitted by habitat quality and food supply); and the horizontal mechanisms in seasonal abiotic environment (e.g. edaphic factors environments. Autumn populations display and weather) influences rodent populations peak densities because of the culmination of both directly (e.g. direct effects of cold the spring/ summer reproductive effort; yet temperatures on survival) and indirectly the population consists primarily of young (through their effect on habitat quality and of the year that have not yet been infected, or food supply; Mills and Childs 1998). It is not are only recently infected and do not yet possible to have scientists continuously have detectable antibody. The cessation of measuring rodent populations and reproduction and over-winter mortality environmental variables wherever rodent­ results in a popUlation nadir in the spring, borne diseases occur. However, this may not but at that time the population consists be necessary. exclusively of older adults, which are more Recent studies using satellite imaging likely to be infected. In an autumn during and geographic information systems have which particularly high population levels demonstrated that remotely monitored occur, crowding would presumably lead to vegetation indices can help predict the more intraspecific contacts, more virus changing risk of human disease in sites as far transmission events, and a proportionally away as East Africa (Linthicum et al. 1987), higher antibody prevalence the following and the south-western United States (Boone

149 Ecologically-based Rodent Management

et a1. 1998; Cheek et a1. 1998). The success of The chance of contracting HPS by these mathematical models will depend handling New World sigmodontine rodents upon the accuracy of the parameter appears to be low. Nevertheless, the disease estimates, and the accuracy of the estimates, is sufficiently severe to warrant strict safety in turn, will depend upon data collected by measures for the general public (CDC 1993), investigators conducting basic field and and there is evidence that wildlife biologists laboratory research into the ecology and are at increased risk. Among the first 100 biology of the rodent reservoirs. cases of HPS in the United States, three were in wildlife biologists, and although a recent e.m,,, s,"". .. c,; ~" ~ serosurvey of over 1,000 American mammalogists demonstrated that the risk of infection with SNV appeared to be low (less ''''''''" ---... t than 1% ), risk increased with the munber of ~ t Insects Peromyscus that investigators had handled Rodent Populations .J during their careers (Armstrong et al. 1994). A study of Fimush mammalogists showed a t more striking relationship. Although no Human Disease mammalogist with less than five years of Figure 4. experience had antibody to Puumala virus, Simplified schematic model of relationships 40% of those who had trapped voles for among ecosystem components within an endemic area for a rodent-borne human disease. Remote more than 10 years had antibody (Bnunrner­ sensors (satellites) may be used for detecting Korvenkontio et al. 1982). These results changes in the ecosystem components which suggest that Puumala virus is more easily may lead to increased risk of disease. From Mills transmitted to humans than is SNV and Childs (1998). (although because of the high mortality of SNV, about half of those infected would not be available for sampling). Fortunately, THE RISK TO RODENT BIOLOGISTS neplu'opathia epidemica is a relatively mild In the United States, the sudden realisation disease. The murine- and sigmodontine­ that wild rodents are the reservoir for associated HFRS, HPS, Lassa fever, and potentially lethal disease has resulted in South American haemorrhagic fevers can be significant changes in the way many rodent much more severe and can lead to fatalities biologists conduct their research and in 15-50% of cases. Relatively simple safety teaching. Mammalogy classes avoid the precautions will minimise the risk of handling of sigmodontine rodents by infection to biologists and are highly students, the establishment of laboratory recommended for all researchers handling colonies from wild captured individuals of all known viral haemorrhagic fever reservoir known reservoir species is strictly species. controlled, and researchers who handle Standard precautions have been reservoir rodents are prudent to follow promulgated for investigators conducting safety guidelines. field studies, which may involve handling

150 The Role of Rodents in Emerging Human Disease

reservoir species for haemorrhagic fever Pest control workers should be alert to viruses. These guidelines, which were the possibility of inhalation of infectious developed during field studies of Junin virus aerosols when working in closed struchlres, in Argentina and the sigmodontine which may be infested by hantavirus or hantaviruses in the Americas, have been arenavirus reservoir species. The doors and published in English (Mills et aL 1995a,b) windows of such structures should be and in Spanish (Mills et al. 1998). Briefly, opened, and the building allowed to air out investigators should wear rubber gloves for at least 30 minutes before beginning when handling traps containing captured work. Clean-up of these structures should be animals, and the traps should be handled in conducted so as to avoid the creation of a manner that will prevent or minimise aerosols. Nesting materials or contaminated contact with rodent excretions or secretions areas should be wetted down with and inhalation of potentially infectious disinfectant, and floors should be mopped, aerosols of these materials. If captured not swept (CDC 1993). rodents are transported, the traps containing Hantavirus infection in laboratory rodent them should be placed in airtight plastic colonies has resulted in extensive outbreaks bags. These bags subsequently should be of human disease (Kulagin et al. 1962). opened and the rodents handled only in an Precautions when initiating laboratory isolated outdoor area by personnel wearing colonies from wild rodents that are known protective equipment (latex gloves, gowns reservoir species for hantaviruses or or overalls, respirators fitted with high­ arenaviruses should include quarantine as efficiency particulate air filters, and defined cohorts and serologic screening goggles). Handling rodents outdoors is upon capture, and again after 30 days (Mills preferred in order to take advantage of the et al. 1995b). disinfectant properties of natural ultraviolet The rodent-borne haemorrhagic fever light and the rapid dilution of aerosols in viruses are only one example of many open circulating air. Rodents should be zoonotic agents that are likely to be hosted anesthetised before handling to prevent by rodents. In this chapter they have been bites and production of aerosols, and the use used as an example to illustrate the potential of sharp instruments such as needles and diversity of rodent-borne disease agents. scalpels should be avoided when possible. Although the diseases they cause are Instruments, working surfaces, and traps dramatic, the risk to researchers can be should be decontaminated using an minimised by the adherence to relatively appropriate disinfectant (e.g. 5% hospital simple safety guidelines. Researchers strength Lysol, or lOO/" household bleach in studying these agents have amassed a large water), and contaminated gloves, disposable amount of new data during the last 5-6 gowns, and wastes should be autoclaved or years. Continued basic research into the burned. Rodent carcasses kept for museum ecology of these host-virus systems specimens can be decontaminated by fixing promises to provide useful models for in 10% formalin for at least 48 hours. understanding host-pathogen coevolution, transmission processes in natural

151 Ecologically-based Rodent Management

populations, and the relationship of Brummer-Korvenkontio, M., Henttonen, H. and environmental factors to host populations, Vaheri, A. 1982. Haemorrhagic fever with renal syndrome in Finland: ecology and virol­ pathogen transmission patterns, and human ogy of nephropathia epidemica. Scandana­ disease. vian Journal of Infectious Diseases, Suppl. 36, 88-91. ACKNOWLEDGMENTS Burt, W.H. and Grossenheider, R.P. 1976. A field guide to the mammals, North America north Thanks to Barbara Ellis for graphics, and to of Mexico, third edition. Boston, Houghton Barbara Ellis, Jamie Childs, Tom Ksiazek, Mifflin Company. and c.J. Peters for helpful comments on the Calisher, Sweeney, W., Mills, ].N., and Beaty, B.J. 1999. Natural history of Sin manuscript. Nombre virus in western Colorado. Emerg­ ing Infectious Diseases, 5, 126-134. REFERENCES Carballal, Videla, CM. and Merani, M.S. 1988. of Argentine haemor- Abbott, K., Ksiazek, T.G. and Mills, J.N. 1999. rhagic fever. European Journal of Epidemiol­ Long-term hantavirus persistence in rodent ogy,4,259-274. populations in central Arizona. Emerging Carleton, M.D. 1989. Systematics and evolution. Infectious Diseases, 5, 102-112. In: Kirkland, G.L. and Layne, J.N. ed., Armstrong, L.R., Khabbaz, R.P. and Childs, J.E. Advances in the study of PeromysClIs (Roden­ 1994. Occupational exposure to hantavirus in tia). Lubbock, Texas Tech University Press, 7- mammalogists and rodent workers. Ameri­ 14l. can Journal of Tropical Medicine and CDC (Centers for Disease Control and Preven­ Hygiene, 51, 94 (Abstract). tion) 1993. Hantavirus infection Arribalzaga, R.A. 1955. Una nueva enfermedad southwestern United States: interim recom­ epidemica a germen desconocido: hiperter­ mendations for risk reduction. Morbidity and mia nefrotoxica, leucopenic a y enantematica. Mortality Weekly Report, 42, 113. Dia Medico, 27, 1204-1210. Cheek, J., Bryan, R. and Glass, G. 1998. Bond,CW.,Irvine, B., Alterson, H.M., Van Horn, Geographic distribution of highrisk, HPS R. and Douglass, R.J. 1998. Longitudinal areas in the U.S. Southwest. The Fourth Inter­ incidence of hantavirus infection in deer national Conference on HFRS and Hantavi­ mice. Fourth International Conference on ruses, March 5-7,1998. Atlanta, Georgia, HFRS and Hantaviruses, March 5-71998, USA (Abstract). Atlanta, Georgia (Abstract). Childs, J.E., Glass, e.W. and Le Duc, Boone, J.D., Otteson, E.W., McGwire, K.C, J.W. 1987. Prospective seroepidemiology of Villard, P., Rowe, J.E. and St. Jeor, S.C 1998. hantaviruses and population dynamics of Ecology and demographics of hantavirus small mammal communities of Baltimore, infections in rodent populations in the Maryland. American Journal of Tropical Walker River basin of Nevada and California. Medicine and Hygiene, 37, 648-662. American Journal of Tropical Medicine and Childs, J.E., Ksiazek, T.G., Spiropoulou, CF., Hygiene, 58, 445-451. Krebs, J.W., Morzunov, 5., Maupin, e.0., Bowen, M.D., Peters, and Nichol, S.T. 1997. Rollin, P.E., Sarisky, J., R.E., Frey, Phylogenetic analysis of the Arenaviridae: J.K., Peters, CJ. and Nichol, S.T. 1994. patterns of virus evolution and evidence for Serologic and genetic identification of cospeciation between arenaviruses and their Peromyscus maniClllatus as the primary rodent rodent hosts. Molecular Phylogenetics and reservoir for a new hantavirus in the south­ Evolution, 8,301-316. western United States. Journal of Infectious Diseases, 169, 1271-1280.

152 The Role of Rodents in Emerging Human Disease

Childs, J.E., Mills, J.N. and Glass, G.E. 1995. Glass, G.E., Watson,AJ., Le Duc,J.W. and Rodentborne hemorrhagic fever viruses: a Childs, J.E. 1994. Domestic cases of hemor­ special risk for mammalogists? Journal of rhagic fever with renal syndrome in the Mammology, 76, 664-680. United States. Nephron, 68,48-51. Childs, J.E. and Peters, CJ.1993. Ecology and Hall, E.R and Kelson, KR 1959. The mammals of epidemiology of arenaviruses and their hosts. North America. New York, Ronald Press. In: 5alvato, MS., ed., The Arenaviridae. New Hugh-Jones, M.E., Hubbert, W.T. and Hagstad, York, Plenum Press, 331-384. H.V. 1995. Zoonoses: recognition, control, Coimbra, T.L.M., Nassar, E.5., Burattini, M.N., de and prevention. Ames, Iowa State University Souza, L.T.M., Ferreira, LB., Rocco, LM., Press, 369p. Travassos da Rosa, A.P., Vasconcelos, P.F.C., Institute of Medicine 1992. Emerging infections: Pinheiro, F.P., Le Duc, J.W., Rico Hesse, R, microbial threats to health in the United Gonziilez, J.P., Jahrling, P.B. and Tesh, RB. States. Washington D.C, National Academy 1994. New arena virus isolated in Brazil. Press, 294p. Lancet, 343,391-392. Jahrling, P.B. and Peters, CJ. 1992. Lymphocytic Committee on Infectious Diseases of Mice and choriomeningitis virus: a neglected pathogen Rats 1991. Infectious diseases of mice and of man. Archives of Pathology and Labora­ rats. Washington, D.C, National Academy tory Medicine, 116,486-488. Press, 397p. Johnson, AM., Bowen, M.D., Ksiazek, T.G., Douglass, RJ., Van Horn, R, Coffin, K and Williams, RJ., Bryan, RT., Mills, J.N., Peters, Zanto,S.N. 1996. Hantavirus in Montana deer CJ., and Nicho!, S.T. 1997. Laguna Negra mouse populations: preliminary results. virus associated with lIPS in western Journal of Wildlife Diseases, 32,527-530. Paraguay and Bolivia. Virology,238,115-127. EIliott, L.H., Ksiazek, T.G., RoIlin, P.E., Spiropou­ Kilgore, P.E., Peters, CJ., Mills, J.N., Rollin, P.E., Iou, CF., Morzunov, 5., Monroe, M., Armstrong, L., Khan, A.S. and Ksiazek, T.G. Goldsmith, CS., Humphrey, CD., Zaki, S.R, 1995. Prospects for the control of Bolivian Krebs, J.W., Maupin, G., Gage, K, Childs, J.E., hemorrhagic fever. Emerging Infectious Nichol, S.T. and Peters, Cr 1994. Isolation of Diseases, I, 97-99. the causative agent of hantavirus pulmonary Krebs, CJ. and Myers, J.H. 1974. Population syndrome. American Journal of Tropical cycles in small mammals. Advances in Medicine and Hygiene, 51,102-108. Ecological Research, 8, 267-399. Enria, DA, Bowen, M.D., Mills,J.N., Shieh, G.J., Kulagin, S.M., Fedorova, N.I. and Ketiladze, E.S. Bausch, D. and Peters, CJ. 1999. Arenavi­ 1962. Laboratory outbreak ofhaemorrhagic ruses. Chapter 111. In: Guerrant, RL., fever with renal syndrome. Journal of Micro­ Walker, D.H. and Weller, P.F. ed., Tropical biology, Epidemiology and Immunology infectious diseases, principles, pathogens, (RUSSian), 33,121-126. and practice. New York, W.B. Saunders, M.L. 1965. Epidemiology of Machupo 1191-1212. Kuns, virus infection. n. Ecological and control Glass, G.E., Childs, J.E., Korch, C.W. and Le Duc, studies ofhemorrhagic fever. American J.W. 1988. Association of intraspecific Journal of Tropical Medicine and Hygiene, wounding with hantaviral infection in wild 14,813-816. rats (Rattus norvegicus). Epidemiology and Lee, H.W., Lee, P.W. and Johnson, K.M. 1978. Infection, 101,459-472. Isolation of the etiologic agent of Korean Glass, G.E., Livingstone, W., Mills, IN., Hlady, hemorrhagic fever. Journal of Infectious W.J., Fine, J.B., Rollin, P.E., Ksiazek, T.G., Diseases, 137,298-308. Peters, Cj. and Childs,J.E.1998. Black Creek Lee, H.W., Park, D.H, Baek, L.J., Choi, KS., Canal virus infection in Sigmodon hispidus in Whang, Y.N. and Woo, M.S.1980. Korean southern Florida. American Journal of Tropi­ hemorrhagic fever patients in urban areas of cal Medicine and Hygiene, 59, 699-703. Seoul. Korean Journal of Virology, 10, 16.

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Lee, P.-W., Amyx, H.L, Cajdusek, D.C, Yanagi­ Mills,J.N. and Childs,J.E.1999. Rodent-borne hara, RT., Coldgaber, D. and Cibbs, CJ.1982. hemorrhagic fever viruses. In: Williams, E.S. New haemorrhagic fever with renal and Barker, 1. ed., Infectious diseases of wild syndrome related virus in indigenous wild mammals. Ames, Iowa State University Press rodents in United States. Lancet, 2,1405. (in press). Linthicum, KJ., Bailey, CL., Davies, F.C. and Mills, J.N., Childs, J.E., Ksiazek, T.G., Peters, Cr Tucker, C]. 1987. Detection of Rift Valley and Velleca, W.M. 1995a. Methods for fever viral activity in Kenya by satellite trapping and sampling small mammals for remote sensing imagery. Science, 235,1656- virologic testing. Atlanta, United States 1659. Department of Health and Human Services. Maiztegui, J.l, Briggiler, A, Enria, D. and Feuil­ Mills, J.N., Childs, lE., Ksiazek, T.C., Peters, C]. lade, M.R. 1986. Progressive extension of the and Velleca, W.M. 1998. Metodos para endemic area and changing incidence of trampeo y muestreo de pequenos mamfferos Argentine hemorrhagic fever. Medical Micro­ para estudios virol6gicos, biology and Immunology, 175, 149-152. OPS/HPS/HCT98.104 edn. Washington, Maiztegui, J.L, McKee, KT., Jr., Barrera Oro, J.C., D.C, Organizaci6n Panamericana de la Harrison, L.H., Cibbs, P.H., Feuillade, M.R, Salud. Enria, D.A., Briggiler, AM., Levis, S.C, Mills, J.N., Ellis, B.A, McKee, KT., Calder6n, Ambrosio, AM., Halsey, N.A and Peters, CJ. C.E., Maiztegui, J.I., Nelson, C.O., Ksiazek, 1998. Protective efficacy of a live attenuated T.G., Peters, CJ. and Childs,J.E.1992.Alongi­ vaccine against Argentine hemorrhagic fever. tudinal study ofJU11in virus activity in the Journal of Infectious Diseases, 177,277-283. rodent reservoir of Argentine hemorrhagic Manzione, N., Salas, RA, Paredes, H., Codoy, fever. American Joumal ofTropical Medicine 0., Rojas, L., Araoz, F., Fulhorst, CF., and Hygiene, 47,749-763. Ksiazek, T.C., Mills, ].N., Ellis, B.A., Peters, Mills, J.N., Ellis, B.A, McKee, K.T.J., Ksiazek, C}. and Tesh, RB.1998. Venezuelanhemor­ T.C., Oro, J.C., Maiztegui, J.L, Calderon, C.E., rhagic fever: clinical and epidemiological Peters, Cl. and Childs, J.E. 1991. Junin virus studies of 165 cases. Clinical Infectious activity in rodents from endemic and nonen­ Diseases, 26, 308-313. demic loci in central Argentina. American McCormick,J.B., Webb, P.A, Krebs,T.W., Journal of Tropical Medicine and Hygiene, Johnson, KM. and Smith, E.S. 1987. A 44,589-597. prospective study of the epidemiology and Mills, J.N., Ksiazek, T.C., Ellis, B.A., Rollin, P.E., ecology of Lassa Fever. Journal of Infectious Kichol, S.T., Yates, T.L, Cannon, W.L, Levy, Diseases, 155,437-444. CE., Engelthaler, D.M., Davis, T., Tanda, McKee, KT., Le Duc, J.W. and Peters, CJ.1991. D.T., Frampton, W., Nichols, CR., Peters, CJ. Hantaviruses. In: Belshe, RB. ed., Textbook of and Childs, rE. 1997b. Patterns of association human Virology. St. Louis, MO, Mosby Year with host and habitat: antibody reactive with Book,615-632. Sin Nombre virus in small mammals in the Mills, J.N., Bowen, M.D. and Nichol, S.T. 1997a. major biotic communities of the southwest­ African arenaviruses-coevolution between ern United States. American Journal of Tropi­ virus and murid host? Belgian Journal of cal Medicine and Hygiene, 56, 273-284. Zoology, 127,19-28. Mills, J.N., Ksiazek, Peters, C]. and Childs, Mills, ].N. and Childs, J.E. 1998. Ecologic studies J.E. 1999a. Long-term studies of hantavirus of rodent reservoirs: their relevance for reservoir populations in the southwestern human health. Emerging Infectious Diseases, United States: a synthesis. Emerging Infec­ 4,529-537. tious Diseases, 5, 135-142.

154 The Role of Rodents in Emerging Human Disease

Mills,J.N., Yates, T.L., Childs, J.E., Parmenter, and the implications for transmission of RR, Ksiazek, T.G., Rollin, P.E. and Peters, hantavirus-assodated adult respiratory CJ. 1995b. Guidelines for working with distress syndrome (HARDS) in the four rodents potentially infected with hantavirus. corners region. No. 41, University of New Journal of Mammology, 76, 716-722. Mexico. Sevilleta LTER Publication. Mills, J.N., Yates, T.L., Ksiazek, T.G., Peters, CJ. Parodi, AS., Greenway, D.J., Ruggiero, H.R, and Childs, J .E. 1999b. Long-term studies of Rivero, E., Frigerio, M.J., Mettler, N., Garzon, hantavirus reservoir populations in the F., Boxaca, M., de, G.L.B. and Nota, R 1958. southwestern United States: rationale, poten­ Sobre la etiologia del brote epidemica de tial, and methodology. Emerging Infectious Junin. Dia Medico, 30, 2300-2302. Lnseases,5,95-101. Peters, CJ., Buchmeier, M., Rollin, P.E. and Morzunov, S.P., Rowe, J.E., Ksiazek, T.G., Peters, Ksiazek, T.G. 1996. Arenaviruses. In: Fields, CL St Jeof, S.C, and Nichol, S.T. 1998. B.N., Knipe, D.M. and Howley, P.M. ed., Genetic analysis of the diversity and origin of Virology. Philadelphia, Lippincott-Raven, hantaviruses in Peromyscus leucopus mice in 1521-1551. North America. Journal of Virolology, 72, 57- Peters, CJ., Mills, J.N., Spiropoulou, CF., Zaki, 64. S.R and Rollin, P.E. 1999. Hantaviruses. Murua, R, Gonzales, L.E., Gonzalez, M. and Chapter 113. In: Guerrant, RL., Walker, D.H. Jofn', Y.C 1996. Efectos del florecimiento del and Weller, P.F. ed., Tropical infectious arbusto Chusquea quila Kunth (Poaceae) sobre diseases, principles, pathogens, and practice. la demograffa de poblaciones de roedores de New York, W.B. Saunders, 1217-1235. los bosques templados frios del sur Chileno. Plyusnin,A, Valpalahti, 0., Vasilenko, V., Boletin de la Sociedad de Biologia, Henttonen, H. and Vaheri, A 1997. Dobrava Concepci6n, Chile, 67, 37--42. hantavirus in Estonia: does the virus exist Musser, G.G. and Carleton, M.D. 1993. Family throughout Europe? Lancet, 349,1369. Muridae. In: Wilson, D.E. and Reeder, D.M. Redford, KH. and Eisenberg, J.F. 1992. ed., Mammal species of the world, a Mammals of the neotropics, the southern taxonomic and geographic reference, 2nd ed. cone. Chicago, The University of Chicago Washington, nc, Smithsonian Institution, Press. 501-755. Robbins, CB. and Van DerStraeten, E. 1989. Nichol, S.T., Spiropoulou, CF., Morzunov, Comments on the systematics of Mastomys Rollin, P.E., Ksiazek, T.G., Feldmann, H., Thomas 1915 with the description of a new Sanchez, A, Childs, lE., Zaki, S., and Peters, West African species. Senckenbergiana CJ. 1993. Genetic identification of a hantavi­ Biologica, 69, 114. rus associated with an outbreak of acute Salas, R, de Manzione, N., Tesh, RB., Rico Hesse, respiratory illness. Science, 262, 914-917. R, Shope, RE., Betancourt, A., Godoy, 0., Niklasson, B., Hornfeldt, B., Lundkvist, A, Bruzual, R, Pacheco, M.E., Ramos, B., Taibo, Bjorsten, S. and Le Duc, J. 1995. Temporal M.E., Tamayo, J.G., Jaimes, E., Vasquez, C, dynamics of Puumala virus antibody preva­ Araoz, F. and Querales, J. 1991. Venezuelan lence in voles and of nephropathia epidemica haemorrhagic fever a severe multisystem incidence in humans. American Journal of illness caused by a newly recognized arenavi­ Tropical Medicine and Hygiene, 53,134-140. rus. Lancet, 338,1033-1036. P AHO (Pan American Health Organization) Schmaljohn, CS. and Hjelle, B. 1997. Hantavi­ 1982. Bolivian hemorrhagic fever. Epidemio­ ruses: a global disease problem. Emerging logical Bulletin Pan American Health Organi­ Infectious Diseases, 3, 95-104. zation, 3, 1516. Schmidt, K, Ksiazek, T.G. and Mills, J.N. 1998. Parmenter, RR, Brunt, J.W., Moore, DJ. and Ecology and biologic characteristics of Ernest, S. 1993. The hantavirus epidemic in Argentine rodents with antibody to the southwest: rodent population dynamics

155 Ecologically-based Rodent Management

hantavirus. The Fourth International Confer­ Wilson, D.E. and Reeder D.M. 1993. Mammal ence on HFRS and Hantaviruses, March 5-7, species of the world, a taxonomic and 1998, Atlanta, Georgia, USA (Abstract). geographic reference. Washington, D.C., Toro, J., Vega, J.D., Khan, AS., Mills, J.N., Smithsonian Institution Press. Padula,P., Terry, W., Yadon,Z., Valderrama, Yahnke, c.J., Meserve, P.L., Ksiazek, T.e. and R, Ellis, B.A, Pavletic, c., Cerda, R, Zaki, S., Mills, J.N. 1998. Prevalence of hantavirus Wun-Ju, S., Meyer, R, Tapia, M., Mansilla, c., antibody in wild populations of Calomys Baro, M., Vergara, J.A., Concha, M., Calder6n, laucha in the central Paraguayan Chaco. The G., Enria, D., Peters, c.J. and Ksiazek, T.G. Fourth International Conference on HFRS 1998. An outbreak of hantavirus pulmonary and Hantaviruses, March 5-7,1998. Atlanta, syndrome, Chile, 1997. Emerging Infectious Georgia USA, (Abstract). Diseases, 4, 687-694.

156 Appendix 1. Currently recognised hantaviruses and the diseases they produce, the small mammal host species and host distribution. Nomenclature and distributions from Wilson and Reeder (1993).

Host subfamily Reservoir Virus Distribution of reservoir

Murinae Apodemus agrarius Hantaan HFRS C. Europe, S to Thrace, Caucasus, and Tien Mtns; Amur River through Korea, to E. Xizang and E. Yunnan, W. Sichuan, Fujiau , Taiwan . A. flavicollis DObrava England, Wales; NW Spain, France, Denmark, S. Scandinavia through European Russia, Italy, Balkans, Syria, Lebanon, Israel; ------II Netherlands Bandicota indica Thai not known Sri Lanka, India, Nepal, Burma, S. China, Taiwan, Thailand, Laos, Vietnam; introduced to Malay Peninsula and Java Rattus norvegicus Nearly worldwide Arvicolinae Clethrionomys glareolus Puumala not known France and Scandinavia to Lake Baikal, S to N Spain, N Italy, Balkans, W Turkey, N Kazakhstan; Britain, SW Ireland -4 C. rufocanus not-named E7 . ,. Scandinaviathrough Siberia to Kamchatka, S to Ural Mtns, Altai ~I ID=­ Mtns, Mongolia, Transbaikal, N. China, Korea, N. Japan ::a ~----_~I ____ o Lemmus sibericus Topografov not known Palearctic from White Sea, W Russia, to Chukotski Peninsula, iD NE Siberia, Kamchatka; Nearctic from W Alaska E to Baffin o Island, Hudson Bay, S in Rocky Mtns to C. British Columbia -::a o Microtus arvalis Spain through Europe to Black Sea and Kirov region, Russia; Cl.. ID ~ ______,Orkney Islands, Guernsey, and Yeu (France) = M. rossiaemeridionalis Tula not known From Finland E to Urals, S to Caucasus, thr()ugh Ukraine Eto -en Rumania, Bulgaria, S. Yugoslavia, N Greece, NW Turkey = 1'1'1 M. californicus IslaVista ___ ~~"","SW Oregon through California, USA, to N Baja California, Mexico 3 ID... M. fortis Khabarovsk not known Transbaikal and Amur Region S though Nei Mongol and E China 1!9, to lower Yangtze Valley and Fujian (IQ= M. ochrogaster Bloodland EC Alberta to S Manitoba, Canada S10 N Oklahoma and :z: c::: Lake ~ ______..., tr kansas E to C Tennessee and W Virginia, USA 3 I»= ~ en ID .... I» U1 en ...... ID Appendix 1. (Cont'd) Currently recognised hantaviruses and the diseases they produce, the small mammal host species and host distribution. rI1 .... n Nomenclature and distributions from Wilson and Reeder (1993). o ~ o OQ Host subfamily Reservoir Virus Disease Distribution of reservoir n' III Arvicolinae M. pennsy/vanicus Prospect Hill not known C Alaska to Labrador, Newfoundland, Prince Edwards Island; S in -

Host subfamily Reservoir Virus Disease Distribution of reservoir Murinae Arvicanthus sp. Ippy Not known S Mauritania, Senegal, Gambia, E through Sierra Leone, Ivory Coast, Ghana, Burkina Faso , Togo, Benin, Nigeria, Niger, :1 Chad , Sudan, Egypt, to Ethiopia; S through N Zaire , Uganda, S Burundi , Kenya, S Somalia & Tanzania, to E Zambia Mastomys natalensis Mopeia Not known S Africa as far north as Angola, S Zaire, and Tanzania Mastomys spp. Lassa Lassa fever Africa south of the Sahara Mus musculus Lymphocytic LCM Most of world in association with humans choriomeningitis Praomys sp. Mobala Not known C Nigeria through Cameroon Republic and Central African Republic, S. Sudan, Zaire, N Angola, Uganda, Rwanda, Kenya , south through E Tanzania to Nand E Zambia I -I Sigmodontinae Bolomys obscurus Oliveros Not known S Uruguay and EC Argentina ::r ~ 111 Calomys cal/osus Machupo Bolivian N Argentina , E Bolivia, W Paraguay, WC to EC Brazil ::u 0 hemorrhagic I ii" fever 0 . ------' C. cal/osus Latino Not known N Argentina, E Bolivia, W Paraguay, WC to EC Brazil ::u I =:=J -0 Cl. C. musculinus Junin Argentine Nand C Argentina, E Paraguay 111 hemorrhagic III= fever - Neacomys guianae Amapari Not known Guianas, S Venezuela, N Brazil :=J ...,= Neotoma albigula Whitewater Not known SE California to S Colorado to W Texas, USA, south to :I ...111 Arroyo Michoacan & W Hidalgo, Mexico '!S, Oryzomys buccinatus? Parana Not known E Paraguay and NE Argentina IrQ= O. albigularis Pichinde Not known N & W Venezuela, E Panama, Andes of Colombia & Ecuador :z: to N Peru =:I III Oryzomys sp.? Flexal Not known Not known = l1:li S. alstoni Pirital Not known NE Colombia, Nand E Venezuela, Guyana, Surinam, N Brazil iij' 111 .... III U1 III U) 111 ...., Appendix 2. (Cont'd) Currently recognised arenaviruses and the diseases they produce, small mammal host species and host distributions. n ""' Nomenclature and distributions from Wilson and Reeder (1 993 ). 2- ! C) IrQ Host subfamily Reservoir Virus Disease Distribution of reservoir t=j. I» Sigmodontinae S. hispidus Tam iami Not known SE USA, Mexico to C Panama, N Colombia and N Venezuela ~ 0- Zygodontomys brevicauda Guanarito Venezuelan S Costa Rica through Panama, Colombia, Venezuela, I» III hemorrhagic Guianas, to N Brazil; including Trinidad & Tobago and smaller 111 Cl. fever islands adjacent Panama & Venezuela ~ C) Unknown Sabia Unnamed (Human cases from Sao Paulo State, Brazil) Cl. 111 Non-rodent Artibeus (bats)? Tacaribe Not known (Isolates from bats on Trinidad and Tobago) -= I»== I»= IrQ 111 3 -=111 Section 2

Methods of Management 7. Rodenticides - Their Role in Rodent Pest Management in Tropical Agriculture

Alan P. Buckle

Abstract

Rodents are serious pests of tropical agriculture. Most crops are attacked, particularly those grown for food by smallholders in the tropics. Globally, principal pest species include Sigmodon hispidus, Arvicanthis ni/oticus, Mastomys nata/ensis, Meriones spp., Bandicota spp., Rattus argentiventer and Microtus spp. Crop protection specialists usually recommend control programs based on integrated pest management (IPM) technologies involving the use of rodenticides in combination with various techniques of habitat manipulation. However, few proper IPM schemes have been developed and implemented on a wide-scale and long-term basis. Rodenticides are much used by growers. Acute compounds, such as zinc phosph ide, are popular with smallholders because they are ch eap but are rarely very effect ive. First generation anticoagulants (e.g. warfarin) are potentially effective, but only where their use is well managed because of the need for freq uent applications of bait in rel atively large quantities. Baits containing the potent second generation compounds (e .g. brodifacoum and flocoumafen) are likely to be the most effective because of the small amounts of bait and labour needed when they are applied, but questions remain about their potential to have adverse environmental impacts in agro-ecosystems. Rod enticides will be im portant in rod ent pest manage ment in tropical agriculture for t he foreseeable future but much remains to be done to optimise their use. Improved decision-making methods, the wider assessment of non-target hazard, synergies between rodenticides and other rat management technologies and more sustainab le exten sion programs are all areas req uiring development. Unfortun ately, few agenci es now seem willing to expend effort on such research, although novel techniques to replace rodenticides still seem a long way off.

Keywords:

Rodents, rodenticides, rodent control, anticoagulants, resistance, integrated pest management, rice , sugar cane, oil palm , tropical crops

163 Ecologically-based Rodent Management

THE RODENT PESTS OF pattern of damage is one in which certain TROPICAL AGRICULTURE overriding climatological or demographic phenomena create specific conditions for rodent populations to reach extraordinary, EW TROPICAL crops are free from or plague, levels. At such times crops may be rodent attack. Among common totally devastated. The development of very F crops, perhaps only mature stands high populations of Mastomys natalensis after of rubber (Hevea brasiliensis) and some crops unseasonal rains in East African crop lands is grown for fibre, such as sisal (Agave sisalana), an example of this type of episode are immune from damage by these (Mwanjabe and Leirs 1997). Another is the ubiquitous pests. Crops grown in tropical very high populations of rodents that occur agro-ecosystems for food, such as cereals in some parts of Southeast Asia coincident (rice, wheat, maize, millet, barley and with the irregular flowering of bamboo sorghum), roots, fruit, legumes and forests (Singleton and Petch 1994). vegetables are particularly susceptible to The number of tropical rodent pest rodent depredation. Also, crops cultivated species involved is very large and appears to on an industrial scale in plantations, such as present a bewildering challenge to those sugarcane, coconut, cocoa and oil palm are attempting to develop sound management commonly attacked. The extent of losses in strategies. However, global rodent pest these agro-ecosystems is highly variable. problems were classified following work by Two damage models may be recognised. In the Expert Consultation of the Organisation the first, if left unchecked by some form of for Economic Cooperation and Develop­ management practice, rodent populations ment, Food and Agriculture Organization reach the carrying capacity of the standing and the World Health Organisation into crop they infest. This is frequently very high seven key components of global significance due to the abundant rodent food and cover (Drummond 1978) and this still provides a that the crops offer. Economically significant useful framework. Six of these problems are losses in the region of 5-25% are often to be found in tropical and sub-tropical, inflicted (Wood 1994). This type of damage food-crop, smallholder agriculture (Table 1). may be overlooked both by farmers and crop The seventh is the cosmopolitan problem of protection specialists and becomes apparent rodent damage to stored products, mainly only when carefully planned damage by Rattus norvegicus and Rattus rattus. assessment programs are implemented over The purpose of this chapter is to review large crop areas (e.g. Posamentier 1989; some of the learnings obtained from a Salvioni 1991). Within this model, patterns number of research and development of the supply of irrigation water and projects aimed at introducing management subsequent harvesting sometimes strategies for these pests of tropical concentrate rodent populations from a wide agriculture. The majority of these projects area into relatively small tracts of crop land were broadly based investigations including at the end of the season and some farmers the assessment of damage levels, studies of then suffer very heavy losses. The second rodent biology and the development and

164 Th e Role of Rodenticides

implementation of rodent management wide range of nationa l and international methods. In rela tion to the latter, many agencies very few schemes currentl y operate studies were based on the use of to fulfil these criteria (Leirs 1997). rodenticides, although a number of All too often those who conduct rodent subsidiary techniques were frequently control programs pay only li p service to rPM incorporated to p rovide elements of ideas and rely almost solely on rodenti cides. integrated pest management (rPM). There are many reasons for this but paramount is the fact that, although potentially effective, many of the techniques INTEGRATED PEST MANAGEMENT AND that co mp lement rodenticides in rPM are THE USE OF RODENTICIDES labour-intensive and their impact is not Few who devise and evaluate rodent immediately obvious to those who must management strategies fail to advocate invest scarce resources to implement them; integrated approaches as the most reliable, in effect they do not satisfy Singleton'S long-term solutions to rodent problems (see criteria. The control of rice-field rats in Richards and Buckle 1987; Mwanjabe and Southeast Asia through habitat Leirs 1997, among many others). A review of manipulation is a case in point. the principles of rodent rPM was recently [The following is based mainly on work provided by Singleton (1997). This analysis with Rattus argentiventer (Lam 1978, 1990) indicates that strong rPM programs must be but may be relevant to other rice rat species environmentally sound, cost-effective, in Asia, such as Rattus flavipectus, Rattus losea sustainable, capable of application over and Rattus rattus l1lindanensis, and also large areas and recognisably advantageous, elsewhere.] Some of the conditions of rice both for growers who implement them and cultivation that exacerbate rat problems politicians who support and fund them. have been long understood (Buckle et However, after many years of work by a a1.1985; Lam 1990; Leung et aI., Chapter 14).

Table 1. The world's major rodent pests of agriculture (from Drummond 1978) *.

Rodent pest species involved Area affected Crops attacked

Sigmodon hispidus Ce ntral and Latin America ri ce, sugar, cotton Arvicanthis niloticus, su b-Saharan Africa food crops Mastomys (Praomys) natalensis Meriones spp. North Africa , Middle East cereals Bandicota bengalensis Indian sub-continent , sugar, cereals, food crops Southeast Asi a Rattus argentiventer Southeast Asia rice (oil palm) Rattus rattus, Rattus norvegicus, Oceanic islands coconuts, food crops Rattus exulans * For various reasons certain regions and pests were omitted in th is analysis. However. a com pl ete list of global rodent pest problems of ope n-field agriculture woul d certainly also include those caused by Rattus fiavipectus in southern China and Indochi na, Microtus spp. ac ross the Holarctic and Mus musculus in mai nland Australia.

165 Ecologically-based Rodent Management

Rats choose to build nests for breeding Acute rodenticides almost exclusively in rice-field bunds that are more than about 300 mm wide and 150 The fast-acting, acute rodenticides are still mm above water level. They breed primarily much used by tropical smallholders, during the reproductive stages of the rice although zinc phosphide is now the only plants and asynchronous planting allows specific rodenticide in this class that remains prolonged breeding by permitting rats to widely available. In the absence of move from harvested fields to others nearby alternatives, growers frequently apply as where rice is still at an appropriate stage for rodenticides other compounds with high reproduction. Weedy rice fields (Drost and mammalian toxicities (e.g. certain organo­ Moody 1982), as well as overgrown, chlorine and organo-phosphide insecticides) uncultivated areas either in or nearby rice contrary to the regulatory approval of the fields provide refugia for rats and compounds concerned. supplementary sources of food. Habitat The benefits of the acute compounds manipulation measures to overcome these mainly lie in their ready availability, low problems are obvious; a reduction in bund cost and rapid action. They are favoured by size, synchronous sowing/transplanting tropical farmers because their effects are and clean rice field cultivation practices, but apparent almost immediately after all are almost impossible to implement on a application. To be set against these wide scale because of other, overriding advantages are their disadvantages. They agronomic and socioeconomic factors. are sold as concentrates and before use must In contrast, rodenticides have a high be mixed with bait bases, usually cereals, to potential to contribute useful elements the desired concentrations. Tropical within rodent IPM strategies (Singleton smallholders are ill-equipped to do this 1997). Of particular importance is their safely and accurately and often, cereals of relatively low cost, both in terms of the price sufficiently high quality to provide attractive of baits in relation to the value of the crop to baits are scarce. Acute rodenticides are sold be protected and the labour needed to apply as powder concentrates and are particularly them. Therefore, rodenticides seem likely to prone to adulteration during manufacture remain central to rodent management and distribution. These characteristics result strategies for some time to come. in baits of very dubious quality. Even when they are properly made, acute rodenticide RODENTICIDES AND THEIR USE IN baits have the drawback of eliciting 'bait TROPICAL AGRICULTURE shyness'. This is where the onset of The types of rodenticides, the techniques symptoms of poisoning in sub-lethally used in their application and some of their dosed animals is so rapid that rodents are advantages and disadvantages were able to relate them to the novel food (the reviewed recently in a general account by bait) which has caused them. Bait shy Buckle (1994). A discussion of them is given rodents are those that will avoid contact here in relation, particularly, to their with the poisoned bait when it is applied in application in tropical agriculture. future. The likelihood of this occurring may

166 The Role of Rodenlicides

be reduced, but not eliminated, by the use of (1987) used manufactured zinc phosphide 'pre-baiting'. In this, the bait base later to be bait cakes in a successful large-scale rodent used in the poisoning campaign is first control campaign in cereals in Bangladesh. offered without poison for several days. The recommended concentration of zinc Rodents slowly overcome their suspicion of phosphide for field use varies from 1% to the novel food (neophobia) and eventually 5%. Zinc baits are generally unpalatable to feed consistently. Only then is the acute rodents and a compromise between the poison introduced. The use of pre-baiting to active ingredient concentration used and the overcome neophobia and reduce bait quantity of bait likely to be eaten must be shyness is time-consuming, poorly reached with the objective of administering understood by smallholders and rarely the maximum quantity of the active practised. ingredient. The preferred concentration is Probably the best results that can be probably 2-2.5% (MAFF 1976). The bait anticipated with the use of zinc phosphide bases used are locally available cereals. They baits, under practical conditions, were may be soaked overnight in water before the demonstrated by Rennison (1976) on farms zinc phosphide is added and this is thought in the United Kingdom. Zinc phosphide to enhance uptake (MAFF 1976) but reduces baits, at 2.5% concentration, were applied by the stability of bait. The baits are placed in trained and experienced rodent control small piles of 20-50 g at intervals of 5-20 m operators. Pre-treatment population on bunds in rice fields or, in other crops, assessment was done by census baiting and wherever rodents are active (Lam 1977; this provided a form of pre-baiting. An Mwanjabe and Leirs 1997). The rate of average level of control of 84% of R. application may be varied, both by the Ilorvegicus was achieved. Few good studies weight of bait used and the distance between have been conducted on the efficacy of acute bait points, in order to accommodate rodenticides in tropical agriculture and it is different pest infestation densities. unlikely that this level of success is ever Undoubtedly, a few days of pre-baiting with achieved. Most studies have suffered from a the cereal to be used later as the carrier for lack of replication, plot sizes that are too the active ingredient will enhance small and with insufficient separation effectiveness. between plots different treatments, poor (or no) statistical analysis and, often, a First generation anticoagulants lack of detailed explanation of the methods The archetypal first generation employed (see Chia et a1. 1990 for a anticoagulant rodenticide is warfarin. After discussion of field trial methodology). These its introduction in the early 1950s, a number failings are common among field studies of of other compounds were developed, rodenticides and it is not surprising, including pival, coumachlor, coumatetralyl, therefore, that highly variable results have and the indandiones diphacinone and been obtained (West et al. 1975; Lam 1977; chlorophacinone. However, with the Mathur 1997). In spite of the shortcomings of possible exception of coumatetralyl (e.g. zinc phosphide, Adhikarya and Posamentier Greaves and Ayres 1969; Buckle et a1. 1982),

167 Ecologically-based Ro dent Management

there is littl e evidence that these compolUlds granaries) the virtual elimina ti on of Norway differ m uch from each other in their efficacy. rat infesta ti ons was possible for the first All these compounds are most potent when time. However, other species are less administered in small daily doses. However, susceptible to it and among the least their most ad vantageous common feature is susceptible are some importan t pests of their chronic mode of action, which means tropi cal agriculture, such as Mn stol'l1Ys that bait shyness does not arise. These novel natnlensis, Me riones spp., Bnndicota spp ., features required the developmen t of a R. argentiventer an d R. rattus. Greaves (1 985) different means of quan tifying the potency gave da ta for 'natural resistance' to warfarin of the first generation an ticoagulants. This for 11 rodent species, of which l"line were was done in terms of the number of days of pests of agriculture (Table 2). This shows consumpti on of field strength baits required that for only three species (R . norvegicu s, to obtain a given mortality percen tile and Sigmodon hispidus and Arvica nthis niloticus) is resulted in the expression 'lethal feeding the LFP99 less than 14 days. period' (LFP). It is a reasonable conclusion that warfarin Warfarin was first developed for use (and the other similar compOlUlds) is against the Norway rat and it is particularly unlikely to be as effec ti ve when used in effec ti ve against that species (Table 2). Used agriculture as it is in commensal situations if against Norway rats in com mensal more than two weeks of continuous no­ situations and in animal husband ry choice feeding is required to deliver an (pig/ poultry sheds, d airies, beef-rearing LFP99· units) and other fa rm buildings (mills and

Table 2. 'Natural resistance' to warfarin of key rodent pest species as indicated by the number of days of no-choice feeding on 250 ppm warfarin baits to achieve lethal feeding period (LFP)50 and LFP99 percentiles (from Greaves 1985)

Rodent species Feeding period (days)

LFPso LFPgg Nesokia indica 1.9 3797. 0 Acomys caharinus 5.4 239.3 Mus musculus 4.8 29.5 Mastomys natalensis 4.8 26.0 Bandicota indica 1.4 25.0 Rattus rattus 3.6 21.0 Tatera indica 5.8 19.2 Rattus argentiventer 3.2 15.5 Sigmodon hispidus 3.7 8 .1 Arvicanthis niloticus 3.8 6.0 Rattus norvegicus 1.7 5.8

168 The Role of Rodenticides

Even against susceptible species, the placements, normally 20%. An important effective use of the first generation advantage of this system was that the use of anticoagulants requires that baits are wax blocks removed the need for fabricated available for consumption by rodents, more bait stations to protect the bait. or less continuously, for several weeks. All applications of rodenticides in Baiting programs were developed, primarily agriculture are more cost effective, and their in the Philippines, for use in tropical effectiveness more long lasting, when large agriculture with this requirement in mind crop areas are treated simultaneously. Thus, (Hoque and Olvida 1987; Sumangil1990). if large numbers of smallholders are Baiting stations were put out at a density of mobilised to conduct baiting campaigns, the two to five per hectare and supplied with effort required by each farmer is minimised, about 150 g of bait. The bait used was the quantities of bait used are small and the generally whole or broken rice grains treated duration of baiting is short (e.g. Buckle with anticoagulant powder concentrates and 1988). However, the sustained baiting oil as a sticker. The bait stations were method can be employed successfully by checked at frequent intervals (at least single smallholders in small plots, but weekly) and the bait replenished. More bait almost continuous baiting may be needed. and baiting stations were put out at sites This creates a 'sink' into which are drawn where complete takes were encountered and rodents from a wide area. Clearly, this baiting continued until takes of bait ceased benefits more farmers than the one or the crop was harvested. This technique conducting baiting and may not be came to be called 'sustained baiting' and its sustainable because its cost falls so development, extension to smallholder inequitably, both in terms of effort and groups and practical application on a money. Using such a system, Sumangil nationwide basis is chronicled in the reports (1990) used 44 kg of bait per treated hectare of the Rodent Research Centre, at Los Banos, on small farms, during a 12-week rice through the mid and late 1970s. This growing season, where rats were numerous. technique remains the only practicable method of application of loose baits containing the warfarin-like compounds in Second generation anticoagulants tropical agriculture. Resistance to the first generation The sustained baiting technique was anticoagulants led to the development of a adapted for use with wax-block baits further series of compounds of greater containing warfarin in oil palm plantations potency that were effective against resistant in Malaysia (Wood 1969). In this practice, a rodents. These include difenacoum, single 15 g block was placed in the weeded bromadiolone, brodifacourn, flocournafen circles of each palm. The baits were checked and difethialone. A third generation of at four-day intervals and replenished where compounds is occasionally referred to in they were taken. Baiting continued until the some publications. The last three requirement to replenish baits declined to a compounds differ from the first two in being predetermined percentage of bait more potent but none differs sufficiently

169 Ecologically-based Rodent Management

from any other to be considered in a class active ingredient that enters the apart. environment. The use of this technique, Early tests of brodifacoum focused on with wax-block baits containing one of the the objective of obtaining a degree of potent second generation anticoagulants, effectiveness against resistant animals that provides the most practical and cost­ was equivalent to that of warfarin when effective method of rodent control using used against fully susceptible ones. Very rodenticides currently available. low concentrations in baits (5 to 20 ppm) fed over several days were sufficient to achieve Anticoagulant resistance this objective (Redfem et al. 1976). \ However, it was soon observed that 50 ppm Resistance to anticoagulants is uncommon in brodifacoum baits were effective at tropical agriculture. There seems to be a providing very high levels of kilL against relationship between the time taken for both susceptible and resistant rodents, anticoagulant resistance to develop and the when rodents fed for only one day on small degree of selection pressure applied (i.e. the amounts of bait (see, for example, Buckle et frequency of use of the anticoagulants and al. 1982, for R. argentiventer). However this the proportion of the pest population benefit could not be readily realised as a exposed). In the tropics, only in oil palm practical advantage because the delayed plantations in Malaysia has this pressure effects of brodifacoum, as an anticoagulant, been such that widespread resistance has meant that given free access to bait, rodents developed to the first generation consume much more before they die than anticoagulants (Lam 1984; Wood and Chung actually needed to kill them. This resulted in 1990). In the United Kingdom, where the development of a technique called resistance has arguably reached its current 'pulsed baiting' in which relatively small extreme, nowhere are resistant rodent quantities of bait are put out at intervals populations impossible to control with between which there is a period in which available techniques, although there is a cost bait is virtually absent; allowing rodents in terms of the need to use the more potent that have consumed a lethal dose to die compounds, sometimes for periods longer before a subsequent application (see Buckle than normal (Greaves 1994) and in greater et al. 1984; Dubock 1984). The principle quantities. This perspective is not intended . practical benefit to arise from the use of to generate complacency. When pulsed baiting in agriculture is that the anticoagulants are used in tropical quantity of bait used is substantially agriculture it is essential to establish reduced. Successful campaigns have been susceptibility baselines and to monitor pest conducted in which application rates as low populations for subsequent changes in as one to two kilograms of bait per hectare susceptibility. Published guidelines set out have been used (Buckle 1988). To the how this should be done (EPPO 1995). These advantage of a reduction in the cost of bait baseline studies would also provide and labour required to transport and apply preliminary performance data on active it is added a reduction in the amount of ingredients and the baits that contain them.

170 The Role of Rodenticides

Decision-making remains to be done in the majority of crops on the relationships between rodent Rodent pest problems in tropical crops are population density, damage levels and crop rarely uniform, either in time or space. If a losses. An aid to decision-making in this rodenticide (or any other control measure) is context is the establishment of the economic to be used cost-effectively, a process is injury level, determined as follows (Dolbeer required by which to decide when and 1981): where to apply it. Frequently in tropical T% = 100(Y/bX) (1) smallholder agriculture this decision is where made on the basis of subjective judgement, T = economic injury level; either by individuals or small groups of Y = cost of control; growers, and is often made too late. It is well X = value of potential crop loss; established that cost-effective rodent b = constant representing the proportion management is most likely when efforts are of potential loss saved by control. co-ordinated over substantial crop areas. Khoo (1980) proposed a systematic Surveillance and forecasting systems have damage sampling scheme for use in oil palm been devised to assist decision-makers in plantations in which the percentage of palms these circumstances, based either on with fresh damage to fruit bunches provided information on pest density or on a criterion dictating the need for the meteorological observations. application of pulsed baiting with second Surveillance systems based on pest generation anticoagulants. Buckle (1988) density have been worked out for sugarcane, conducted large-scale pilot trials of an oil palm and rice. In sugarcane, the 'Hawaii integrated rice rat management scheme trapping index' (Hampson 1984) is widely which involved farmers undertaking used to determine the need for rodenticide frequent monitoring of the percentage of rice applications. Snap-trap lines are set and hills with rat damage as a trigger for the rodent population density, expressed as an need for control action. This parameter is index of trapping success, is used as a related to, and more easily assessed than, the decision-making tool. The pitfalls of this percentage of rat-damaged rice tillers. The technique were pointed out by Hampson advantages of these methods are that (1984) but no better method has been assessments may be conducted by the devised in spite of the great economic growers themselves, the data obtained importance of the crop and the significance reflects the level of rat damage/yield loss of rodent damage as a constraint to and that it is possible to target decisions so production in some areas. that applications may be made, when The assessment of rodent damage can be necessary, to land parcels of moderate size used as another indirect index of rodent (e.g. 50 to 100 ha). A disadvantage is that density and, if the relationship between sampling is relatively labour intensive. damage and crop loss is understood, Climatic factors are of limited importance provides additional data on the latter as determinants of pest population densities important parameter. However, much work in seasonal irrigated crops (e.g. lowland rice)

171 Ecologically-based Rodent Management

and in perennial crops (e.g. oil palm) and indirect gauges, such as damage decision-making is then best founded on assessments, are used as the decision­ measures of pest population.<;. However, in making tools, a reasonable understanding of rain-fed crops early-warning systems based the dynamic relationships between rodent on rainfall data may be useful in predicting populations, damage and yield loss is rodent pest outbreaks. Mwanjabe and Leirs needed. (1997) used such a system, combined with damage assessments, to predict outbreaks of ASSESSMENT OF NON-TARGET M. tlatalctlsis in Tanzanian maize fields. An HAZARDS advantage of this approach is that useful information is obtained from established In the 'good IPM check-list' provided by national meteorological monitoring systems. Singleton (1997) it is probably the need for Although substantial work is required on a schemes to be environmentally sound that case-by-case basis to validate the predictive has caused a degree of reluctance among accuracy of such methodology. crop protection researchers to use methods The mechanisms briefly described have based on roden !icides in tropical agriculture. been developed in order to target rodent Of course, the requirement for crop control efforts more efficiently but decision­ protection practices to inflict no unnecessary making is always likely to carry some harm on the environment is of the highest uncertainty. Pest populations may be low importance but refusal to work with until a susceptible crop stage is reached and rodenticides has now reached the level of then there may be a rapid influx from 'chemophobia' in some quarters. In the neighbouring infested habitats. This makes opening chapter of this book a 20-year hiatus it necessary to monitor pest populations in is mentioned during which little progress quite large areas and not exclUSively in has been made in rodent management crop lands. All these systems require a in developing countries. This is partly degree of coordination from some central attributed to too much an emphasis on agency, such as a national surveillance rodenticides. However, the contention that network or a plantation crop protection very little innovative work on rodenticides advisor. Only the method developed for use has been done in tropical agriculture for the in sugarcane is widely adopted and none of past 10 years is borne out by a study of the those designed for tropical smallholders has reference list of this chapter and very few yet gained general acceptance. The challenge projects receiving funding from remains to crop protection researchers and international agencies have included any vertebrate pest managers, therefore, to substantial element concerned with develop and implement practical and improving rodenticide applications. effective systems for monitoring rodent pest Methods for the assessment of the populations to allow timely and appropriate potential for rodenticide applications to harm management actions to be taken in tropical the environment are well established smallholder agriculture. Whether direct (Edwards et al. 1988; Brown 1994). Generally, rodent population density measures or rodenticide applications pose negligible risks

172 The Role of Rodenticides

to soil and aquatic systems because of the occasional rodenticide use on a limited nature of the compounds and their methods number of predatory and scavenging of use. This is particularly the case with species, but such thinking is seldom done. anticoagulants. Baits are discrete, used at low rates of application, and carry low EXTENSION concentrations of, usually, insoluble active ingredients, which are bound readily to soil The fact that smallholders are the most likely particles and do not move into plants. agency by which rodent control measures, However, by their nature, all rodenticides are particularly rodenticides, are to be applied is potent vertebrate toxicants. Their principle often overlooked by those developing risks lie in the potential for non-target management techniques (Posamentier 1997). animals to consume directly baits laid for Conflicting pressures on smallholders' time rodents (primary poisoning) and for and money, their uncertain perception of the scavengers and predators themselves to be importance of the pest problem being poisoned when consuming the bodies of addressed and many other socioeconomic contaminated rodents (secondary poisoning). factors jeopardise the sustainability of Those few extensive field studies that have otherwise well-designed and cost-effective been performed to quantify these potential schemes. Adhikarya and Posamentier (1987) effects (Tongtavee et a1. 1987; Hoque and undertook a 'knowledge, attitude and Olvida 1988) have shown that pulsed baiting practice' (KAP) survey to establish first base­ with wax blocks containing second line information on rodent control practice generation anticoagulants poses few risks to and perceptions among smallholder cereal wildlife populations in Southeast Asian rice growers in Bangladesh. Armed with this fields, but more studies are needed both in information they designed a multi-media rice and in other agro-ecosystems. campaign to modify beliefs and stimulate All rodent management techniques have action. This substantial program met with the potential to affect the environment considerable initial success but its long-term adversely and this is not restricted only to impact is uncertain. those methods based on rodenticides. For It is tempting to look for successful example, the habitat modification methods models of extension of sustainable rodent often recommended in rice fields (removal control programs and attempt to draw of weedy land patches, lowering of bunds, lessons from them. A search for such models increasing field size, periodic deep flooding in current smallholder tropical agriculture is of growing areas and extensive synchronous largely fruitless (Leirs 1997). However, oil planting) would have a significant palm plantations in Malaysia have long detrimental effect on a very wide range of benefited from well organised control non-target taxa that rely on these remnant programs based on anticoagulant baiting. habitats as their only footholds in an These programs are founded on a base of otherwise ecologically barren rice long-term research on the biology and monoculture. Such potential impact needs to control of the pest funded by those with be weighed against the possible effect of most to gain from its results, the plantation

173 Ecologically-based Rodent Management

sector agri-businesses. As a result, Rattus tropical agriculture mentioned by Leirs tiomanicus is arguably the best understood (1997) and in the first chapter of this book rodent pest of tropical agriculture (see Wood will remain. 1984; Wood and Liau 1984 a,b). Within an estate, or estate group, rat management CONCLUSIONS decisions are made by a single person or In the medium and long-term we look small team, on the basis of well-understood forward to the introduction of novel economic criteria. Resources are usually technologies for rodent pest management available to conduct control operations as The beginnings of some of these are and when necessary. Rodenticide described elsewhere in this book. Those applications are made by trained workers, engaged in their development must keep with no other distracting tasks on the day of sight of the reasons for the past failure of application, and baits are applied over what were considered to be well-designed extensive areas with reasonable expectation, crop protection systems but which proved to therefore, that the investment will be be impractical or unsustainable (Singleton rewarded. The situation in smallholder 1997). Presently, however, there is an urgent cropping could not be more different. need for improved rodent pest management Several agencies may be responsible for in many smallholder agro-ecosystems in decisions, including government crop order to alleviate immediate hardship. For protection, surveillance and extension the time being these are best founded on services, farmer groups and individual IPM principles, with rodenticides used as an growers; all with their own inertia and important element. However, more work is affected by different motivational factors. still needed. Decision-making systems are The financial implications of action or required to help hard-pressed crop inaction are poorly understood and money protections workers to determine when and is rarely available when it is needed. Work is where management programs are needed. done by poorly-trained smallholders, with More extensive field studies of the non­ conflicting time constraints, and the target hazards of rodenticides are required treatments are too often made on small areas so that objective data are available in order with little chance of return on investment to dispel fears, if these prove to be from higher crop yields. In some respects unwarranted, of unacceptable adverse this is an unequal comparison however. Oil environmental impacts. Also, the palm is a perennial crop and lends itself to development is needed of innovative rodent pest management because of the extension technologies to motivate constancy of conditions within crop fields. smallholder farming communities and to Whereas, smallholder systems based on a make well-designed rodent pest mosaic of crop types and pest problems management programs sustainable. present much more difficult conditions. Nevertheless, until some of the problems mentioned above are overcome the current poor status of rodent pest management in

174 ne Role of Rodenticides

REFERENCES Drost, D.e. and Moody, K. 1982. Rat damage in weed control experiments in rainfed trans­ Adhikarya, R. and Posamentier, H. 1987. planted rice. Tropical Pest Management, 28, Motivating farmers for action; how multi­ 295-299. media campaigns can help. Deutsche Gesells­ Drummond, D.C 1978. The major agricultural chaft fUr Technische Zusammenarbeit (GTZ) rodent problems of developing countries. GmbH, Eschborn, Germany, Schriftenreihe, Paper presented to the OECD /FAO /WHO 185,209p. Expert Consultation on Rodent Problems, Brown, R.A 1994. Assessing the environmental Control and Research, Paris, France, 2-5 May impact of rodenticides. In: Buckle, AP. and 1978,34p. Smith, R.H., ed., Rodent pests and their Dubock, AC 1984. Pulsed baiting-a new control. Wallingford, UK, CAB International, technique for high potency, slow acting Wallingford,363-380. rodenticides. In: Dubock, A.C, ed., Proceed­ Buckle, AP. 1988. Integrated management of rice ings of the Conference on the Organisation rats in Indonesia. FAO (Food and Agriculture and Practice of Vertebrate Pest Control, Organization of the United Nations) Plant Elvetham Hall, UK, 30 August to 3 September Protection Bulletin, 36, 111-118. 1982,105-142. Buckle, AP. 1994. Rodent control methods: EPPO (European Plant Protection Organization) chemical. In: Buckle, AP. and Smith, R.H., 1995. Guideline for the evaluation of resist­ ed., Rodent pests and their control. Walling­ ance to plant protection products. Testing ford, UK, CAB International, 127-160. rodents for resistance to anticoagulant roden­ Buckle, AP., Rowe, F.P. and Abdul Rahman, H. ticides. EPPO Bulletin, 25, 575-593. 1982. Laboratory evaluation of the anticoagu­ Edwards, P.J., Brown, R.A, Coulson, J.M. and lants coumatetralyl and brodifacoum against Buckle, AP. 1988. Field methods for studying Rattus argentiventer in peninsular Malaysia. the non-target hazard of rodenticides. In: Tropical Pest Management, 28,126-130. Greaves, M.P., Smith, B.D. and Greig-Smith, Buckle, AP., Rowe, F.P. and Abdul Rahman, H. P.W., ed., Field methods for the study of 1984. Field trials of warfarin and brodifacoum environmental effects of pesticides. BCPC wax block baits for the control of the rice field Monograph No.40. Thornton Heath, UK, rat, Rattus argentiventer, in peninsular Malay­ British Crop Protection Council, 77-88. sia. Tropical Pest Management, 30, 51-58. Greaves, J.H. 1985. The present status of resist­ Buckle, AP., Yong, Y.C and Rowe, F.P. 1985. ance to anticoagulants. Acta Zoologica Damage by rats to rice in South-East Asia Fennica, 173, 159-162. with special reference to an integrated management scheme proposed for peninsu­ Greaves, J .H. 1994. Resistance to anticoagulant lar Malaysia. Acta Zoologica Fennica, 173, rodenticides. In: Buckle, AP. and Smith, R.H., 139-144. ed., Rodent pests and their control. Walling­ ford, UK, CAB International, 197-217. Chia, T.H., Buckle, AP., Visvalingam, M. and Fenn, M.G.P. 1990. Methods for the evalua­ Greaves,J.H. and Ayres, P. 1969. Some rodenti­ tion of rodenticides in oil palm plantations. cidal properties of coumatetralyl. Journal of In: Proceedings of the Third International Hygiene, Cambridge, 67, 311-315. Conference on Plant Protection in the Tropics, Hampson, S.J. 1984. A review of rodent damage 20-23 March 1990, Genting Highlands, to sugar cane with criteria for the use of Malaysia. Malaysian Plant Protection Society, rodenticides. In: Dubock, AC, ed., Proceed­ 19-26. ings of the Conference on the Organisation Dolbeer, R.A 1981. Cost-benefits determination and Practice of Vertebrate Pest Control, of black bird damage for corn fields. Wildlife Elvetham Hall, UK, 30 August to 3 September Society Bulletin, 9, 45-51. 1982,227-251.

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Hoque, M.M. and Olvida, J.L. 1987. Comparison Pest Management in Africa, 21-25 October of baiting methods for ricefield rats in the 1996, Morogoro, Tanzania. Belgian Journal of Philippines. In: Richards, CG.J.R and Ku, Zoology, 127 (supplement 1), 137-144. T.Y., ed., Control of mammal pests. London, Mwanjabe, P.S. and Leirs, H. 1997. An early Taylor and Francis, 237-248. warning system for II'M -based rodent control Hoque, M.M. and Olvida, J.L. 1988. Efficacy and in smallholder farming systems in Tanzania. environmental impact of flocoumafen In: Leirs, H. and Schockaert, E., ed., Proceed­ (Storm) wax block baits used for rice field rat ings of the International Workshop on Rodent control in the Philippines. In: Crabb, A.C and Biology and Integrated Pest Management in Marsh, RE., ed., Proceedings of the Africa, 21-25 October 1996, Morogoro, Thirteenth Vertebrate Pest Conference, 1-3 Tanzania. Belgian Journal of Zoology, 127 March 1988, Monterey, USA, 75-81. (supplement 1),49-58. Khoo, CK. 1980. 'Pulsed baiting' with brodifa­ Posamentier, H. 1989. Rodents in agriculture­ coum baits to control oil palm rats in Malay­ review of findings in Bangladesh. Sonder­ sia. Selangor Planters Associations, Annual publikation der GTZ No.16. Deutsche Report/Journal, 198,42--46. Gesellscha ft fiir Technische Zusammenarbeit Lam, Y.M. 1977. Zinc phosphide-an effective (GTZ) GmbH, Eschborn, Germany, 108p. rodenticide for the rice field rat, Rattus argen­ Posamentier, H. 1997. Communication in tiventer. Malaysian Agricultural Journal, 51, national rodent management programmes. 228--237. In: Leirs, H. and. Schockaert, E., ed., Proceed­ Lam, Y.M. 1978. The rice field rat. Information ingsofthe International Workshop on Rodent Paper No.2. Malaysian Agriculture Research Biology and Integrated Pest Management in and Development Institute, 37p. Africa, 21-25 October] 996, Morogoro, Tanzania. Belgian Journal of Zoology, 127 Lam, Y.M. 1984. Further evidence of resistance to (supplement 1),171-180. warfarin in Rattus rattus diardii. MARDI (Malaysian Agricultural Research and Devel­ Redfern, R, Gill, J.E. and Hadler, M.H. 1976. opment Institute) Research Bulletin, 12, 373- Laboratory evaluation of WBA 8119 as a 379. rodenticide against warfarin-resistant and non-resistant rats and mice. Journal of Lam, Y.M.1990. Cultural control of rice field rats. Hygiene, Cambridge, 77, 419--426. In: Quick, GR, ed., Rodents and rice. Report of an expert panel meeting on rice rodent Rennison, B.D. 1976. A comparative field trial, control, 10-14 September 1990, Los Banos, conducted without pre-baiting, of the roden­ Philippines, 65-72. ticideszinc phosphide, thallium sulphate and gophacide against Rattus l1oroegicus. Journal Leirs, H. 1997. Preface. In: Leirs, H. and Schock­ of Hygiene, Cambridge, 77,55-62. aert, E., ed., Proceedings of the International Workshop on Rodent Biology and Integrated Richards, CG.J.R. and Buckle, A.P. 1987. Pest Management in Africa, 21-25 October Towards integrated rodent pest management 1996, Morogoro, Tanzania. Belgian Journal of at the village level. In: Richards, CGJ.R. and Zoology, 127 (Supplement 1), 3--5. Ku, T.Y., ed., Control of mammal pests. London, Taylor and Francis, 293-312. MAFF (Ministry of Agriculture, Fisheries and Food) 1976. Control of rats and mice-refer­ Salvioni, M. 1991. Evaluation ofrat damage in ence manual for pest control personnel. rice fields in Madagascar. Tropical Pest United Kingdom, MAFF, 97p. Management, 37, 175-178. Mathur, R. 1'.1997. Effectiveness of various Singleton, GR.1997. Integrated management of rodent control measures in cereal crops and rodents: a Southeast Asia and Australian plantations in India. In: Leirs, H. and Schock­ perspective. In: Leirs, H. and Schockaert, E., aert, E., ed., Proceedings of the International cd., Proceedings of the International Workshop on Rodent Biology and Integrated Workshop on Rodent Biology and Integrated

176 The Role of Rodenticides

Pest Management in Africa, 21-25 October Wood, B.]. 1969. Population studies on the 1996, Morogoro, Tanzania. Belgian Journal of Malaysian wood rat (Rattus tiomanicus) in oil Zoology, 127 (supplement 1),157-169. palms, demonstrating an effective new control method and assessing some older Singleton, C ,R. and Petch, D.A. 1994. A review of ones. Kuala Lumpur, Planter, 45, 510--525. the biology and management of rodent pests in Southeast Asia. A ustralian Centre for Inter­ Wood, Bl1984, A long term stud y of Rattus national Agriculture Research Technical tiomanicus populations in an oil palm planta­ Reports, 30, 65p. tion in Johore, Malaysia. 1. Study methods and population size without controL Journal Sumangil, J.P. 1990. Control of ricefield rats in the of Applied Ecology, 21, 445-464. Philippines. In: Quick, G.R, ed., Rodents and Wood, BJ 1994. Rodents in agriculture and rice. Report of an expert panel meeting on rice forestry. In: Buckle, A.P. and Smith, RH., ed., rodent control, 10-14 September 1990, Los Rodent pests and their controL Wallingford, Banos, Philippines, 35--47. UK, CAB International,45-83. Tongtavee, K., Hongnark, 5., Atrchawakom, T., Wood, RJ. and Chung, C.F. 1990. Warfarin resist­ Hongsbhanich, N., Brown, R.A. and ance of Rattus tiomanicus in oil palms in Richards, C.C.J.R.1987, The safety and Malaysia and the associated increase in Rattus efficacy ofbrodifacoum (Klerat) wax blocks diardii. In: Davis, L.R. and Marsh, RE., ed., and zinc phosphide for rodent control in Proceedings of the Fourteenth Vertebrate Thailand. In: Richards, c.G.J.R. and Ku, T.Y., Pest Conference, 6-8 March 1990, Sacra­ ed., Control of mammal pests. London, mento, USA, 129-134. Taylor and Francis, 173-180. Wood, B.J. and Liau, SS. 1984a. A long term West, RR, Fall, M.W. and Libay, J.L. 1975. Field study of Rattus tiomanicus populations in an trial of multiple baiting with zinc phosphide oil palm plantation in Johore, Malaysia. n. to protect growing rice from damage by rats Recovery from control and economic aspects. (Rattus rattus mindanensis).In: Proceedings Journal of Applied Ecology, 21, 465--472. rd 3 Annual Scientific Meeting. Crop Protec­ Wood, B.J. and Liau, 5.5. 1984b. A long term tion Society of the Philippines, 143-147. study of Rattus tiomanicus populations in an oil palm plantation in Johore, Malaysia. Ill. Bionomics and natural regulation. Journal of Applied Ecology, 21, 465--472.

177 Grant R. Singleton , Sudarmaji, Jumanta, Tran Quang Tan and Nguyen Quy Hung

Abstract

Di gging, trap ping, flooding, netting, rat drives and physical barriers are the norm fo r ro dent control in rice fi elds in most developing countries. We provide a bri ef overvi ew of phys ical methods of control ai med at reducing pre-h arvest damage by rodents, then consider in detai l the use of trap-barrier system s. An important catalyst for adopti on of ph ysical co ntrol in Southeast Asi a is th e use of bounties for each rat captured. In Austra li a, uses of bounties to cont rol vertebrate pests have been singularl y unsuccessful. Differing socioeconomics an d more intense trappi ng may provi de better results in developing coun tries. The re is a scarcity of good data to assess whethe r bounties based on physical actions of co ntrol are effective. In contrast, experimental field studies support the strategic use of trap-barrier systems (TBS) using early crops ('trap crops ') as a lure to rodents . Experimental studies in West Java , Indonesia, and the Mekong and Red River Deltas of Vietnam, indicate that TB S plus trap crops (TB S+ TC) are cost-effective in most seasons. Yield increases of up to 1 t/ha have been recorded up to 200 m from a TB S+ TC. The need to invest money into traps and fences, which protect neighbouring crops , requires a community-based approach for rodent management. An untested reco mmendation is that one TBS+ TC (25 x 25 m) would be sufficient for every 15 ha of rice crop. Although we require more detailed knowledge of the population ecology and biology of rodent pest species, what we already know has had an important influence on the development of management strategies incorporating physical methods.

Keywords

Rice-field rat, physical control, tra~barrier system, bounty, rodent management

178 Physical Control of Rats in Developing Countries

INTRODUCTION control used in developing countries, then consider in detail the use of trap-barrier systems. The latter will cover historical N DEVELOPING COUNTRIES, innovations in the use of the technique, its physical methods of control are efficacy across different rice agro-ecosytems, I probably the most commonly used benefit-cost analyses, strengths and approaches by farmers to combat rodent weaknesses of the approach, research needs, pests. This is simply because they generally and its likely role in ecological and cannot afford, or do not have ready access to, sustainable management of rodent pests at a chemical rodenticides, fumigants, nest boxes village and district level. for birds of prey, or other forms of rodent control. PHYSICAL METHODS-GENERAL Physical methods have been long recognised as effective for reducing the Many inventive techniques have been impact of rodents in post-harvest stores and developed by farmers in developing in intensive animal production units where countries to catch or kill rats or to deflect they damage structures and foul foods them from their crops. These include the (Jenson 1965; Brooks and Rowe 1979; methods outlined in Box 1. Meehan 1984). Actions include mechanical Other methods are more peculiar to proofing inside and outside buildings or particular regions and countries. These ships, physical barriers preventing access to range from placing offerings in the corner of an area and various means of trapping. crops to a particular god, to catching large Nevertheless, post-harvest food loss to male rats, sewing their anus closed and rodents remains a substantial problem in letting them go again. Farmers believe that tropical and sub-tropical regions (Morley 'sewn rats' will become aggressive through and Humphries 1976; Elias and Fall 1988; an inability to use their bowels and therefore Prakash and Mathur 1988). Post-harvest scare neighbouring rats away. This latter losses and impacts on livestock production technique is inhumane and there is no will not be considered further in this evidence that it is effective. chapter. Instead we refer interested readers to review articles and leaflets on rodent The efficacy of the techniques described management in large food stores (Meyer in Box 1 for controlling rodent populations is 1994), pig production units (Brown and rarely assessed. Many are inappropriate Singleton 1997), and small to medium-sized given the risk they present to humans. For food stores and food processing units in example, in their desperation to protect their developing countries (Posamentier and van crops from rodents, some farmers redirect Elsen 1984; Bell 1998). mains-power so that it flows through wire This chapter will focus on physical suspended centimetres above a flood­ methods aimed at reducing pre-harvest irrigated rice crop. The wire is strung around damage by rodent pests. We will provide a the margins of the crop, killing any rat that brief overview of physical methods of comes in contact with it. This method has

179 Ecologically-based Rodent Management

Box 1. Methods promoted by farmers in developing countries to catch or kill rats or to deflect them from their crops - • Various snare and live-traps, usually made of bamboo, that garrotte a rat or break its back (see Mathur 199 7; Schiller et aI. , Chapter 18 ). • Bamboo tubes-simply offer cover for rats and either they get stuck or they are caught alive a ~ empt ied into a bag. • Digging of burrows to kil l rats in situ; occasionally dogs are used to locate burrows or to he lp hu nt rats flushed fro m burrows (e.g. Posamentier and van Elsen 1984). • Rat drives or battues-where rats are driven from cover and herded towards nets (Singleton and Petch 1994). • Stalking at night with a kerosene light and a net at the end of a long handle-in Co Dung village of Hai Duong province in Vietnam , farmers apply this method from 1900- 2200 hrs at specific times of the year and each farmer catches from 5-15 kg of rats per night. • Electrocution--electrical wire is strung the length of a rice crop about 10- 50 mm above a flooded paddy; wet rats that make contact with the wire are quickly killed. As indicated below, this method presents an unacceptably high risk to human health. • Physical barriers-these usuall y consist of plastic or metal sheeting and are placed aro und or along the borders of crops or around areas where grain is stored (e.g. Lam 1988 ). • Physical barriers plus traps-live-multiple-capture traps are inserted intermittently at the base of a - physical barrier. The traps are placed against small holes in the barrier. Rats enter the traps, attracted to the developing crop or stored food that is on the other side of the barrier (e.g. Lam et al. 1990; Singleton et al. 1998). • Metal rat guards-sheets of metal are wrapped around the trunk of a tree , higher than 1 m from the ground , to prevent rodents from climbing trees to access fruits. The design of the guards depends on the climbing habits of the rodent species; some are fl at against the tree, whilst others are conical or circul ar metal sleeves, flush with the trunk of the tree but projecting outwards at, or less than, 90° from t he trunk (e.g. Posamentier an d van Elsen 1984). • Scaring devices - wh ite cloth or plastic is attached to a bamboo pole approximately 1 .2 to 1.5 m high. The white material flapping in the wind supposedly mimics the flight of owls and therefore frightens rats away from the immediate vicinity. These 'scare-owls' are erected in ripening crops where rat damage is evident. been observed by one of us (G. Singleton) in BOUNTY SYSTEMS the Philippines and Vietnam. In southern Luzon, Philippines, 11 Bounty schemes in general human fatalities were reported in the late 1980s (Quick and Manaligod 1990). In Thai In developing countries, management Binh province in the Mekong River Delta, actions are often poorly coordinated. This three people were killed in 1997. results in rats quickly reinvading areas where control has been cond ucted. Sometimes governments introduce a bounty system as an incentive for widespread concurrent control. Inherent weaknesses of bounty systems are that they require rats to

180 Physical Control of Rats in Developing Countries

be caught and they are generally invoked A recent review of bounty schemes by once densities are already high. This leads to Hassall and Associates (1998) identified the two major problems. The first is that following reasons for their failure. bounties promote inefficient reliance on ~ Fraud~schemes are abused by people physical methods of rodent control such as they are supposed to serve. live-trapping, digging and rat drives, replacing management programs based on ~ Harvesting mentality-bounties are seen the use of rodenticides, better farm hygiene, as an ongoing source of income rather than habitat manipulation and! or changes in a control measure. farm management practices. The second is ~ Inefficiency of control-financial that bounties encourage a crisis incentives promote management systems management mentality~acting when rat which provide bodies of animals; as numbers are high, rather than the more discussed above, there are generally more appropriate use of early tactical efficient methods for control. management (see Redhead and Singleton

1988; Brown et a1. 1998). Often the rationale ~ Compensatory growth by pest for invoking a bounty system is more to do populations-unless more than 50% of a with political expediency rather than pest population is removed by a bounty, developing an effective, community-based then at best, the pest population will management strategy. Governments have to maintain numbers through enhanced be seen to be doing something to help survival, higher rates of immigration from farmers in their fight to save their crops from uncontrolled areas and better reproductive the ravages of high density rodent performance (Caughley 1977; Hone et a1. populations. The collection of tens of 1980). thousands of rat bodies has a strong visual effect, providing a sense of satisfaction to ~ Inadequate benchmarks for success-few farming communities that they have waged programs have appropriate success criteria a good fight against their perennial enemy. and so they continue from one campaign to the next vvith the sole criteria being that Bounty schemes have been around for they caught many animals last time hundreds of years and have been adopted in through imposing a bounty. many countries. In Australia, bounties were This review primarily considered the first introduced in 1830 for the tails of appropriateness of bounties in Australia. It unregistered dogs in metropolitan Sydney. concluded that bounties were not a cost­ Since then, bounties have been used for both effective system for managing vertebrate introduced (e.g. foxes and wild horses) and pests. native species (e.g. dingoes, species of wallaby, Tasmanian tiger) (Breckwoldt Bounty schemes for rodents 1988). In Australia, as elsewhere, there is no compelling evidence that bounty schemes Rodents have all the life history have been successful in achieving their characteristics that suggest they would not management aim. be the appropriate target for a bounty

181 Ecologically-based Rodent Management

scheme. They are highly fecund, can all years) is 200 dong for a rat tail (14,000 produce a litter every three weeks, are dong to US$l). Bounty schemes have been extremely mobile and are widely distributed also implemented in Cambodia and the across a landscape. Moreover, most rat Philippines. drives or bounty systems are conducted In 1991 in Luang Prabang province in once rats have already become a significant northern Lao PDR, a sparsely populated problem. Often then it is too late to protect region by Asian standards, over 600,000 rat the ripening crop. tails were collected in just 2-3 months (see The issue of compensatory growth of Singleton and Petch 1994 for details). The poputations, therefore, is particularly bounty scheme stopped because the money important when considering the potential ran out. These figures are impressive and it effectiveness of bounties for controlling may have been a successful campaign. The populations of rodent pests. In the case of officials that one of us (G. Singleton) spoke to Norway rats, Rattus norvegicus, in urban were certainly impressed by the number of environments in the United States of rats they caught and had little doubt about America, populations which have been its success. However, there was no reduced to 10-25% of their pre-treatment quantitative assessment of whether there level, double their population size within 2- was a substantial impact on pre-harvest 4 months and are back to >75% of pre­ losses caused by rats. In that year it was still treatment level by 6-8 months (Emlem et a1. common for growers to report losses of 1948). Similarly, trapping high numbers of greater than 50% to their crops (WaIter muskrats (Ondatra zibethicus) in Germany, Roder, pers. comm.). had little impact on the dynamics of their In August 1998, a rat bounty of 50 rupiah abundance. Indeed, it was estimated that per rat was instigated in four adjoining annual loss due to trapping was less than the villages in West Java, Indonesia. Over number of naturally surplus individuals in a 164,000 rats were collected from 1,790 ha in population (Halle and Pelz 1990). less than a month. In one village of 230 ha, an Perhaps the implementation of bounty average of 222 rats were caught per ha. The schemes in developing countries may hold bounty was instigated during the land greater promise. In these countries, the preparation for a third rice crop for 1998. A density of people per hectare is up to two third crop is unusual for West Java and the orders of magnitude higher and individual mass action against rats was activated to holdings are measured in fractions of a guard against rat to the newly sown hectare rather than thousands of hectares. crop. The action seemed to be successful, In Lao People's Democratic Republic although there was no control site for (POR), the rat bounty is around 70 kip per rat comparison and no quantification of crop tail (4,000 kip to US$l). In Indonesia, in West damage. Nevertheless farmers were satisfied Java, the rat bounty is 50 rupiah for the head with the outcome. of a rat (9,000 rupiah to US$l). In Vietnam, in More impressive still were the numbers the Red River Delta, the going price during a of rats caught under a bounty system in bounty season (bounties are not available in Vietnam. In 1997, 22 provinces applied a rat

182 Physical Control of Rats in Developing Countries

bOlUlty scheme for specific times of the year catch, however most are locked into and 55 million rats were killed . The conducting nightly control campaigns combined cost for the provincial during the generative sta ge of the rice crop governments involved was approximately because they can ill afford to lose much of 62 billion dong (see Table 1). thei r potential harvest to rats. These intensive physical ac ti vities and bolUl ty In 1988, in the first two months of the schemes elsewhere need to be assessed yea r, 8.5 m illi on rats were killed throughout against specific criteria of success. Apart Vietnam lUlder the bOlUlty system. In the from a simple benefit-cost analysis, it is one province ofVinh Phuc, over 5 million rat important also to take into account whether ta ils were returned from January-September the time, effort and resources could have 1998-the bOlU1ty season closed in October. been more effectively marshalled for an This is in a province where the human alternati ve strategy of rodent control. Such a population is around 1.1 m illion. strategy that may even centre on a Regardless of the theoretical evidence coordinated, restricted, bolUlty season that that suggests bounties may be an inefficient shifts focus to earlier tactical intervention. means of controlling rat populations, digging, trapping, flooding, fumigation, and PHYSICAL CONTROL AS AN ADJUNCT TO ra t drives are the norm for rodent control in RODENTICIDE BAITS rice fields in most developing cOlUltries (see Ja hn et aI., Chap ter 17 and Schiller et aI., Knowledge from both the population ecology Chapter 18) . Unfortw1ately, there is a and feeding behaviour of rats indicates that scarcity of good data to assess whether these the best time to use rodenticide baits in and physica l actions of control are effective or arolUld rice crops is at maximum tillering. not. In regions such as West Ja va, the This coincides with the onset of breeding and intensity of physical activities directed at with the final weeks of a 2-6 month fallow controlling rats is high. There, some people period when food quality and quantity have get paid a levy on the munber of rats they been low.

Table 1. Number of rats returned for bounty payments In three northern and three southern provinces of Vietnam for the first five months of 1997. (Source: Ministry of Agriculture and Rural Development, Vietnam.)

Province Area rice damaged (ha) Vietnamese dong paid for bounty Red River Delta (North) Hai Duong 4 139 3363257 672651400 Hanoi 10000 650000 130000000 Vinh Phuc 6729 9008700 1801 740000 Mekong River Delta (South) Long An 3500 4600000 100000000 Quang Ngai 4752 180225 36015000 Sac Li eu 2990 550000 9000000 ~

183 Ecologically-based Rodent Management

Hence the rat population would be at a The TBS was first developed to protect relatively low density and bait acceptance crops in areas where rat damage was high would be high. Once panicle initiation (e.g. crops adjacent to abandoned begins, rats show low acceptance of baits agricultural land, early planted crops). In (Buckle 1988). In India, local traps then Malaysia, a TBS that extended for 5 km was become a useful control measure together used successfully to protect reclaimed with fumigation and weed control cropping lands that were planted out of (Mathur 1997). synchrony. The most rats caught in one night was 6,872, with 44,101 rats caught in nine weeks. Subsequent studies in Malaysia TRAP-BARRIER SYSTEMS (Lam et al. 1990) and the Philippines (Singleton et al. 1994) focused on the use of In developing countries, a common method small rectangular TBSs (0.25 ha to 4 ha). for protecting a crop from invading rodents Again, promising results were obtained is to use plastic fences to deflect rats and when rat densities and crop losses in mice away from the crop. If the rats are surrounding areas were high. However, successfully kept out they are generally benefit-cost analyses indicated that losses deflected into neighbouring crops. The net would have to be greater than 30% for the effect is that crop losses in a village are rarely TBS method to be cost-effective on a regular reduced. In the 1980s, Lam (1988) developed basis (Singleton et a1. 1994; Lam Yuet Ming, a variation of the drift fence and pitfall pers. comm.). method commonly used for trapping small More promising results were obtained mammals. The variation consisted of placing when the TBS was used to protect a crop that a plastic fence along the margin of a rice crop was locally attractive to rats, e.g. late­ and placing small holes in the fence just harvested rice crops or vegetable crops above the irrigation water. Adjacent to each maturing after the rice crops had been hole is a multiple-capture cage trap harvested (see Lam and Mooi 1994). This led suspended on bamboo above the water level to the development of a second generation (on the crop side of the fence). A mud TBS, consisting of an early or late planted mound provides access to the hole and 'trap crop' within the TBS which lures thence to the trap. The dimensions of the rodents to the traps. The expectation was fence and trap are shown in Figure 1. that rats from the surrounding areas would This fence plus trap method has been be drawn to the trap crop and then enter the variably described as the 'environmentally traps. The TBS plus trap crop (TBS+ TC) friendly system', the 'active barrier system', would then provide a halo of protection to the 'plastic fences and multi-capture trap' the neighbouring rice crops. and the 'trap-barrier system' (TBS). The trap-barrier system or TBS is now the commonly accepted description used in most Southeast Asian countries and is what we will use in this chapter.

184 Physical Control of Rats in Developing Countries

(a) -

Bank ~ HIIIo--- Plastic Fence

Rice Trap Crop ~ Water Bank Rat Trap ----- ~~~ \-- 25m

Bamboo

Bank

Earth Mou nd Rat Trap

(c)

Cb)

Figure 1. (a) Schematic diagram showing the design of the trap-barrier system plus trap crop of rice (lBS+ TC) of rice. (b) TBS and lC in Sukamandi; West Java. (c) TBS in position.

185 Ecologically-based Rodent Management

Experimental field studies in different ~ The TBS+ Te generally provides a halo of agro-ecosystems protection to surrounding crops within 200 m of the fence. The protection is stronger Most of the early claims of the successful use of the closer the crop is to the TBS. a TBS for controlling rats could not be substantiated because there were no ~ The halo of protection provided by a TBS appropriate control sites or replication of trials. varies markedly between seasons. In West Economic data for evaluating the benefit--cost Java, protection extended toaminumum of ratio of a TBS were lacking also. It was as 200 m in two of the three dry seasons, but recent as 1993 that the first replicated and was less pronounced beyond 5 m in the wet controlled study was conducted (Singleton et seasons. In this climatic zone, the TBS+ Te al. 1994). The results from that study indicated is generally more cost effective during the that the benefits of using a TBS were at best dry season rice crop when rat densities are equivocal. These results switched the focus to generally at least an order of magnitude the concept of a T8S+Te, first suggested by higher than in the wet season and their Lam (1988) but which again had not been impact on rice crops is greatest. properly evaluated. Beginning in 1995, controlled studies of ~ Yield increases to surrounding crops are the cost-effectiveness of a TBS+ Te were generally 0.3 to 1.0 t/ha. conducted in irrigated lowland rice crops in ~ The relative benefit--costs are higher if rat West Java, Indonesia. The trap crop was rice densities are higher, however the transplanted three weeks earlier than the relationship between rat density and yield surrounding rice crops. The results from the loss does not appear to be linear. Rice crops 1995 dry season and the 1995/96 wet season are able to partially compensate moderate were extremely promising with benefit--cost tiller damage by rats if it occurs prior to ratios in the vicinity of 20:1 (Singleton et al. maximum tillering (see Singleton et al. 1998). Subsequent studies conducted in 1998 for further details). different geo-climatic zones in West Java (1996-1997) and in the Mekong and Red ~ In West Java, the optimum size of a TBS+ Te River Deltas in Vietnam (1997-1998), have is in the range of 20 x 20 m to 50 x 50 m. followed a similar experimental design When a 10 x 20 m early trap crop was (after Singleton et al. 1998), allowing employed, there was a net loss to farmers. comparisons of the robustness of the efficacy of the second generation TBS. The main ... The comparative performance of the variations in experimental design were the TBS+ Te across the different agro-climatic size of the TBS and lack of replicates in the regions indicates that the technique is likely Vietnamese studies (Tables 2 and 3). to be effective in a wide range of rice agro­ The findings from these experimental ecosystems. The positive reports from studies are summarised in Tables 2-6. The Malaysia (e.g. Lam and Mooi 1994), where main inferences that can be drawn from it was first trialled, adds credence to this these studies are as follows. observation.

186 Physical Control of Rats in Developing Countries

In Vietnam particularly, and Indonesia in arOlmd 3 kg per ha or 45 kg if the halo of 1995- 96, the yield increases at the treatment protection to the sllrrolmding crop extended sites appeared high given the relatively low to 15 ha. The number of rats caught dming number of rats caught. G iven that rats weigh the TBS studies in Indonesia in the dry around 165-200 g and consume about 20- season in 1997, and in Vietnam in the 25% of their body weight per day, then an summer season in 1997, provide more ind ividual rat would take about 30 days to convincing cases for the realised increases in consume 1.5 kg of rice. Yet each rat yield (Table 2). represented a reduction in damage of

Table 2. Overview of when rats were caught in 'trap-barrier system (TBS) plus trap crop' in Indonesia during 1995- 1997. Note the different sizes of TBS. See Singleton et al. 1998 for methods.

Size TBS(m) Season ....QI Timing of rat captures Total ftI .5:! rats Q. Tlllering­ Flowering­ Harvest QI caught a: Booting Heading Site: West Java, Sukamandi 2 500 m2 (50 x 50) Dry season 1 63 82 40 185 1995 2 28 45 17 90 Proportion of total rats 33.1% 46.2% 20.7% Wet Season 1 96 11 10 117 1995/96 2 42 4 9 55 Proportion of total rats 80.2% 8 .7% 11.1% 200 m2 (10 x 20) Dry Season 1 96 11 29 136 1996 2 16 27 26 69 Proportion of total rats 54.6% 18 .5% 26.8% Wet Season 1 15 6 7 28 1996/97 2 50 4 8 62 Proportion of total rats 72.2% 11.1% 16.7% 2 500 m2 (50 x 50) Dry Season 1 75 514 117 706 1997 2 43 441 364 848 900 m2 (30 x 30) 1 65 202 66 333 2 11 86 54 151 400 m2 (20 x 20) 1 46 248 108 402 2 24 85 56 165 Proportion of total rats 10.1% 60.5% 29.4%

187 Ecologically-based Rodent Management

Singleton et al. (1998) proposed three therefore the cost is US$200 per season; factors that together may explain the Vietnam-US$80 (1,016 million dong), the apparent disparity between the number of traps last for minimum of two seasons but rats caught and the resulting increase in not the fence, so the average cost over two yield on the treatment sites. Firstly, each rat seasons is US$50. In Vietnam, this cost can be is likely to have damaged many tillers discounted because the used plastic is during the generative stage, compounding adapted for other purposes and the live rats the loss in yield. The earlier these rats are are often sold to the local market for meat. removed the greater the resulting increase in The traps are the most expensive items of yield. Secondly, the removal of rats leads to a TBS. In Indonesia, they constitute about substantially fewer females breeding in the 60% of the cost. Traps also are easily vicinity of each TB5-an important removed. It is not uncommon for traps to consideration given that breeding disappear overnight, especially when the commences during the maximum tillering system is trialled for the first time in a stage, the average litter size is around 10 and district. Generally, however, peer group the first litter is weaned prior to harvest. pressure at the village level quickly puts a Thirdly, rats in live-capture traps provide an stop to traps being stolen or 'borrowed'. early visual cue to farmers to begin other Staff at the Research Institute for Rice in rodent control activities, leading to more Indonesia have been experimenting with effective rodent control activities on the TBS ways of reducing the cost of traps. The most plots relative to the control plots. Typically promising development is the recycling of in West Java, farmers wait until there is 18-20 litre tins which previously held obvious rat damage to the maturing crop cooking oil or biscuits. They are about a before embarking on intensive rodent quarter of the price of a standard cage trap, control activities. yet they catch about 90 rats for every 100 caught in a standard trap (Table 7). These Economics of a second recycled traps provide the added benefit of generation TBS the possible development of a village-based industry for their manufacture. Cost of a trap-barrier system for trapping Adoption rate of TBS+ TC technology rats in rice crops The benefit-cost ratio of a TBS+ TC varies The cost of the materials for a 25 x 25 m TBS from a gain of 20 times the initial investment with 10 cage traps (allowing for two in a TBS to a net cost when rat densities are replacement traps during a cropping low (Table 6). High benefit-cost ratios are season), and the labour costs required to only meaningful at the village level, because construct a TBS, varies markedly between they only occur if there is a halo of protection countries. In April 1998, the relative costs for extending 150 to 200 m from the TBS. materials were: Indonesia-US$44.75 but should last for four seasons, therefore the cost is US$l1.40 (114,250 rupiah) per season; Malaysia-US$800, should last four seasons,

188 Physical Control of Rats in Developing Countries

Table 3. Overview of when rats were caught in 'trap-barrier system (TBS) plus trap crop' in Vietnam during 1997. Note the different sizes of TBS. Methods were based on Singleton et al. 1998.

Size TBS(m) Season Replicate Timing of rat captures Total Tlllerlng- Flowerlng- Harvest rats Booting Heading caught

Site: Red River Delta 360 m2 Spring 1997 Ha Bac 17 34 13 64 Proportion of total rats 26.6% 53.1% 20.3% (12 x 30) Summer 1997 Ha Bac 40 76 18 134 Proportion of total rats 29.9% 56.7% 13.4% (12 x 30) Summer 1998 Vinh Phuc 119 54 16 189 Proportion of total rats 63.0% 28.5% 8.5% Site: Mekong Delta - Tra Vinh 1000 m2 Summer 1 (Chien) 184 79 40 -303 (30 x 30 m) -Autumn 1997 2 (Cheng) 228 88 67 383 3 148 154 21 323 4 182 87 42 311 5 151 127 34 312 Proportion of total rats 54.7% 32.8% 12.5% Autumn- Spring 1 (Cheng) 72 67 46 185 1997 2 106 89 50 245 3 118 81 62 261 4 105 112 72 289 Proportion of total rats 40.9% 35.6% 23.5% Site: Mekong Delta - Ho Chi Minh 1 000 m2 Winter-Spring 1 482 355 196 1033 1997 2 529 194 4 727 3 551 266 5 822 Proportion of total rats 60.5% 31.6% 7.9%

189 Ecologically-based Rodent Management

Table 4. Effect of the trap-barrier system (TBS) plus trap crop on rice yields (kg/ha) at various distances from the TBS, in Indonesia. These estimates were based on the weight (water content approximately 14%) of unhu"ed rice harvested from 10 m2 quad rats (Repl =replicate; nth =sample from north of TBS; sth =sample from south of TBS; se =standard error of mean yield estimates for the control plots).

Rice yield (kg/ha) Control Site: West Java Srn SOm 100 m 1SOm 200 m Mean se Dry Season 1995 Replicate 1 5600 4750 3500 4750 2313 98.7 Replicate 2 5600 3900 3650 4100 4638 74.7 Mean 5600 4325 3575 4425 3475 Yield relative to control (%) +61% +24% +3% +27% Wet Season 1995/96 Repll nth 6230 5930 5760 5860 5660 5736 37.6 Repl 15th 5990 6070 5920 5690 5560 5498 44.5 Repl 2 nth 6630 5620 5560 5490 5780 4736 48.9 Repl 25th 6250 5590 5670 5430 5670 5210 48.5 Mean 6275 5803 5728 5618 5668 5295 88.0 Yield relative to control (%) +19% +10% +8% +6% +7% Dry Season 1996 Repl 1 nth 4 608 4536 4549 4501 4604 4768 32.8 Repl15th 4495 4593 4576 4575 4539 4705 25.4 Repl 2 nth 4525 4501 4593 4437 4510 4646 28.7 Repl 2 5th 4600 4694 4558 4605 4549 4667 48 .0 Mean 4 557 4581 4 569 4529 4550 469 7 19. 2 Yield re lative to control (%) -3% - 2% - 3% - 3% - 3% Wet Season 1996/97 Repll nth 7 312 7 166 7 317 7165 7 316 7087 12.9 Repl 1 5th 7 301 7201 7112 7135 7 165 7148 52.5 Repl 2 nth 6627 6615 6634 6580 6761 7 317 35.9 Repl 25th 6580 6782 6622 6611 6639 7273 38.4 Mean 6955 6941 6921 6873 6970 7206 27.4 Yield relative to control (%) - 3% - 3% -4% - 5% -3% Dry Season 1997 (50 x 50 m on ly) Repll nth 5200 5400 5800 5400 5300 4100 114.0 Repl 15th 5000 5000 4900 4900 5000 4000 70.7 Repl 2 nth 4800 4700 4500 4600 4400 3920 58.3 Repl 25th 4300 4200 4200 4300 4350 3980 86.0 Mean 4825 4825 4850 4800 4762 4000 41.7 Yield relative to control (%) +21% +21% +21% +20% +19%

190 Physical Control of Rats in Developing Countries

Table 5. Effect of the trap-barrier system (TBS) plus trap crop on rice yields (kg/ha) at various distances from the TBS, in Vietnam. These estimates were based on the weight (water content approximately 14%) of unhulled rice harvested from 10 m2 quad rats (se = standard error of mean yield estimates for the control plots).

Mean Rice yield (kg/ha)a Control

Srn SOm lOOm lS0m 200 m Mean se Site: Red River Delta Spring 1997 Yield relative to 5269 5236 5028 4886 control (%) +8% +7% +3% Summer 1997 Yield relative to 3941 3888 3736 3605 control (%) +9% +8% +4% Site: Mekong Delta Summer-Autumn Site 1 (Chien) 3100 3200 3000 320 0 2700 2817 1997 Yield relative to control (%) +10% +14% +6% +14% -4% Site 2 (Cheng) 3 200 3 200 3150 3000 3600 28 17 Yield relative to control (%) +14% +14% +12% +6% +28% Winter-Spring (Cheng) 4960 4640 4410 4660 4520 4 256 43 .9 1997/ 98 Yi eld relative to control (%) +17% +9% +4% +9% +6%

a The mean rice yie lds for each distance from the TBS were from two measurements, except in winter- spring 1997/ 98 when there were six measurements.

Table 6. The effect of a trap-barrier system (TBS) plus trap crop on mean yield increases up to 200 m from the TBS and the associated benefit-cost ratios, in the Red River and Mekong River Deltas, Vietnam, and West Java, Indonesia. Costs were calculated from material costs of the TBS and labou r costs associat ed with building the fence and the daily clearing of rats from traps. Benefits were based simply on the increase in yield rel ative to an untreated site. The dimensions of the respective TBS, the rat density during the growing season and the t iming of rat damage to tillers, provides context for the variation in benefit-cost ratios.

Year and season Dimensions Rat density Timing of main tiller Mean yield Benefit-cost of TBS damage increase ratio (t/ha) Vietnam Red River Delta Spring 1997 12 x 30 m Low Flowering to harvest 0.3 Summer 1997 12 x 30 m Low Flowering to harvest 0.3 - Mekong River Delta Summer 1997 33 x 33 m Site 1 Medium No data Site 2 Medium No data Winter 1997 33 x 33 m Low/ Med Throughout

191 Ecologically-based Rodent Management

Table 6 . (Cont'd) The effect of a trap-barrier system (TBS) plus trap crop on mean yield increases up to 200 m from the TBS and the associated benefit--cost ratios, in the Red River and Mekong River Deltas, Vietnam, and West Java, Indonesia. Costs were calculated from material costs of the TBS and labour costs associated with building the fence and the daily clearing of rats from traps. Benefits were based simply on the increase in yield relative to an untreated site. The dimensions of the respective TBS, the rat density during the growing season and the timing of rat damage to tillers, provides context for the variation in benefit--cost ratios .

Year and season Dimensions Rat density Timing of main tiller Mean yield Beneflt--cost of TBS damage increase ratio

INDONESIA West Java 1995 Dry 50 x 50m Very high After booting 1995/96 Wet 50 x 50 m Low Maximum tillering 0.5 7:1 1996 Dry 20 x 10 m Medium Transplanting and -0.1 Net cost tillering 1996/ 97 Wet 20 x 10 m Low Low damage - 0 .2 Net cost 1997 Dry 50 x 50m Med/ high Maximum tillering to 0.8 14:1 harvest (all crops) 30 x 30 m 0.5 10:1 20 x 20 m 24:1

Table 7. Comparison of the efficacy of different trap designs in a trap-barrier system (TBS). See Singleton et al. (1998) for description of the 'standard trap'. Trap designs 11 to IV are modifications of a recycled 18 litre tin of vegetable oil (350 x 230 x 230 mm). The comparison was conducted in rice crops at Sukamandi, West Java, during the 1998 dry season. The rice crops were two weeks old and the traps were set for three weeks (May 18- June 3). There were three sample plots spaced 500 m apart. Each TBS was 50 x 100 m with eight traps per plot. One of each trap type was placed in random order along the two 100 m sides of the TBS (SE = standard error).

Trap type Replicate Rats captured Total Mean SE Cost ( Rupiah) I (standard trap) 1 51 317 105.7 40.18 30000 2 184 3 8 2 11 (wire mesh back) 1 22 193 64.3 25.46 6000 2 110 3 61 III (wire mesh front and back) 1 50 277 92.3 32.41 8 000 2 156 3 71 IV (entrance only wi re mesh) 1 24 69 23.0 7.81 4 000 2 36 9

192 Physical Control of Rats in Developing Countries

In developing countries in Asia, this is well population from reaching a density above beyond the area of crop owned by an which they cause unacceptable economic individual family. However, the results have hardship to growers. This is referred to as been sufficiently promising to have the the economic injury level (ElL). To prevent a governments of both Indonesia and Vietnam species reaching its ElL, a lower population express strong support for the threshold is identified at which appropriate implementation and adoption of this simple control actions are implemented. technology. For example, in the Mekong This threshold level is relatively easy to River Delta the concept of a TBS+ TC was define for actions that have a rapid impact only first tested in early 1997, yet by May on the pest population, such as the use of 1998 there were more than 100 TBSs chemical rodenticides (Buckle 1988). This is established in five provinces. In Indonesia, not the case for the use of a TBS+ Te. In this the field trials on the TBS were initially situation, the decision point is at land conducted on a research farm (440 ha) and preparation, to enable the trap crop to be then on a commercial seed farm (1,000 ha planted three weeks in advance of the main with farmers share-farming areas of up to 5 crop. By comparison, the decision of ha). Following our trials, large TBS+ TC (50 x whether to use chemical rodenticides is 50 m or 100 x 100 m) were established and made just before maximum tillering of the both institutions have been pleased with the rice crop (around day 40-45 post returns for their outlay. At the research farm transplanting). there was just one TBS+TC in 1996/97 and it An informed decision of whether or not caught over 26,500 rats. The next year there to use a TB5+ TC requires a population were three TBS+ TCs and over 48,000 rats model that enables reasonable accurate were caught. In 1998, all the plant variety forecasts of rodent population densities for trials on the research farm were conducted the forthcoming cropping season. These within a TBS, and there were more than five models have been developed for some other large TBS+ TCs. regions for mouse plague management in In Malaysia, the country of its origin, the Australia Pech et al., Chapter 4), TBS is generally only used in areas that have however such models in Southeast Asia are acute rat problems (e.g. previously lacking, underlining the need for sound abandoned fields or asynchrony of cropping ecological studies of the principal rodent at borders of districts with different pest species in rice farming systems. irrigation schedules) or high value crops Effective decision analysis on the use of (e.g. research farms). TBS+ TC therefore relies on the development When to use a 185+le? of an ecologically-based management system for rodent pests. Effective and efficient pest control strategies generally have a monitoring protocol that Weaknesses of the TB5+ determines whether particular control le actions need to be implemented. These In weighing up the potential of the protocols are based on preventing a pest TBS+ TC, an economic benefit-cost analysis

193 Ecologically-based Rodent Management

is one of a number of considerations. Others rodenticides, provides governments with include those listed in Box 2. another option for investing funds into Whether these points are minor or major rodent management. will depend on the socioeconomic context of the end-users and on the effectiveness and Moving to village-level management thoroughness of the extension campaign. The impressive cost- benefit ratio for the Moreover, govenunents have shown TBC + TC needs to be viewed in the context through the implementation of bounty that these were experimental studies. The systems that they are prepared to invest in challenge is to transfer this teclulology management of rodent pests. This raises the readily and effectively to rice farmers. An possibility of government subsidies for the importa nt consideration is the average size TBS+ TC at village or regional levels. of family holdings in Southeast Asia, which Subsidising the cost of the materials for a is 0.5 to 1.5 ha. A TBS which encloses 0.25 ha TBS+ TC would be much cheaper than could provide protection to neighbouring funding a bounty system and grain farmers without them outlaying money for production is likely also to be higher under a materials, providing the labour required to TBS+ TC pest management system. maintain the TBS or taking the concomitant The exciting potential of the TBS+ TC risks associated with planting an early trap acting as a platform for an integrated crop. Therefore the TBS + TC will be most strategy for managing rodent pests, and effective if it is part of a community-based therefore lessening the reliance on chemical approach to rodent pest management.

• High initial cost-many farming fam ilies in Southeast Asia do not have the disposable income to invest in pest management methods. • High labour involvement-the traps need to be checked every day, although stoppers (e.g. clump of straw) can be placed in the opening of the traps on days when no labour is available. • Strong vigi lance on maintenance-the fence needs to be checked da ily for evidence of rats going through or under the fence: weed growth needs to be controlled near the fence. • Early trap crop attracts avian and insect pests-this needs to be facto red into a benefit-<:ost analysis. • Mechan ics of growing an arly crop-the main difficulty is the avai lability of sufficient water three weeks in advance of the general irrigation schedule to maintain firstly a rice nursery and then the transpl anted trap crop. An earlier maturing va ri ety of ri ce may help overcome this problem. • Non-target captures-amphibians and repti les are caught in the traps. The experimental protocol requ ires these species be re leased. Whether farmers wou ld re lease all of these species is problematical. • Humaneness-protoco ls have been developed (see Singleton et al. 1998) which include the use of carbon monoxide from the exhaust of motor cycles or automobiles fo r ki ll ing rats. Th e adoption of recom mended methods will depend on the operator but he/she should be encouraged to ki ll the rats humanely. • Envi ro nmental contam in ation- proper disposal and recyc li ng of the pl astic fe nces are required .

194