Rattus Tanezumi in the Upland Rice Terraces of Banaue, Philippines: Demography, Habitat Use, Crop Damage and Yield Assessment

Home , Apomys, Banaue, Chrotomys, Large Luzon forest rat, Malayan field rat, Palm rat

Rattus tanezumi in the Upland

Rice Terraces of Banaue, Philippines:

Demography, Habitat Use, Crop Damage

and Yield Assessment.

Rachel W. Miller

A thesis submitted for the degree of Masters of Science.

School of Biological, Earth and Environmental Sciences,

The University of New South Wales

Submitted April 2007.

Certificate of Originality

I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, nor material which to a substantial extent has been accepted for the award of another degree or diploma at UNSW or any other educational institution, except where any due acknowledgement is made in this thesis. Any contribution made to the research by others, which whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis.

I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project’s design and conception or in style, presentation and linguistic expression is acknowledged.

(Signed)………………………………………..

iii

Acknowledgements

Firstly, I would like to thank Dr Grant Singleton (CSIRO) and Dr Ravindra Joshi (PhilRice) for conceiving this project and applying to AusAid for an Australian Youth Ambassador for Development (AYAD). Grant’s field visit, academic advice and technical support have been invaluable.

I owe a lot to Jocelyn Lamuton and Janet Hangdaan of Banaue, who taught me everything I needed to know about rice, Ifugao culture and how to navigate around rice terraces. Their maturity, intelligence, patience, negotiation skills and impeccable work ethic made data collection both easy and enjoyable.

Thanks Dr Peter Banks (UNSW) for visiting Banaue and once again for being my academic supervisor, your intelligence and patience are endless.

The farmers’ survey would not have been possible without the friendly cooperation of 360 farmers and the multilingual interviewing techniques of Jocelyn Lamuton and Romeo Heppog, thank you.

I thank Alex Stuart for providing photographs & sharing his trapping data.

I must acknowledge the few interested volunteers that braved the rice fields to come rat trapping in the wee hours of the morning. Thanks Steph, Henry, Dr Kenneth, Daniele, Kelvin and Marjorie.

Thanks also to my international visitors Mum, Fi, Kate, Tam, Scott and Jen for coming and checking on me during my 14 month stay in Banaue.

Last but not least I’d like to thank the people of Banaue for making “the rat girl” feel very welcome. Particularly, my (now) husband Kelvin Labador, the Nabannal & Bustamante families; my good mates, Ben, Henry, Germaine, Gladys, Jessy, Julio, Derek and Steph; my Ilogue neighbours; and of course the farmers.

I acknowledge the support provided to me from the AYAD Program, CSIRO Sustainable Ecosystems, PhilRice, IRRI, the NSW National Parks and Wildlife Service and the University of New South Wales. iv

Summary

Rodents cause significant damage to agricultural crops throughout the world, including rice, the staple food for the increasing population of Southeast Asia. Little is known about the ecology of pest rodent species, resulting in much effort being concentrated on ineffective, time consuming control practices. This research was designed to understand the demography and habitat use of the major pest rodent (Rattus tanezumi) of the Banaue rice terraces in order to identify the most efficient time and location to undertake pest control. Rodent crop damage and associated yield loss was also assessed in order to provide information for a cost : benefit analysis of rodent control practices. And the beliefs, perceptions and practices of Banaue rice farmers were investigated to assist in identifying future compatible rodent control programs.

Replicated cage trapping was undertaken for a twelve month period over the entire rice cropping season in two study sites in the Municipality of Banaue Philippines. The breeding season of R. tanezumi corresponded with periods of food availability from the transplanted to ripening stages of the rice crop. A non-breeding season occurred from the fallow to seedling stages. The distinct breeding season occurred within the rice fields and adjacent village and scrub habitats. Radio-tracked and spool-and-line tracked R. tanezumi moved from adjacent habitats into the rice field during the breeding season, and individuals persisted in all habitat types, including the rice field, during the fallow, non- breeding season. Overall rice yield was significantly greater (43%) in areas where rodents were excluded by fencing compared to areas where rodents were not excluded. More rodent damage to rice tillers occurred at the booting than at the ripening stage of the rice crop.

These results suggest that to prevent rodent damage, control should be undertaken at the end of the R. tanezumi non-breeding season (prior to transplanting), before rodent numbers multiply and crop damage occurs. Further, the cost-benefit analysis of non-chemical rodent control programs in Banaue, suggests that benefits accrue once yield loss is likely to exceed 5%. v

Table of Contents

Thesis Title...... i

Certificate of Originality...... ii

Acknowledgements...... iii

Summary...... iv

Table of Contents...... vi

List of Tables...... viii

List of Figures...... ix

Chapter 1 Introduction...... 1 1.1 Impacts of vertebrate pests ...... 2 1.2 Ecologically based rodent management...... 4 1.3 The Philippines – rice production and pests...... 6 1.4 Banaue rice production, pests and Ifugao Culture...... 8 1.5 Aims of study...... 10

Chapter 2 Study Area and Rodent Species...... 11 2.1 Study area...... 12 2.1 Rodent species of Banaue...... 16

Chapter 3 Demography of Rattus tanezumi...... 23 3.1 Introduction...... 24 3.2 Methods...... 27 3.2.1 Field techniques...... 27 3.2.2 Data analysis...... 30 3.3 Results...... 32 3.3.1 Trap success...... 32 3.3.2 Breeding history of adult females...... 34 3.3.3 Pregnancy rates and litter size...... 36 3.3.4 Body Condition...... 39 3.4 Discussion...... 44 vi

Chapter 4 Habitat Use and Movement of Rattus tanezumi...... 48 4.1 Introduction...... 49 4.2 Methods...... 53 4.2.1 Microhabitat features...... 53 4.2.2 Spool-and-line tracking...... 53 4.2.3 Radio-tracking...... 55 4.3 Results...... 58 4.3.1 Microhabitat features...... 58 4.3.2 Spool-and-line tracking...... 60 4.3.3 Radio-tracking...... 62 4.4 Discussion...... 65 4.4.1 Implications to local rodent control practices...... 66

Chapter 5 Crop Damage and Yield Assessments...... 68 5.1 Introduction...... 69 5.2 Methods...... 72 5.2.1 Crop Sampling...... 72 5.2.2 Total Percentage Damage Estimate...... 73 5.2.3 Yield Measurements...... 73 5.3 Results...... 76 5.3.1 Crop Sampling...... 76 5.3.2 Total Percentage Damage Estimate...... 78 5.3.3 Yield Measurements...... 78 5.4.4 Photo-points...... 81 5.4 Discussion...... 83 5.4.1 Crop Damage and Yield Assessment...... 83 5.4.2 Cost : Benefit of Rodent Control...... 84

Chapter 6 Beliefs, Perceptions and Practices of Ifugao Rice Farmers...... 87 6.1 Introduction...... 88 6.2 Methods...... 89 6.3 Farmer Survey...... 91 6.4 Results and Discussion...... 93 vii

6.4.1 Farmer and Household Profile...... 93 6.4.2 Rice Yield...... 97 6.4.3 Rodent Damage Characteristics...... 98 6.4.4 Rodent Management Practices...... 100 6.4.5 Farmers’ Beliefs...... 102

Chapter 7 Discussion...... 104 7.1 Key Results of Study...... 105 7.2 Implications for Other Rice Agricultural Systems...... 106 7.3 Where to from here ? ...... 107 7.3.1 Management Focus...... 107 7.3.2 Further Research...... 108

References...... 110

viii

List of Tables

Table 3.1 Variation in percentage trap success of Rattus tanezumi in relation to macro-

habitat type and rice cropping stage (Results of the split-plot ANOVA)…………....32

Table 3.2 Variation in body condition of male Rattus tanezumi in relation to macro-

habitat type and rice cropping stage (results of the split-plot ANOVA)……………..39

Table 3.3 Variation in body condition of female Rattus tanezumi in relation to macro-

habitat type and rice cropping stage (results of the split-plot ANOVA)……………..39

Table 4.1 Habitat attributes recorded monthly at each trap location...... 54

Table 4.2 Linear combinations (factors) of habitat attributes, determined by a principle

component analysis...... 58

Table 4.3 Habitat attributes and combinations of attributes that best predict the

probability of capturing R. tanezumi, for months June 2004 – April 2005 in Banaue.....59

Table 4.4 Spool-and–line tracking results for 6 Rattus tanezumi, Banaue 2004...... 61

Table 4.5 Radio-tracking results for 10 individual Rattus tanezumi, Banaue 2004/05 ....63

Table 5.1 Results of the generalised linear model on % cut tillers, using S-Plus...... 76

Table 5.2 Percentage estimate of rodent damage to the rice crop up to the booting and at

the ripening stages at two study sites in Banaue...... 79

Table 5.3 Actual yield (random samples) and maximum potential yield (exclusion

fences) calculations for the 2004 rice cropping season at Liwang, Banaue...... 80

Table 6.1 Summary of Farmer and Household Profile responses from the 2004 Banaue

Farmers’ Survey...... 96

Table 6.2 Farmers’ response Comparison of yield between the 2003 and 2004 rice

cropping season in Banaue...... 97

Table 6.3 Intensity of rat damage during the 2004 cropping season compared to other

years, % of respondents...... 97

Table 6.4 Rodent management practices of 360 Banaue rice farmers...... 101 ix

List of Figures

Figure 2.1 Banaue location map, in relation in relation to the city of Manila on the island

of Luzon, Philippines (© www.pwsb.com) ...... 13

Figure 2.2 Banaue rice-terraced landscape, Poitan Village, May 2004. Shown are the four

macro-habitat types referred to in this study. Photograph taken by Rachel Miller...... 14

Figure 2.3 Rattus tanezumi, Banaue 2004. Photograph taken by Rachel Miller...... 18

Figure 2.4 Rattus exulans, Banaue 2004. Photograph taken by Rachel Miller...... 18

Figure 2.5 Chrotomys mindorensis, Banaue 2004. Photograph courtesy of Alex Stuart

(University of Reading, United Kingdom)...... 19

Figure 2.6 Rattus everetii, Banaue 2004. Photograph courtesy of Alex Stuart (University of

Reading, United Kingdom)...... 19

Figure 2.7 Bullimus luzonicus, Banaue 2004. Photograph courtesy of Alex Stuart

(University of Reading, United Kingdom)...... 20

Figure 2.8 Apomys sp., Banaue 2004. Photograph courtesy of Alex Stuart (University of

Reading, United Kingdom)...... 20

Figure 3.1 Live capture cage trap (R. tanezumi). Photograph taken by Rachel Miller.....29

Figure 3.2 Necropsies of female Rattus tanezumi, 9 embryos in late 2nd trimester.

Photograph taken by Rachel Miller ...... 29

Figure 3.3 Rattus tanezumi percentage trap success in rice field, village and scrub macro- habitats, across the rice cropping season. Tukeys post hoc test shows a (booting/flowering, ripening) < b (stubble), where a and b = ab (fallow/seedling, transplanted, tillering)...... 33

Figure 3.4 Changes in percentage of adult female Rattus tanezumi breeding throughout

the rice cropping season. Monthly trapping data was pooled into cropping stages.....35

Figure 3.5 Percentage of female adult Rattus tanezumi that had bred during the transplanted stage of the crop, at 2 sites where no animals were killed (control, 15 females captured) and at 2 sites where animals were killed (Liwang and Poitan, 12 females captured)...... 35 x

Figure 3.6 Percentage of R. tanezumi females pregnant at each stage of the rice cropping

season. Numbers in () represent the number of females captured and necropsied...... 37

Figure 3.7 Percentage of Rattus tanezumi females in the 2nd and 3rd trimester of pregnancy, at each stage of the rice cropping season...... 37

Figure 3.8 Percentage of Rattus tanezumi females pregnant, in each macro-habitat

respectively, across the rice cropping season...... 38

Figure 3.9 Relationship between skeletal size (head and body length) and body mass in

male (177) Rattus tanezumi from Banaue in 2004-05...... 40

Figure 3.10 Relationship between skeletal size (head and body length) and body mass in

female (148) R. tanezumi from Banaue in 2004-05. Pregnant females were excluded ...40

Figure 3.11 Comparison of male Rattus tanezumi body condition between the 3 macro-

habitat types, rice field, village and scrub...... 41

Figure 3.12 Comparison of female Rattus tanezumi body condition between the 3 macro-

habitat types, rice field, village and scrub...... 41

Figure 3.13 Comparison of male Rattus. tanezumi condition across the stages of the rice cropping season. Tukeys post hoc test shows a (transplanted) < b (stubble), where a

and b = ab (seedling, tillering, booting/flowering and fallow)...... 42

Figure 3.14 Comparison of female Rattus tanezumi condition across the rice cropping

stages…………………………………………………………………….……..42

Figure 4.1 Rattus tanezumi with spool and line attached, Banaue 2004. Photograph taken

by Rachel Miller...... 57

Figure 4.2 Rattus tanezumi with radio-collar, Banaue 2004. Photograph by R. Miller …..53

Figure 4.3 & 4.4 Schematic summary of habitat utilised by individual R. tanezumi radio- tracked in Session 1 (Figure 4.3), during the ripening to fallow stage, and Session 2

(Figure 4.4), during the seedling and transplanted stage of the rice cropping season..60

Figure 5.1 Crop sampling methodology, sample taken at every 5th hill along a row at each

5m distance across the longest axis of a paddy...... 72

Figure 5.2 Rat exclusion fences, Liwang, Banaue. Photograph taken by Rachel Miller ...75 xi

Figure 5.3 Cut rice tiller, typical rodent damage. Photograph taken by Rachel Miller ....75

Figure 5.4 Percentage of rice tillers cut at the booting and ripening stage of the cropping cycle, in paddies with low <10%, medium 10-25% and high >25% visual rodent damage...... 77

Figure 5.5 The proportion of the total damage rodents caused to the rice crop at booting and ripening in Liwang and Poitan. Combining the two sites, 73% of damage occurred

up to booting and 27% at ripening...... 77

Figure 5.6 Liwang photo-points a booting, b flowering, c ripening, and d stubble...... 81

Figure 5.7 Poitan photo-points a booting, b flowering, c ripening, and d stubble...... 82

Figure 6.1 Jocelyn Lamuton (centre) and Romeo Heppog (right), interviewing a Batad rice

farmer. Photograph taken by Rachel Miller...... 90

Figure 6.2 Size of paddy most susceptible to rat damage...... 98

Figure 6.3 Location within a paddy where rat damage occurs...... 98

Figure 6.4 Location of high damaged paddies to major irrigation channel...... 99

Figure 6.5 Location of high damaged paddies within a terraced valley ...... 99

Chapter 1

Introduction.

1.1 Impacts of Vertebrate Pests

A species is considered a pest if it negatively impacts upon human populations and/or natural ecosystems. Generally, pests to natural ecosystems are introduced by humans (directly or indirectly) and specifically threaten native flora and fauna species. For example, the introduction of the red fox (Vulpes vulpes) to mainland Australia has been linked to the decline of native small and medium sized mammal populations, to the point of extinction of some species (Saunders et al. 1995). Australia has a particularly high diversity of alien vertebrates when compared to the rest of the world, and the impacts of some introduced species such as rabbits are infamous. Other introduced agricultural animals such as pigs, goats and cattle have also reduced flora species diversity in native forests and caused significant land erosion problems. There is also an emerging problem of over-abundant native species which impact upon natural ecosystems and must be managed to prevent biodiversity loss.

Vertebrate pests to human populations are introduced or native species which negatively impact upon economic or social values associated with agriculture, infrastructure, or human health. The expansion of human populations has increased the interface between wildlife and humans (Fall & William 2002), and intensified man-made agricultural systems provide a major food source, supporting dramatic increases in vertebrate pest populations, such as exemplified by population irruptions of the introduced house mouse in Australian wheatfields (Singleton et al. 2005).

Foremost amongst vertebrate pests on human interests are the rodents. They are a major pest to human populations because they eat agricultural crops in the field; spoil and contaminate stored food; destroy infrastructure; and may carry diseases (Singleton 2003a). Yet out of the approximate 1700 rodent species in the world, only 5-10% are urban or agricultural pests (Stenseth et al. 2003). Rodents are a particularly problematic pest due to their ability to increase in numbers at a rapid rate, as a result of a short period of time to reach sexual maturity, short gestation, large litter sizes and opportunistic foraging 3 behaviour (Aplin et al. 2003). Many of the most devastating impacts of rodent pests are concentrated in the agricultural ecosystems of the world’s developing countries. Pre-harvest losses to wheat, corn rice, vegetable and fruit crops in Africa (Leirs 1999), South America (Stenseth et al. 2003), and Asia (Singleton 2003a) threaten food security by significantly affecting the ability of farmers to produce self-sufficient staple foods. For example, in Tanzania, damage caused by rodents results in an annual estimated yield loss of 5-15% of maize, equating to food which could feed 2 million people and valued at $45 million (Leirs 2003). Native rodents in parts of South America cause crop damage varying between 5-90% (Stenseth et al. 2003).

In the rapidly growing population of Asia, the single most important crop is rice, producing 35-60% of the total food energy of humans in the Region (Khush 1993; Singleton 2003a). Overall pre-harvest losses to traditional rice production are in order of 5-10% in Asia. By nature, rodent damage is patchy On a local district scale damage has been recorded as high as 50%, particularly in areas where cropping frequency has increased to 2-3 crops per year. A loss of 5% rice production in Asia accounts for roughly 30 million t, sufficient to feed close to 200 million people for a year (Singleton 2003a).

The major rodent pest to lowland irrigated rice crops in South-East Asia, including Indonesia, southern Philippines, Cambodia, Thailand, Malaysia and Vietnam is Rattus argentiventer (the rice field rat) (Aplin et al. 2003; Boonsong et al. 1999; Leung 1998; Singleton 2003a; Tuan et al. 2003). It is ideally suited to rice field habitat due to an apparent preference for dense grassy waterlogged areas (Aplin et al. 2003). In Indonesia it is responsible for annual pre-harvest losses of around 17% (Leung et al. 1999). Other major pest species attributed to pre- harvest rice crop losses in Asia include: Rattus rattus complex in Northern Philippines and the uplands of Laos; Bandicota indica in Bangladesh and Cambodia; Rattus norvegicus in China; Rattus losea in China, Vietnam and Laos; Bandicota bengalensis in India and Bangladesh (Singleton 2003a). 4

Traditional approaches to control rodents in Asia are based on lethal management practices; farmers respond with such a control method when rodent populations have exploded and damage has already commenced, resulting in high numbers of rodent deaths (Leirs et al. 1999). Unfortunately, this reactionary approach is not sustainable and has little impact on reducing the damage caused by rodents (Brown et al. 2003a). Other farmers just accept yield loss caused by rodents or may not even plant a 2nd or 3rd crop because they think rats are “too smart” and rodent damage is unavoidable.

Chemicals are widely used as the primary means of rodent control (Buckle & Smith 1994). However, the indiscriminate use of chemicals can be ineffective when knowledge of habitat use and breeding cycles of a target species is limited (Brown et al. 2003a). Although the chemicals used are cheap, they are often non-specific (eg. zinc phosphide), killing non-target species (including domestic animals), endangering human health, water supplies and the environment. Other more specific chemicals, such as first or second generation anticoagulants are expensive, require frequent applications of bait in large quantities and there is a potential for anticoagulant resistance (Buckle 1999).

1.2 Ecologically Based Rodent Management

In recent years, many researchers have been moving away from the use of chemicals, introducing the concept of ecologically based rodent management (EBRM) (Singleton 1997). EBRM identifies that different species of rodents have varying demography and habitat use and even one species’ ecology varies across different landscapes. Thus, before management strategies can be developed and implemented, basic research of taxonomy, ecology and population dynamics of the target rodent species is required (Leirs et al. 1999). This includes gaining knowledge of natural and agricultural factors, such as shelter and food availability, that contribute to the limitation of pest rodent populations (Jacob et al. 2003). Unlike reactionary approaches by farmers, EBRM, will seldom provide masses of dead rodents. Instead, the idea of EBRM 5 is to keep rodent numbers below levels that cause significant agricultural losses (Leirs et al. 1999).

Of equal importance to EBRM, is gathering information on the knowledge and perceptions of local farming communities in order to select compatible control programs (Aplin et al. 2003). Additionally, gathering information on the time and money used by farmers for rat control enables a cost benefit analysis to be undertaken (Stenseth et al, 2003; Tuan et al. 2003; Singleton et al. 2005).

An example of EBRM in practice is the control of rodents in the Red River Delta, Vietnam (Brown et al. 2006; Brown et al. 2005b; Brown et al. 2003b; Brown et al. 1999; Tuan et al. 2003). Field surveys were designed to determine rodent species composition, population dynamics and habitat use of the major pest species. A questionnaire was conducted specifically for local farmers, to gather information on agricultural practices, farm characteristics, and specifically rodent problems, management and farmer attitudes. Based on the ecological and farmer knowledge gathered, a series of compatible rodent management practices were developed for farmers to implement. Two treated sites where farmers were asked to conduct a set of rodent management practices were selected, and two non-treated sites where farmers were asked to continue their typical practices. Farmers on treated sites used trap-barrier systems (TBS), destroyed burrows in refuge habitats after planting, minimised the size of bunds to prevent burrowing, synchronised rice cropping, and removed weeds and piles of straw. There was no difference in rodent abundance and damage between the treatments, however, there was a 75% reduction in the use of rodenticides at the treatment sites, and the benefit : cost of applying EBRM was 17 : 1 compared to 3 : 1 at non-treated sites (Brown et al. 2006).

EBRM has also been implemented at the village level in West Java, Indonesia (Singleton et al. 2003b; Singleton et al. 2005; Singleton et al. 1998; Brown et al. 2003a). Similarly, surveys were conducted to gain knowledge of the rodent species’ ecology, and the practices and beliefs of farmers. Management 6 practices including TBS, synchronised cropping, reduction in size of irrigation banks, a rat campaign 2 weeks prior to transplanting, and general hygiene around villages were applied. The implementation of EBRM saw a 50% reduction in rodenticide use, tiller damage reduced 1.9 times, and there was an average benefit : cost of 25 : 1 (underestimated because the cost of chemical was unknown/not included) (Singleton et al. 2005).

1.3 The Philippines - Rice Production and Pests

This study examines rodents as pests of rice production in the Philippines. The typical Filipino diet consists of rice (every meal), fish or meat, some vegetables and occasionally fruit. Current food production in the Philippines is sufficient (caloric needs) to support the population, however, the fact that the mean per capita intake is low indicates unequal distribution of food. Urban workers and the rural landless spend 50-70% of their income on purchasing rice (Angeles- Agdeppa 2002).

Fifty percent of agricultural lands in the Philippines are dedicated to rice production. By Asian standards Philippine grain yields are low. Lack of spending on agricultural technology and infrastructure means Philippine yields have not risen as rapidly as in comparable countries (Estudillo et al. 1999; Coxhead 2000). The trade and price policies set by the National Food Authority (NFA) which aim to achieve self-sufficiency and price stability, have lead to output growth being primarily driven by agricultural area expansion. This expansion is largely in the available, forested uplands of the Philippines, causing major land degradation problems. Technical progress (including pest management) could raise yields on existing croplands, working towards self sufficiency targets without expansion of agricultural lands (Coxhead 2000).

Increasing yields is particularly important considering the current Philippine population of 84 million is expected to rise to 120 million in the next 25 years. With this population increase, demand for rice is expected to increase by 65% in a country that is already importing rice (Angeles-Agdeppa 2002). 7

The introduction of high yielding rice varieties to the Philippines in 1973, the so called “Green Revolution”, was initiated through a government program called “Masagana 99”. The government provided credit and advice on rice farming, focusing on the use of high yielding rice varieties, fertilizers and insect pesticides to reach the goal of harvesting 99 cavans per hectare (Palis 1998). Pesticide use was encouraged to combat the effects insect pests (stem borers, rice leaf folder and other lepidopterous larvae), considered by farmers to be a main constraint to high rice yields (Listinger et al. 1980). The widespread introduction and availability of pesticides saw farmers spray insecticides frequently either for prevention or simply because if a neighbour sprays they spray as well (Espina 1983). Recent research has shown, however, that leaf feeder control does not increase yields, indicating a large proportion of insecticide use may be unnecessary (Heong et al. 1994). Pesticide use in the Philippines has also been shown to have a negative effect on farmer health, farmer health has a positive effect on rice productivity and that there are social gains from a reduction in insecticide use in Philippine rice production (Antle & Pingali 1994).

Rodents as pests of rice production in the Philippines have received relatively little attention. In Luzon and the Visayas, the major rodent pest is Rattus tanezumi (Rattus rattus Complex), and in Mindoro and Mindanao, R. argentiventer. The official rodent crop (rice) damage figure released by the Bureau of Plant Industry is 3-5%. However, farmer groups from Pangasinan, Nueva Ecija, Isabela and Iloilo, reported in 2001 that rodent damage was higher than 10%, and individual farmers reported damage up to 30-50% (Singleton et al. 2003a). Reports from PhilRice (Philippine Rice Research Institute) staff, suggest rat damage to rice has increased in areas of Luzon where direct seeding takes place and in hybrid rice nurseries (Singleton et al. 2003a), which are both a government initiative to increase rice production (Angeles-Agdeppa 2002). Rodents are not only a pest to rice crops in the Philippines, they also cause major damage to vegetables (personal observations) and crops such as sugarcane (Hoque & Sanchez 2001). 8

1.4 Banaue Rice Production, Pests and Ifugao Culture.

The Ifugao people have been farming the rice terraces of Banaue for at least 2000 years (Barton 1955). The traditional agro-ecological system of the Ifugaos was able to support a considerably high population density for centuries without depleting its natural resources (Medina 2003).

An Ifugao farming system comprises the rice terrace farm, private woodlot, swidden farm, irrigation canal and residential lot. Importantly, the woodlots (muyong - consisting of second growth forest above the rice terraces) were maintained by selective harvesting and replanting to prevent soil erosion and provide moisture necessary for terrace cultivation (Razalan 2003).

The name Ifugao, is derived from the term ipúgo, meaning “people of the hills”, they believe they are direct descendents of skyworld deities. Rituals accompanied all stages of rice cultivation involving blessing from the bulul (rice god) to make sure rice growth is robust, to drive away pests and to ensure a plentiful harvest. Rice fields are considered an invaluable treasure, ruled by a unique law of inheritance, where land is not parcelised, but wholly inherited by the first child to safeguard a total farming system.

The unique agro-ecological habitat was sustained through a strong social network of definite leaders, territories, work organisations and a system of law based on custom and taboo. Rituals initiated by the tumona (chieftain) of a village at each stage of the rice cropping season, guaranteed the synchronisation of cropping. The traditional rice varieties and the altitude of Banaue, allow for only one rice cropping season a year. Traditional cropping has the following working seasons:

lukya – taking the rice from the granary; hipngat – general field cleaning panal – sowing bolnat – transplanting ulpi – end of planting season hagophop – weeding and replacing stunted seedlings 9

bodad – terrace wall cleaning paad – rice maturing time ngilin – harvest day eve ani – harvest day morning upin – after harvest season kahiw – thanksgiving and replenishing the granary.

Today, a majority of the Ifugao population has been converted to a Christian religion, predominantly the Catholic Church. Although much of the Ifugao culture still remains, rituals are not followed by many closely, leading to a break-down in the synchronicity of cropping. With the promotion of Banaue as a tourist destination, since it’s listing on the World Heritage List, and the decreasing level of self-sufficiency of Ifugaos, there has been an increase in wood carving and furniture production, severely decreasing forest resources. People are seeking quick income generating activities, increasing the misuse of natural resources which in turn threatens the stability and irrigation of the rice terraces.

Pests are a major concern for rice production in Banaue. A farmers’ survey, undertaken by PhilRice in 1998 (Joshi et al. 2000), considered non-insect pests such as earthworms, rodents, golden apple snails and house sparrows, as more damaging than insect pests. Giant earthworms were linked to the erosion of terraces and regarded the number one pest. Rodents were ranked as the number one non-insect pests to directly damage the rice crop, followed by golden apple snails and house sparrows (lowest). Farmers were aware of what stages the rice plant is most vulnerable to non-insect pests, however, they did not know how to manage the pests. Generally farmers had difficulty identifying less obvious insect pests and distinguishing various rice diseases. They also had little exposure to new rice technologies and integrated pest management.

1.5 Aims of Study

This study aims to attain the fundamental information required to implement “ecologically based rodent management” in the upland, rainfed, rice agro- ecosystem of Banaue. Specifically, the four aims of the study are to investigate:

1. the demography of the major rodent pest species throughout a complete rice cropping cycle;

2. the habitat use and movements of the major rodent pest species;

3. rodent crop damage and associated yield loss, to provide information for a cost : benefit analysis;

4. the beliefs, perceptions and practices of Ifugao rice farmers in order to assist in identifying future compatible rodent control programs.

The research was conducted as an offshoot of an Australian Youth Ambassador for Development (AUSAID) project in collaboration with PhilRice and CSIRO, Australia. This project provided a unique opportunity to simultaneously collect quantitative data to address ecological, pest management questions, and these data form the basis of the research thesis.

In Chapter 2, I introduce the study area and rodent community of Banaue. In Chapter 3, I examine the rodent dynamics and demography throughout a complete rice cropping cycle. In Chapter 4, I study the habitat use and movement of R. tanezumi. I assess rodent crop damage and associated yield loss during the Banaue 2004 rice cropping season in Chapter 5. In Chapter 6, I investigate the beliefs perceptions and practices of Ifugao rice farmers. And in Chapter 7, I draw together the key findings of the study, assess the implications on other rice agricultural systems and discuss future directions for rodent management and further research in the Banaue rice terraces. 11

Chapter 2

Study Area and Rodent Species.

2.1 Study Area

This study was conducted in Banaue, Ifugao Province, Philippines. Ifugao Province is situated in the Cordillera Mountain ranges of central Luzon, 320 km north of Manila. The population of Ifugao in the 1995 census was 149 598 with a total land area of 252 778 ha, 64% grassland, 26% forest, and 8% agriculture (Medina 2003). 73% of agricultural land is used to grow rice, followed by 14% for corn, 12% for fruit and 1% for vegetables and legumes. Rice is grown by 90% of farmers in a terraced, upland, rain-fed system (Joshi et al. 2000).

The Banaue rice terraces characteristically extend on the middle and lower slopes of the rugged mountain landscape, with peaks of 1100 m (asl.) and valleys rapidly falling to 900 m (asl.) (Joshi et al. 2004). Mountain peaks above the terraces are covered by secondary forest (muyong), providing moisture for terrace irrigation and preventing soil erosion (Razalan 2003). Directly, adjacent to the terraces are areas dominated by tall grass and cane species, with little or no forest canopy, which are occasionally interrupted by small scale swidden farming. For the purposes of this study these areas are classified as “scrub”. The village residential lots are grouped together, and at the two sites used in this study, are located at the top of the valley along a road, above the rice terraces (Figure 2.2). Typically pigs, chickens, ducks and dogs are raised in the villages. Waste management is limited, garbage is burnt and sewage and grey water is not collected, flowing down slope behind villages.

Ifugao has a dry season from December to April and a rainy season throughout the rest of the year. Average annual rainfall is 3 700 mm (Medina 2003). The single rice cropping season typically starts in January with the sowing of seedling beds and harvest is in August. However, in recent times farmers have become less synchronised, with cropping times varying up to 2 months within some villages.

Figure 2.1 Banaue location map, in relation to the city of Manila on the island of Luzon, Philippines. (© www.pwsb.com) 14

Forest

Village

Scrub

Rice Field

Figure 2.2 Banaue rice-terraced landscape, Poitan Village, May 2004. Shown are the four macro-habitat types referred to in this study. 15

Rice cropping stages described in this study are:

i. seedling – sowing of rice seeds to form seedling beds (within paddies).

ii. transplanted – seedlings transplanted from seedling beds into planted rows.

iii. tillering – the rice plants have grown into a full vegetative state.

iv. booting – a bulge forms at the base of the rice plant (commencement of reproduction.

v. flowering – flowers are produced at the top of the plant, commencing the production of rice grain

vi. ripening – the grain on the panicles harden ready for harvest.

vii. stubble – grain has been harvested, the cut bases of rice plants remain in the paddies.

viii. fallow – the stubble of the rice plants have been removed or worked back into the paddy mud.

2.2 Rodent Species of Banaue

The following rodent species list was compiled during trapping for this and a University of Reading study (conducted by Alex Stuart) in Banaue, Ifugao, April 2004 – May 2005.

Rattus tanezumi (Rattus rattus Complex) – Asian House Rat

Rattus tanezumi (synonym: Rattus rattus mindanensis)) is a hybrid of R. rattus species originating in Southeast Asia. It is the major pest species to rice production in the lowlands and uplands of the Philippines, including Banaue. Rattus rattus Complex are distributed throughout mainland Southeast Asia, islands of South Asia and the Pacific region (Aplin et al. 2003).

In most countries R. rattus Complex is confined to village and urban habitats (Aplin et al. 2003). In the uplands of Laos, R. rattus Complex is the dominant pest in field and village environments, with radio-tracking studies showing the animals also use forest edge habitat (Aplin et al. 2003).

This species has a diet of rice plants, vegetable crops, invertebrates, stored grain/food, household waste and domestic animal feed. Rattus tanezumi can cut whole tillers at all stages of rice plant growth and are agile enough to climb and directly eat the panicles of mature plants.

The species nests in any convenient space, drawing dry soft material, such as leaves/grasses, in a bundle into a confined space. Nests are built in burrows, between rocks, in thick grasses, low shrubs, the fork of a tree, in straw piles in a harvested field, in fallen logs, in the walls and roofs of dwellings, amongst stored grain sacks, and in piles of cut wood (Aplin et al. 2003). In Banaue, it is common for burrows to be dug directly into the banks between rice terraces to build nests.

In Banaue, the species dorsal fur is reddish to greyish brown, often with lighter belly fur (Figure 2.3). Individuals, however, can vary greatly, with some grey- 17

black individuals captured. Adults weigh 150 – 280 grams, gestation is 21 days and average litter size in Banaue is 7.

Rattus exulans – Pacific Rat

Rattus exulans is distributed across mainland Asia, on islands of Indonesia, Philippines and New Guinea, and across into Melanesia, Micronesia, Polynesia and New Zealand. In Southeast Asia it is found in village gardens and houses and less commonly found in cropping areas (Aplin et al. 2003).

Rattus exulans is a pest in the rice fields of Banaue, however, is low in abundance compared to R. tanezumi. It also inhabits villages, however was not captured in scrub or forest habitat during this study.

In Banaue, animals have grey to greyish brown dorsal fur and lighter belly fur (Figure 2.4). When folded back, the long facial vibrissae typically reach beyond the ears. Adults weigh only 50-100 g, thus are often confused with mouse species. However, unlike Mus species, R. exulans has a distinguishable elongated metatarsal pad on the foot (Aplin et al. 2003).

Mus musculus – House Mouse

Mus musculus are commonly referred to as the subspecies castaneus in Philippine populations. Throughout Asia, house mice are responsible for major losses in stored grain (Joshi et al. 2004), are found around human habitation, and rarely exist in cropping areas (Aplin et al. 2003).

In Banaue, during this study, M. musculus was only captured inside houses and in animal enclosures.

Generally the fur is uniform in colour, a plain brown to grey-brown. Adults weigh < 30 g.

Figure 2.3 Rattus tanezumi, Banaue 2004.

Figure 2.4 Rattus exulans, Banaue 2004. 19

Figure 2.5 Chrotomys mindorensis, Banaue 2004 (Stuart)

Figure 2.6 Rattus everetii, Banaue 2004 (Stuart) 20

Figure 2.7 Bullimus luzonicus, Banaue 2004 (Stuart)

Figure 2.8 Apomys sp., Banaue 2004 (Stuart). 21

Chrotomys mindorensis – Luzon Striped Shrew Rat

Chrotomys mindorensis is one vulnerable endemic species of the Chrotomys genus found in Luzon, Philippines (Rickart & Heaney 1991). Also recorded on the island of Mindanao. It inhabits primary and secondary forest and sometimes occurs in adjacent agricultural areas (Heaney et al. 1998).

In Banaue, it was predominantly trapped in forest and scrub habitat, however, it was also captured in village and rice field habitats. Diet consists of invertebrates. The close proximity of forest to the rice terraces in Banaue, is perfectly suited for C. mindorensis to enter the rice fields in search of invertebrate prey. Chrotomys mindorensis is likely to have a beneficial impact on Banaue’s agricultural systems, by helping control invertebrate pests, particularly the introduced Golden Apple Snail (Joshi et al. 2004).

The species has brown dorsal fur with two distinctive black stripes along its back from head to tail. The fur of the belly is white and the tail is shorter than the its body length (Figure 2.5). Teeth are designed specifically for eating invertebrates, not for cutting vegetation. Adult weight is 160 -350 g in Banaue.

Rattus everetii – Common Philippine Forest Rat

Rattus everetii is an endemic species to the Philippines, occurring in all regions, excluding the Batanes island group and the Palawan and Sulu faunal regions. It is common in primary forest, uncommon in secondary forest and generally absent in agricultural areas (Heaney et al. 1998).

During this study, R. everetti was only captured in forest and scrub habitats in Banaue.

Although also a brown-grey coloured rat, R. everetii is distinguishable from R. tanezumi because of its large size and distinctive white end to the tail (Figure 2.6). Adult weight is 200-400 g in Banaue. 22

Bullimus luzonicus – Large Luzon Forest Rat

Heaney (1998) described B. luzonicus as only known in the Luzon Provinces of Aurora, Benguet and Camarines, in mixed primary and secondary lowland forest as well as montane and mossy forest at higher altitudes.

In Banaue, B. luzonicus was only captured in forest and scrub habitat.

Bullimus luzonicus is a large, uniformly coloured chocolate brown rat, with a white tip on the end of the tail (Figure 2.7). A ventral gland is visible on adults. It was the largest rodent species captured in Banaue during this study, with adults weighing up to 800 g.

Apomys sp.

Only one individual Apomys sp. was captured in the forest habitat during preliminary trapping for this study in April 2004. Brown body fur, tail white on underside and brown on top (Figure 2.8), and two pairs of mammae present. Adult weight of 100 g.

Most likely to be Apomys datae or Apomys abrae.

Chapter 3 Demography of Rattus tanezumi.

3.1 Introduction Throughout the world, rodent populations are considered a serious pest due to their ability to increase at a rapid rate (Singleton 2003a). Rodents are capable of rapid population growth because of the short period of time to reach sexual maturity and their high reproductive potential (Aplin et al. 2003). For example, Rattus tanezumi females reach sexual maturity between 2-4 months (average 80 days) after birth, they have a 21-29 day gestation period, typically have litters of 4-10 pups, and can again become pregnant a few days after giving birth. As a result, populations can show near exponential growth under ideal conditions. Hypotheses on rodent dynamics suggest that predation (Ylonen et al. 2002; Arthur et al. 2004), disease (Telfer et al. 2005), food quality (Batzli 1992) and social behaviour (Krebs 1999; Sutherland 2005) may contribute to curb population growth. But for many species the availability of food exerts a dominant force on whether or not females will breed. And in agricultural ecosystems, the food preferred by some species of rodents is also the food being cultivated for human consumption.

Although food availability is widely considered a major limiting factor of rodent populations (Sinclair and Krebs 2002; Klemola et al. 2000; Blackwell et al. 2003; Bergallo & Magnusson 1999) the precise effect of food on population dynamics will differ depending on the species, the particular population and the local environmental factors (Krebs 1999). Some research indicates a strong relationship between food availability, body condition and reproduction for rodents (Turchin & Batzli 2001; Perrin & Johnson 1999; Singleton et al. 2001). In a review of field based, food supplementation experiments, Boutin (1990) reported that of those rodent populations provided supplementary food, 74% showed increases in body condition, and 72% of adult females showed advanced breeding and an increase in breeding activity (proportion of population breeding). The timing of food availability also seems critical in determining population responses to food 25

supply. For example, high food availability during winter, a season when there is usually a hiatus in breeding activity for rodents, can allow winter breeding (Huitu et al. 2003; Singleton et al. 2004; Banks & Dickman 2000). Spring populations then commence the typical breeding season from a higher base, which may then lead to high summer and autumn population sizes and even population outbreaks. Similar patterns are seen in the relationship between breeding and cropping systems. For example, the onset of and length of reproductive activity of Rattus argentiventer (Rice-field rat) in Vietnam, Indonesia and Malaysia correlates directly with the rice cropping season. Onset of breeding occurs near the maximum tillering stage of the rice crop and the breeding season continues through to the ripening stage (Leung et al. 1999; Brown et al. 2006; Lam 1983). When one crop is grown per year a single breeding season occurs, and when two crops are grown per year, two breeding seasons occur (Singleton et al. 2004; Tristiani et al. 1998; Lam 1983; Lam 1980).

Characterising the dynamics of demographic changes of rodent populations is therefore an essential component in understanding the response of a population to food supply. This is particularly important where agricultural crops are the potential food supply. Determining the onset and cessation of breeding in relation to food quality and quantity will help determine the appropriate time to undertake rodent control measures. Moreover, understanding how foods of human origin affect such breeding is most valuable to developing strategies of ecologically-based rodent management see (Singleton et al. 1999a) for overview.

In the Banaue rice terraces of northern Luzon, Philippines, (for one complete annual cropping cycle), I examined patterns in rat body condition, reproduction and population size from the initial planting of rice seedlings through to harvest and fallow. I monitored population changes in the three major macro-habitats which differ in temporal patterns for food supply in the seasonal rice terraces, 26 the more stable high food areas around houses and the relative stable low food areas in the vegetated margins of the terraces. In doing so I aim to:

I. determine whether breeding activity of Rattus tanezumi is related to food availability; II. determine the commencement and cessation of the breeding season of Rattus tanezumi; III. determine whether breeding activity of Rattus tanezumi differs amongst macro-habitat types; IV. determine whether body condition of Rattus tanezumi changes at different stages of the rice cropping season.

3.2 Methods

3.2.1 Field Techniques

Cage Trapping

Over 1 year (May 2004 – April 2005), trapping was undertaken on a monthly basis at two study sites (Poitan and Liwang) using live-capture cage traps. One hundred and twenty traps (60 per site) were placed in the same locations each month in three macro-habitat types: 1. rice field, 2. village and 3. scrub vegetation adjacent to rice fields. At each site, traps were set along two transects in each macro-habitat for four consecutive nights, by which time trap success decreases dramatically. Ten cage traps were set along each transect, spaced approximately 10 m apart. Traps were baited with comote (local sweet potato), checked early in the morning, re-baited and left open during the day. Traps were placed under existing low shrubbery or covered with leaf litter, to provide shelter for captured animals.

All rodents captured were weighed, measured (tail, head & body, hind foot and ear length) and external sexual features recorded. Sexual maturity of males was measured by the condition of the testes: non-descended, partially descended, or fully descended. External signs of sexual maturity of females were measured by examining the vaginal opening and the size of teats. Teats were classified as barely visible, prominent but not lactating, or prominent and currently lactating. The vaginal opening recorded as not open (membrane intact), not open but membrane broken, open with small hole, or open with large hole (Aplin et al. 2003). The abdomen of females also were palpated to assess pregnancy.

Non-pest rodent species were marked using an ear punch and released at the point of capture. Pest species of rodent (Rattus tanezumi, Rattus exulans and Mus musculus) were euthanised on site by cervical dislocation. Internal features of the reproductive system were recorded for each female R tanezumi captured, in order 28

to identify its breeding status. Ten females per cropping stage, was deemed the minimum sample size required to represent the breeding activity of the population. Therefore, if fewer than ten individuals were captured additional trapping for females was undertaken independent of the study sites but still in a similar rice ecosystem.

Each female was necropsied to investigate the condition of the uterus, the development stage of embryos, and to assess the presence of placental scars. The condition of the uterus was recorded as very thin with no obvious blood supply (typically characteristic of juveniles), thin with blood (entering first breeding season), thick no embryos (early stages of pregnancy or recently given birth), or with embryos (pregnant). The embryo development stages were assessed as 1st (0-7 days), 2nd (8-14 days) or 3rd (15-21 days) trimester. The first 5-6 days of 1st trimester are not visible in rats (Aplin et al. 2003), however, development of small bulges (no distinct body form) occur at the end of the trimester. Individuals with visible 1st trimester characteristics were recorded, however, 1st trimester was not considered in the data analysis because the data collected was not representative of the entire embryonic stage. Embryos were considered to be in 2nd trimester if a distinct head and body structure was visible. Embryos in late 2nd trimester developed limbs with no distinct toes. In 3rd trimester, embryos were identified by the development of distinct toes and the emergence of ears. The number of sets of placental scars on the uterus was also recorded, to identify the number of litters a female had previously delivered.

The regular removal of individuals through lethal sampling may have influenced the population processes at Poitan and Liwang. To examine this possibility, additional trapping was conducted at 2 other sites in the 11 month of the 12 month sampling cycle.

Figure 3.1 Live capture cage trap (R. tanezumi).

Figure 3.2 Necropsies of female R. tanezumi, 9 embryos in late 2nd trimester. 30

3.2.2 Data Analysis

Trapping was conducted monthly, however, the timing of cropping was not synchronous between and within the two study sites. As a result the number of replicates sampled for each cropping stage varied. To prevent gaps in the data for each macro-habitat across all stages of the cropping cycle, trap success (the total number of R. tanezumi captured, divided by the number of traps set and multiplied by 100 for percentage calculations) data were pooled for the fallow/seedling and booting/flowering stages of each rice crop.

A split-plot ANOVA was performed to examine variation in percentage trap success. There were no temporal differences in the percentage trap success between Poitan and Liwang (P>0.25), therefore, data from transects across each macro-habitat were pooled, giving 4 transects in each macro-habitat. The factors tested in the ANOVA were macro-habitat, transects nested within macro-habitat and cropping stage, including all interactions. The percentage data were not transformed because, after visual inspection, no strong departures from a normal distribution were observed (Quinn & Keough 2002).

Age Structure

Individuals were considered adults if they weighed more than the lightest 5% of males or females captured that showed signs of reproductive activity (adult females > 99g and adult males > 91g). Adult females were assigned to one of two further groups; adults which had never bred (barely visible nipples, placental scars absent, uterus thin, and embryos absent), and adults which had bred (nipples elongated/lactating, uterus thick, placental scars and/or embryos present). Gaps between the bars of the cage traps allowed small rats (juveniles) to escape. This meant there was a possible underestimate of the percentage of juveniles, therefore juveniles were not considered in the age structure analysis. 31

Two chi-squared analyses were performed to compare the adult age structure of females captured at different stages of the cropping cycle, and between the two sites where kill trapping was conducted (Poitan and Liwang) and the two control sites (no kill trapping). The latter analysis was done on data collected for 11 months only.

Condition

Condition was estimated from an allometric comparison based on body mass and skeletal size (head and body length) for each individual R. tanezumi captured. Male and females were analysed separately, and pregnant females were excluded. Relative condition was calculated following Krebs et al 1993 by first regressing skeletal size against body mass for each sex and then determining the predicted body mass of each individual from the regression formula based on the skeletal size of an individual. Condition (index) of each individual is then calculated as the ratio of observed body mass to predicted body mass.

predicted body mass (Y) = [slope of regression x skeletal size (X)] – the constant

condition index = observed body mass predicted body mass

A two factor ANOVA was carried out to assess whether there was variation in body condition associated with macro-habitat type and/or cropping stage. Sexes were analysed separately.

3.3 Results

3.3.1 Trap Success

From May 2004 to April 2005, 290 R. tanezumi were trapped; 138 females and 158 males. Total trap success was 5.03% over 5760 trap nights.

There was no overall macro-habitat effect on percentage trap success, or significant difference between the four pooled replicate transects within each macro-habitat (Table 3.1). Traps success varied with cropping stage, with an indication that there was a macro-habitat interaction (P=0.08 for crop stage x habitat interaction). Trap success was significantly higher during the stubble stage in the rice field habitat. Trap success in scrub and village habitats decreased during the booting to ripening stages (Figure 3.3).

Combined trap success at the transplanted stage, after 11 months of kill trapping, was 5.20% at Poitan and Liwang. The combined trap success (5.83%) was similar at the additional 2 replicate sites (no killing).

Table 3.1 Variation in percentage trap success of Rattus tanezumi in relation to macro-habitat type and rice cropping stage (Results of the split-plot ANOVA).

Source DF Mean Sq F Ratio Prob > F Macro-habitat 2 52.095 2.6948 0.1210 Cropping Stage 5 45.8619 3.3413 0.0119 Pooled Macro-habitat transects 9 19.3318 1.4084 0.2131 Cropping stage* Macro-habitat 10 25.64 1.868 0.0756 Error 45 13.7258

16 b 14 12

10 ab rice field 8 village ab 6 ab a a scrub 4 % Trap Success Trap % 2 0

g le ing dling ring nin e lanted tille lower ripe stubb nsp tra fallow/se oting/f bo

3.3.2 Breeding history of adult females

The percentage of adult R. tanezumi female breeding was significantly different across the copping cycle (chi² = 308.441, p<0.0001). From booting to ripening all adult females were in breeding condition. During the non-cropping stages many adult females were not in breeding condition, particularly during fallow, when nearly 80% of females captured had never bred (Figure 3.4).

At the control sites (no kill trapping), a greater proportion of adult females were not in breeding condition (chi² = 16.718, p<0.0001) (Figure 3.5).

100

60 never bred

40 has bred/ breeding

% Adult Females 20

) ) ) ) ) ) ) 9 0 0 2 7 2 2 1 1 1 (2 (2 ( (10 ( ( g g g g d g n le (31) lin te n tin ri in b low ( d n ri o e n al e la e o e f e p till b w p stub s s o ri n fl a tr

Figure 3.4 Changes in percentage of adult female Rattus tanezumi breeding throughout the rice cropping season (with sample sizes). Monthly trapping data was pooled into cropping stages.

100 never bred 80 have bred/breeding

% Adult Females % Adult 20

no killing kill trapping for 11 months

3.3.3 Pregnancy rates and litter size

The average litter size of pregnant adult R. tanezumi female was 7.45 (n=30). An additional 65 R. tanezumi were captured during preliminary and supplementary trapping, in addition to the monthly trapping in Liwang and Poitan.

Female pregnancy was highest from the booting to ripening stages, peaking during ripening at almost 80% (Figure 3.6). No females were pregnant during the fallow and seedling stages, and few animals were pregnant during the transplanted and stubble stages of the rice crop.

All pregnant females during the stubble stage were in 3rd trimester, suggesting the time of conception would have been during the ripening stage (Figure 3.7). The low percentage of pregnant females at the transplanted stage in 2nd trimester, suggesting time of conception would have occurred just prior to or shortly after transplanting. Given this information the breeding season of R. tanezumi in Banaue is from transplanting to ripening, and the non-breeding season from stubble to the seedling stages of the cropping season. A peak of breeding intensity occurred during the flowering and ripening stage of the crop.

At the most prolific breeding period during the flowering and ripening stages, pregnant females inhabited the rice field and scrub macro-habitats (Figure 3.8). During the stubble stage, at the beginning of the non-breeding season, pregnant females were only captured in the village. Pregnant females were present in the scrub habitat during all rice cropping stages within the R. tanezumi breeding season.

100

20 % Females Pregnant % Females

) ) 9) ) 2 1 2 0 10) 1 (2 (22 ) ( (10) (3 ( g ( g d n g g le e ri tin in b nt o n b a ille o e u pl T B ip St Fallow (17) Seedlin s lowering R n a F Tr

Figure 3.6 Percentage of Rattus tanezumi females pregnant at each stage of the rice cropping season. Numbers in () represent the number of females captured and necropsied.

40 2nd Trimester 30 3rd Trimester

% Females 10

g g le w rin ng o dling ni e lanted ootin wering tubb Fall p Tille B o S Se Fl Ripe Trans

Figure 3.7 Percentage of Rattus tanezumi females in the 2nd and 3rd trimester of pregnancy, at each stage of the rice cropping season. 38

100

80 Village 60 Rice Field

Scrub 40

% FemalesPregnant 0

w ing ing ring ing e en ller oot Fallo Ti B low Stubble Seedling F Rip Transplanted

Figure 3.8 Percentage of R. tanezumi females pregnant, in each macro-habitat respectively, across the rice cropping season.

3.3.4 Body condition

On average, male rats were larger than females in Banaue. Male adults averaged 191.3 g and 191.4 mm head and body length, compared to 170 g and 182.3 mm head and body length in adult females (pregnant females excluded). Body size was a reasonable predictor of body mass, explaining more than 60% of the variance for both males (Figure 3.9) and females (Figure 3.10).

Male condition differed significantly between the macro-habitat types; males caught in the village habitat were in poorer condition that those caught in the rice fields and scrub (Figure 3.11 & Table 3.2). Female condition did not differ significantly between the three macro-habitat types (Figure 3.12 & Table 3.3).

Table 3.2 Variation in body condition of male Rattus tanezumi in relation to macro-habitat type and rice cropping stage (results of the split-plot ANOVA).

DF Sum of Squares F Ratio Prob > F Macro-habitat 2 0.1551 4.4873 0.0128 Cropping Stage 5 0.2042 2.3631 0.0425 Macro-habitat*Cropping Stage 10 0.3089 1.7869 0.0673 Error 152 2.6276

Table 3.3 Variation in body condition of female Rattus tanezumiin relation to macro-habitat type and rice cropping stage (results of a split-plot ANOVA).

DF Sum of Squares F Ratio Prob > F Macro-habitat 2 0.0483 0.9322 0.3966 Cropping Stage 5 0.1435 1.1084 0.3599 Macro-habitat*Cropping Stage 10 0.0968 0.3738 0.9557 Error 115 2.9772

350

300 y = 2.3378 x - 256.21 R2 = 0.6045 250

200

150

100 (g) Mass Body 50

120 140 160 180 200 220 240 Head and Body Lenght (mm)

Figure 3.9 Relationship between skeletal size (head and body length) and body mass in male (177) Rattus tanezumi from Banaue in 2004-05.

350

300 y = 1.9943 x - 193.5 R2 = 0.6793 250

200

150

Body Mass (g) Mass Body 100

50 0

120 140 160 180 200 220 240

Head & Bosy Length (mm)

Figure 3.10 Relationship between skeletal size (head and body length) and body mass in female (148) Rattus tanezumi from Banaue in 2004-05. Pregnant females were excluded. 41

Figure 3.11 Comparison of male Rattus tanezumi body condition between the 3 macro-habitat types, rice field, village and scrub.

Figure 3.12 Comparison of female Rattus tanezumi body condition between the 3 macro- habitat types, rice field, village and scrub.

b 1.1 ab 1.08 ab 1.06 ab 1.04 ab 1.02 a 1 0.98 0.96 Condition Index Condition 0.94 0.92

g ng lin i llow d e fa e tillering stubble s transplanted booting/flower

Figure 3.13 Comparison of male Rattus tanezumi condition across the stages of the rice cropping season. Tukeys post hoc test shows a (transplanted) < b (stubble), where a and b = ab (seedling, tillering, booting/flowering and fallow)

1.18 a a 1.16 a 1.14 1.12 a a a 1.1 1.08 1.06 1.04

Condition Index Condition 1.02 1 0.98

g g g in rin llow dl e e illerin w fa e t lo stubble s /f g transplanted in ot o b

Figure 3.14 Comparison of female Rattus tanezumi condition across the stages of the rice cropping season. 43

The mean body condition of male R. tanezumi was significantly higher during the stubble stage compared to the transplanted stage of the rice cropping season (Figure 3.13). There are no differences in male condition across the other cropping stages. No significant variation in female body condition was detected across the rice cropping stages (Figure 3.14).

3.4 Discussion

There was a strong relationship between rice cropping in Banaue and reproductive activity of female R. tanezumi, highlighting the direct link between human agricultural practices and the potential rate of increase of rodent populations. The breeding season closely corresponded with periods of food availability of rice, from the transplanted to ripening stages of the crop, with a peak on breeding during the generative period of the rice crop (booting to ripening) rather than the vegetative period. This was then followed by a non- breeding season during the rice fallow and the seedling stage. This relationship occurred at both study sites where rice cropping was asynchronous, whereas abiotic factors which might influence rat breeding (e.g. temperature, photoperiod) did not vary. This suggests that food is the main factor determining the onset and length of the breeding season in this agro-ecosystem. Similar findings were reported by Sanchez and Benigno (1985) for Rattus tanezumi in lowland irrigated rice cropping systems in southern Luzon. The breeding season of R. tanezumi in these cropping seasons in Luzon are longer than those reported for Rattus argentiventer in Malaysian (Lam 1983), Indonesian (Leung et al. 1999; Singleton et al. 2004) and Vietnamese (Brown et al. 2006) lowland irrigated rice fields. This suggests that R. argentiventer is not as opportunistic as R. tanezumi in being able to take advantage of invertebrates and grass seeds to breed when the rice crop is not at an appropriate nutritional stage.

Given the timing of breeding activity and to allow a two month delay from birth to young rats entering the trappable population, R. tanezumi denisity in Banaue was expected to peak in the rice field habitat at the ripening and stubble stages of the rice crop. However, trap success was not significantly higher during the ripening stage. Krebs et al. (1994) showed that Mus musculus in the Australian wheatbelt, were less likely to enter traps when wheat was in excess in the vicinity of live traps. A similar situation may have occurred when rice was in excess 45 during this study. In fact, village and scrub trap success decreased during this period, suggesting that even though food may be available in these habitats, R. tanezumi will move into the rice field when an abundance of high quality food is available (Krebs et al. 1994).

Krebs et al. (1994) suggested further that if low trap success is caused by superabundant food, capture rates will increase substantially after harvest when the crop is depleted. In Banaue, trap success was 240% higher in the rice field during the stubble stage, compared to ripening.

Given this tight relationship between crop stage and rat breeding, Ifugao farmers may be able to control rat populations by synchronising their rice crop to limit rat breeding potential. Assuming, R. tanezumi females reach sexual maturity on average at 70 days, in a synchronous system, the R. tanezumi breeding season from transplanting to ripening is limited to 3 months (approximately 90 days), allowing females to produce a maximum of four litters. However, crop development varied by up to six weeks (42 days) at the study sites, increasing the theoretical maximum number of litters to six. Moreover, if cropping is synchronised, females born during the first litter (after 21 days) of the breeding season will probably not reach sexual maturity before the conclusion of the breeding season. However, an extended, asynchronous cropping season would allow females born in the first litter reaching sexual maturity and conceiving before the end of the breeding season. Considering the average litter size in Banaue is 7.5, one adult female in a synchronous cropping season can produce approximately 30 offspring. In the event that cropping has a six week extension, this figure would more than double to 72 offspring in a breeding season. There is also the exponential effect of the females from the first litter contributing to breeding; assuming an even sex ratio at birth, this would result in an additional 27 offspring, or a total of 99 offspring. Therefore a six week extension in the cropping season could results in a 330% increase in the rodent population. 46

The efficacy of methods for reducing pest populations, which rely upon removal of individuals by physical or chemical control techniques, will be affected by the population size at the commencement of the main breeding season. Control will have to run for longer where the breeding season is extended because of an extension in the timing of availability of high quality food and will require more intensive effort and cost because of the higher density of the populations. Introducing control measures when the population is already breeding or conducting episodic rodent controls may not only be ineffective but may even increase the reproductive output of a population (Davis 1987). Some evidence for this was shown in the comparison of the breeding dynamics at the sites where kill trapping and non kill trapping was conducted (Figure 3). A significantly higher proportion of adult females were in breeding condition at the sites where kill trapping was done. It is possible that the monthly removal of adults led to a breakdown in social suppression of breeding. This would not be a problem where cropping was synchronous and rat control widespread.

Reproduction is typically condition dependent, which in turn is linked to food availability (Batzli 1992). The decrease in body condition from transplanting to flowering may be explained by higher densities of rats in the proximity of the rice field during this time or by the transition of energy into increased somatic growth when food first becomes available (Boutin 1990). Increased body condition at the stubble stage may be directly related to the high quality of the ripening grain and the abundant availability of this food during the ripening stage of the crop. Unlike males, significant differences may not have been detected in female body condition due to the variation in their multiple reproductive phases, however, with greater replication these differences may have become more apparent.

Interestingly, all three macro-habitat types (rice field, village and scrub) had the same distinct breeding and non-breeding seasons. This indicates the food in the 47 village and scrub habitats available all year round, is not sufficient (in quality or quantity) to support reproduction at a high level, and the addition of the high quality rice crop is needed to induce a strong pulse in breeding. If rice crops are essential for reproduction, does this mean individual R. tanezumi are required to enter the rice field, during the transplanted to ripening stages in order to reproduce? In chapter 4, I examine whether individuals captured in the village and scrub habitats do enter the rice field to forage during the breeding season. I also examine whether other micro-habitat features influence the movements of R. tanezumi individuals. 48

Chapter 4 Habitat Use and Movement of Rattus tanezumi.

4.1 Introduction

Investigation into the habitat use of vertebrate pests has many conservation benefits. It enables researchers to a) recognise and forecast invasion of natural and agricultural landscapes; b) identify overlaps in habitat use with native species; and c) develop control strategies to mitigate adverse effects of the pest species (Cox et al. 2000). Additionally, the population dynamics of species are often influenced by the spatial arrangement and composition of habitat patches (Walker et al. 2003; Gyllenberg & Hanski 1997). Thus, studying the movement of pests helps build a complete profile of a species’ biology, providing beneficial information when looking to control pest species through specific management actions such as habitat manipulation (Aplin et al. 2003).

The factors affecting habitat use by vertebrates is probably best understood for small mammals. Directly or indirectly, habitat selection by small mammals is primarily influenced by factors relating to access to food and/or shelter (predator evasion) (Lin & Batzli 2004; Aplin et al. 2003; Batzli 1992). These decisions are made at varying spatial scales; the micro-habitat scale reflects small scale variation in food patch quality or shelter from predation, while the larger macro-habitat scale reflects broader variation in the availability of food resources or shelter. Changes in macro habitat quality may stimulate movement of rodents between habitats. This is particularly dramatic in agricultural systems where rodent populations are suddenly deprived of the major food source when a crop is harvested (Aplin et al. 2003).

Pulliam (1988) described the population level consequences of such movement as a source-sink dynamic, when individuals of the same population utilise habitat patches of different qualities. In this model, productive habitat, where breeding is at a higher rate than mortality and where there is a net emigration away from that habitat, is referred to as a ‘source’ habitat. A sink habitat is one replenished through immigration from source habitats, because little or no breeding takes 50

place (Runge et al. 2006; Pulliam 1988; Lidicker 1975). For example, in southeastern Australia wheatfields when there are outbreaks of house mouse, Mus domesticus, populations, there are also irruptions of mouse populations in natural eucalypt woodlands. However, these woodlands are sink habitat because there is little breeding in these habitats and mouse populations increase prior to any breeding there (Singleton et al. 2007).

Source-sink dynamics has proven to be a popular concept and is widely used to describe small mammals population processes within habitat mosaics, but it’s application is not universal. For example, Virgl & Messier (2000) found that annual variation in survival rate in marginal habitat patches (sinks) was explained more by temporal changes in habitat suitability than by density per se, in contrast to a simple prediction of the source-sink model. They found that annual emigration in a muskrat (Ondatra zibethicus L.) population was highest from the more marginal sink habitat and lowest in the principal source habitats. Van Horne (1988) also identified that density can be a misleading indicator of habitat quality. Conclusions about source-sink models may need to be modified to better predict dispersal strategies in environments where annual change in population size is primarily independent of density and, where spatial disparities in habitat quality are not static (Virgl 2000). Further, Morris et al (2004) explained that differences in habitat suitability, differences between habitats in population regulation and, the way that stochastic events alter carrying capacity may all affect the net flow of individual animals from one habitat to another. Therefore, overtime, “preferred habitat” changes as density and population growth vary, and so does the direction of dispersing individuals between habitats (Morris et al. 2004).

Man-made environments such as agricultural ecosystems typically possess a mosaic of habitats at the scale at which small mammal population processes occur. For example, rodent pests persist in a number of varying agricultural 51

landscapes throughout the world, from the wheat belt in south-east Australia, to orchards in Europe, sugar crops in California and rice fields in Asia. These landscapes often contain not only the agricultural crop but may contain remnant, adjacent patches of natural or introduced vegetation, urban development or fallow land. Rodents are known to successfully invade and utilise crop habitats, which provides a major food source supporting dramatic increases in pest rodent populations. However factors influencing their relative use of each component of the habitat mosaic are less well known.

In Southeast Asia, Rattus argentiventer is the major rodent pest in rice agricultural landscapes. R. argentiventer appears well suited to rice field habitat due to its apparent natural preference for waterlogged areas with dense grassy cover (Aplin et al. 2003). In lowland irrigated rice fields it burrows in bunds between fields, banks of irrigation channels and in and around raised vegetable patches from which it can readily invade rice paddies to forage (Aplin et al. 2003).

Rattus rattus Complex, on the other hand is generally associated with village and urban habitats around the world. However, it is present in cropping areas including rice fields and gardens in Asia and the Pacific. Notably, it accounts for less then 10% of rodent captures in agricultural systems where R. argentiventer is present (Cambodia, Vietnam, Indonesia and Malaysia), and where R. agentiventer is absent (Philippines, Laos and Bangladesh) it is often the dominant rodent pest species (Aplin et al. 2003). In Laos R. rattus occurs in an upland rain-fed agricultural system, where it is the dominant pest species in the village and field environments and also occurs in forest-edge habitat. Farmers in Laos have noticed R.rattus has an aversion to entering water, thus damage to rice crops is generally around the edge of paddies only (Aplin et al. 2003).

This study investigates the habitat use and movements of R. tanezumi (R. rattus Complex) in the upland rice agro-ecosystems of the Philippines. In Chapter 3, I showed that R. tanzumi were captured in three macro-habitat types, rice field, 52 village and disturbed vegetation, during this study in Banuae. In forest habitat, native rodents species were captured, however, no R. tanezumi were captured. In this chapter I examine the movement of R. tanezumi between the three macro- habitat types during the breeding and non-breeding seasons and assess whether specific micro-habitat features influence the movements of individual animals. Based on current hypothesis on Rattus rattus Complex habitat use described above, I test the following specific predictions about rodent movements and habitat use in the upland rice terraced agricultural ecosystem of Banaue.

I. R. tanezumi captures are significantly influenced by micro-habitat features at each trap location.

II. R. tanezumi captured in the village and disturbed vegetation habitats enter the rice field to forage during the breeding season.

III. R. tanezumi located in rice fields during the breeding season, move out of the rice field to other habitats after the crop is harvested in search of food.

4.2 Methods

4.2.1 Microhabitat Features

Monthly rat trapping, was undertaken for one year (May 2004 – April 2005) at two study sites (Poitan and Liwang). Traps were placed in the same locations each month in three macro-habitat types 1. rice field, 2. village and 3. scrub vegetation adjacent to rice fields. At each site, 10 traps were set along two transects in each macro-habitat. Every month, habitat attributes were recorded within a 1m diameter at each individual trap location (Table 3.1). These included factors which have previously been found to be associated with micro-scale movements of Rattus species elsewhere (Cox et al. 2000), including potential surrogates for key resources such as food availability and shelter.

A principle component analysis, using JMP statistical package, was undertaken to determine the relationship between habitat attributes (not including presence/absence data *Table 4.1) at trap locations, creating uncorrelated linear combinations of attributes (factors). These factors along with binomial response attributes (presence/absence data) were then modelled in relation to R. tanezumi captures for each month using step-wise regression (JMP). A single analysis which included all months was not possible because of the nature of the habitat attributes, some which varied month to month while others did not. Monthly models with the lowest AIC values identified the habitat attributes and combinations of attributes that best predicted the probability of capturing R. tanezumi.

4.2.2 Spool and Line Tracking

Six adult individual R. tanezumi were spool-and-line tracked at the tillering, booting, flowering and ripening stages of the rice cropping cycle at 2 sites (Liwang and Poitan). Spool and line tracking offers a much more detailed assessment of microhabitat selection made by free-moving animals as opposed to 54 trap based data which only reflects a single movement decision. Rats captured were sexed, weighed and breeding condition determined. Spools were super- glued to the back underfur (in the direct line of the tail) of each animal (Figure 4.2) and held in place until firmly attached, usually after approximately 2 minutes. Each rat was released at the site of capture. The end of the line was tied to vegetation near the trap and marked for future location. On the day following capture, the spool line was collected and at every 5 m interval micro-habitat attributes were assessed (Table 4.1). The collection of a single spool line, including the assessment of habitat attributes took up to 3 hours.

For each individual animal, the mean across the length of the spool line was calculated for each micro-habitat feature, as well as the percentage of spool line in each macro-habitat type (rice field, scrub and village).

Table 4.1 Habitat attributes recorded monthly at each trap location.

Attributes Description

At trap location

Leaf litter depth The depth of the litter layer (cm) was measured within a 1m diameter of the trap location. Understorey density Percent cover of understorey was estimated at each trap location. Understorey The maximum height of the understorey measured in maximum height centimetres. Canopy cover Percent cover of canopy was estimated at each trap location. Canopy maximum The maximum height of the canopy was estimated in height metres at each trap location. *Human refuse Presence/absence of human refuse within a 1 m diameter of trap location. *Ground vegetables Presence/absence of ground vegetables within a 1 m diameter of trap location. 55

*Trees Presence/absence of trees within a 1 m diameter of trap location. *Logs Presence/absence of logs within a 1 metre diameter of trap location.

Distance from trap location to: Irrigation channel Distance, in metres, of an irrigation channel from trap location. Dwelling/animal Distance, in metres, of human dwelling or animal enclosure enclosure from trap location. Rice field Distance, in metres, rice field macro-habitat from trap location. Scrub Distance, in metres, of scrub macro-habitat from trap location. Forest Distance, in metres of forest macro-habitat from trap location.

4.2.3 Radio-tracking

Ten individual R. tanezumi were radio-tracked, five during the ripening to fallow stage of the rice crop (Session 1: Liwang x 3, Poitan x 2)and another five during the seedling to transplanting stage (Session 2: Liwang x 2, Poitan x 3). Rats captured were, sexed, weighed and breeding condition determined. Each rat was fitted with a single-stage (40 pulses per minute) radio transmitter (Sirtrack, New Zealand), attached to a plastic cable tie fitted around the animal’s neck (Figure 4.1). Radio-collars weight averaged 5g, equivalent to <5% of the weight of an individual rat. Prior to release, collared individuals were placed back into the trap and observed for a few minutes to check that the collar did not affect breathing or movement. Once satisfied with the collar attachment, each rat was released at the site of capture.

A TR-4 microprocessor controlled receiver (Sirtrack, New Zealand) with antenna (3 element folding Yagis) was used to track transmitters each with a unique radio 56

frequency. Radio-tracking took place in daylight hours because access during night time was too difficult due to the steep, dangerous topography of the rice terraces. However rats were active during daylight hours and the tracking is likely to reflect both movements between nest sites and movements associated with active pursuits. Each radio-tracked fix location was determined from GPS, and observations including macro-habitat type, whether the rat was active or inactive, rice cropping stage, nest type and nest location were recorded. Home range size for each animal was calculated by in ArcView using “distances between fixes”.

Figure 4.1 Rattus tanezumi with spool and line attached, Banaue 2004.

Figure 4.2 Rattus tanezumi with radio-collar, Banaue 2004. 58

4.3 Results

4.3.1 Microhabitat Features

Five uncorrelated linear combinations (factors) were generated from the principle component analysis of habitat attributes (not including presence/absence data). Factor 1, showed a positive relationship to distance to rice and negative relationships with distance to dwelling and scrub vegetation. Factor 2, showed a negative relationship to the density and height of understorey. Factor 3, showed a positive relationship to canopy cover height. Factor 4, showed a negative relationship to leaf litter depth. Factor 5, showed a negative relationship to distance to irrigation channel. The accumulation these five factors explained 82% of variance in the analysis (Table 4.2).

Table 4.2 Weightings linear combinations (factors) of habitat attributes, determined by a principle component analysis.

Factor 1 2 3 4 5

Leaf litter depth (cm) -0.009 -0.033 -0.009 -0.984 -0.013

Understorey density % -0.113 -0.637 0.126 -0.002 0.154

Understorey max. hgt. (cm) 0.026 -0.517 -0.035 -0.058 -0.019

Canopy cover % -0.119 -0.001 0.594 0.082 0.033

Canopy max. hgt. (cm) -0.047 -0.090 0.578 -0.071 0.109

Dist. to irrigation channel (m) -0.113 0.078 -0.007 -0.009 -0.957

Dist. to dwelling/animal enclosure (m) -0.344 -0.030 0.112 -0.035 0.237

Dist. to rice field (m) 0.487 0.122 -0.090 0.074 0.197

Dist. to scrub (m) -0.417 0.048 0.007 0.088 -0.127

Accumulated % Variance 24 41 59 70 82 59

Table 4.3 Habitat attributes and combinations of attributes that best predict the probability of capturing R. tanezumi, for months June 2004 – April 2005 at two study sites in Banaue (n=371). Values represent P values for parameter estimates of the individual terms in the final model.

June July Aug Sept Oct Nov Dec Jan Feb March April

Factor 1 0.206 0.048 0.002 0.010

Factor 2 0.162 0.045

Factor 3 0.225 0.131 0.078 0.241

Ground vegetables 0.925 0.088 0.048

Household refuse 0.908 0.180 0.107

*Dist to irrigation channel *0.002

*Dist to dwelling/animal enclos. *0.081 *0.066 *0.085

*Dist to rice field *0.187 *0.228

R² 0.118 0.029 0.086 0.059 0.055 0.052 0.178 0.027 0.082 0.036 0.028

In September, October and November, Factor 1 had a significant affect (p<0.05) on the model that predicted the probability of capturing R. tanezumi (Table 4.3). The negative relationship of distance to dwelling/animal enclosure and distance to disturbed vegetation in Factor 1 (Table 4.2), suggests that animals were more likely to be captured closer to these habitat attributes and conversely for the positive relationship with distance to rice field. Presence of ground vegetables significantly affected the probability model in September. And the significance of Factor 2 in February, predicted that captures were more likely where the understorey was less dense and at a lower height.

The inclusion of some factors and stand alone habitat attributes, improved monthly models (Table 4.3) without appearing significant in individual tests of terms in the model (p>0.05). However, in general all models only explained between 2.7% (January) and 17.8% (December) of variation in capture success.

4.3.2. Spool and Line Tracking

Overall, the six spooled animals were tracked in areas with a mean understorey cover of 40% and a low 8% canopy cover. Root ground vegetables were present at 29% of spool locations and on average animals were within 4.6m of a rice field and 8.5m of scrub macro-habitat types. Two animals trapped in the rice field during the tillering stage of the rice crop, were also tracked in scrub macro- habitat type and traveled along irrigation channels. A third animal trapped during the booting stage, remained entirely in the rice field macro-habitat, utilising an irrigation channel to travel between paddies. Both animals trapped in the scrub macro-habitat during the ripening and flowering stages of the rice crop, traveled to rice fields to forage. Fresh rodent tiller damage was observed adjacent to both spool lines. The sixth animal trapped at a village during the ripening stage of the rice crop, traveled to nearby scrub habitat and then into the rice field.

Table 4.4 Spool-and–line tracking results for 6 individual R. tanezumi, Banaue 2004.

Animal A B C D E F Mean

Sex M F M F M F

Macro-habitat @ trap Rice Rice Rice Scrub Scrub Village location Cropping stage Tillering Tillering Booting Flower Ripen’g Ripen’g /month /June /June /June /July /Aug /Aug

Length of spool 70m 55m 80m 85m 140m 75m 84m tracked % spool in rice field 38% 10% 87% 38% 52% 49% 45%

% spool in scrub veg. 54% 30% 0% 62% 40% 23% 34%

% spool in village 0% 0% 0% 0% 0% 30% 5%

% spool in irr. channel 8% 60% 13% 0% 8% 8% 16%

Leaf Litter Depth 1 cm 1.4 cm 0.8cm 1.6cm 1.5cm 0.9cm 1.2cm

Understorey Density 44% 50% 28% 41% 42% 36% 40%

Understorey 44 cm 48 cm 90 cm 72cm 76cm 61cm 65cm max.height Canopy Cover % 13% 0% 0% 1% 19% 15% 8%

Canopy max. height 0.58 m 0 m 0m 0.1m 1.5m 0.6m 0.5m

Dist. to irrig channel 17m 3.3m 19m 20m 24m 11m 16m

Dist to dwelling 388 m 400 m 325m 185m 170m 13m 247m

Dist. to rice field 4.5m 1.6m 0.3m 5.3m 5.9m 10m 4.6m

Dist. to scrub 5 m 11.8 m 19m 3.6m 3.4m 8m 8.5m

Ground vegetables 62% 40% 7% 25% 16% 21% 29% present %

4.3.3 Radio-tracking

Minimum convex polygon home ranges averaged 2.8 ha for animals in both Session 1 and Session 2. Animals averaged 67m between fixes, but individual rats moved distances up to 177 m (rat 5 in session 1). 40% of day fixes in Session 2 were active, compared to 17% in Session 1. Animals were observed swimming in open transplanted paddies for periods of up to 15 minutes as late as 9 am in full sunlight. The number of nests sites averaged higher in Session 1 (2.4), compared to Session 2 (1.2) due to the high percentage of active fixes during Session 2.

Three out of the 4 animals trapped and collared in rice field macro-habitat in Session 1, moved (3-4 week period) from the rice field into scrub or village macro-habitats in the stubble/fallow stages of the rice crop, traveling distances up to 177 m. One of these animals was originally trapped in a rice field at the fallow stage then moved to rice fields that still had ripening grain, before finally moving to scrub habitat when all fields were in stubble or fallow stages. One remained in the rice field habitat continuously. A fifth animal trapped in village macro-habitat remained in the village throughout the period it was radio-tracked during Session 1.

All three animals trapped and collared in the rice field macro-habitat in Session 2, remained predominantly in the rice field from seedling to transplanted stages of the rice crop. One animal did move to the scrub habitat before returning to the rice field. Two animals were trapped and collared in scrub macro-habitat, one remaining in the scrub, the second moving into the rice field during the transplanted stage of the rice crop. 63

Table 4.5 Radio-tracking results for 10 individual R. tanezumi, Banaue 2004/05. *S1 = Session1 and S2 – Session 2.

Animal Date tracked Number of % Fixes Avge.Distance Home Number of fixes active Between Fixes Range Nests

1 7/10/04 – 10/11/04 15 0 3 m - 1 2 7/10/04 – 10/11/04 15 33% 60 m 0.6 ha 3 3 7/10/04 – 10/11/04 15 20% 41 m 1.2 ha 3 4 4/11/04 – 30/11/04 10 10% 81 m 3.6 ha 2 5 5/11/04 – 29/11/04 9 0 133 m 5.9 ha 3 Mean S1 17% 64 m 2.8 ha 2.4

6 6/02/05 – 26/03/05 20 25% 52 m 3.8 ha 3 7 8/02/05 -18/02/05 5 0 69 m - 1 8 10/03/05 – 28/03/05 3 0 50 m - 1 9 10/03/05 – 30/3/05 10 100% 110 m 2.9 ha 0 10 12/03/05 – 30/03/05 8 75% 68 m 1.6 ha 1 Mean S2 40% 70 m 2.8 ha 1.2

Total Mean 27% 67 m 2.8 ha 1.8 64

30 1 Village

20 5 Scrub

10 3 Rice 4

2 0 ripening stubble fallow

Figure 4.3 & 4.4 Schematic summary of habitat utilised by individual R. tanezumi radio- tracked in Session 1 (Figure 4.3), during the ripening to fallow stage, and Session 2 (Figure 4.4), during the seedling and transplanted stage of the rice cropping season. = animal movement between macro-habitats or into a field with a different cropping stage. = animal remains in same macro-habitat, cropping stage may change over this time. *Note: 1. line distance is not representative of the length of time animals were tracked, and 2. cropping was not synchronous between paddies at a site.

Village

20 6

Scrub 10 10 8

Rice 9 7 0 seedling transplanted

4.4 Discussion

Microhabitat features recorded at each trap location had a weak relationship to R. tanezumi captures (Prediction I). Indeed most final models explained relatively little variation in trap success. Although microhabitat assessment is a common approach to measure small mammal habitat choice, it frequently fails to reveal strong relationships. In this study the probable reasons for a lack of strong relationships between microhabitat and trap success include: 1. lack of variation in the features recorded, thus not measuring features that may have had an impact, 2. not selecting features on a small enough scale, 3. baited traps luring animals away from their usual habitat choices (which may be corrected by conducting trapping at a larger scale), and/or 4. the impact of microhabitat features being constrained by other more influential factors such as food, competition and other social interactions.

Spool-and-line tracking results, support Prediction II, by identifying the movement of R. tanezumi from village and scrub macro-habitats in to the rice field during the breeding season (specifically flowering and booting stages of the rice crop). These movements into the rice field may explain why all three macro- habitat types have the same distinct breeding and non-breeding season, that is, R. tanezumi from each macro-habitat access quality food during the productive phases of the rice cropping season (identified in Chapter 3).

R. tanezumi spool-and-line tracked, appeared to have a preference for high percentage understorey cover, canopy cover did not appear to be important and root vegetables were observed to be present at many locations along spool paths (29%) However, this conclusion does not include relative availably of habitats and a more robust assessment for habitat choices of each spooled animal would be gained from comparison of movement paths with random generated paths from the site of capture of each spooled animal (Moura et al. 2005). 66

Radio-tracking results do not conclusively support Prediction III, “R. tanezumi located in rice fields during the breeding season, move out of the rice field to other habitats after the crop is harvested in search of food”. Although there was movement of some animals from the rice field to scrub habitats at the conclusion of the breeding season, these may have been part of their daily home range movements, as shown by spooled animals during the breeding season. Of note, however, was the movement of one animal tracked 177 m in one day to move from the rice field to the nearest village habitat after the rice crop had been harvested. This may suggest a shift of some animals in the population out of the rice field at the conclusion of the breeding season, due to the rice field habitat no longer providing enough food for high densities of R. tanezumi or sufficient shelter. Trapping results in Chapter 3, do show that some R. tanezumi exist in the rice field habitat throughout the non-breeding season.

The data does not show a clear source and sink operating for R. tanezumi in the Banaue agro-ecosystem. Although radio-tracking results show distinct movements of animals across macro-habitat types, breeding occurs in all macro- habitat types, not fitting the source-sink model.

There are limitations in comparing the home-range data collected in this study to other research of the same species, given that only day time radio-tracking fixes were collected. The omission of nocturnal activity results in incomplete home- range data.

4.4.1 Implications to Local Rodent Control Practices

Unfortunately, these radio-tracking and trapping results do not highlight a single specific macro-habitat to concentrate rodent control practices at the optimum time at the transplanted stage of the rice crop. R. tanezumi occurs in all 3 macro- habitats during the transplanted stage, often not burrowing, but nesting or moving in overgrown areas between rice fields and in scrub vegetation during 67 the day. Local farmers currently conduct bank cleaning and scrub burning practices as their primary means of rodent impact control. The results from this study suggest that this would best be undertaken across all areas synchronously just prior to the application of control methods at the transplanted stage of the rice crop, in order to reduce nesting sites and locate burrows.

Another consideration when undertaking control practices, are native species such as Chrotomys mindorensis and Rattus everetii who also occupy scrub and village habitats. To avoid non-target killings of these species, R. tanezumi specific control methods need to be put in place, ruling out the use of non-specific poisons/chemicals. Ideally, if farmers could successfully synchronise cropping, a trap-barrier system (Singleton et al. 2005; Singleton et al. 1998; Brown et al. 2006) would remove any threats to native species. Although not rigorously tested in an upland agro-ecosystem, the spool and radio-tracking data in this study suggests rats are mobile enough for a trap-barrier system to be affective.

Chapter 5 Crop Damage and Yield Assessments.

5.1 Introduction

Rodents are attributed to pre-harvest crop losses in many countries around the world. For example, rodents cause damage to maize and wheat crops in Africa (Rabiu & Rose 2004; Mwanjabe et al. 2002), wheat systems in India (Dubey & Thakur 1999), macadamias in Hawaii (Tobin et al. 1997), sugar beet crops in California (Salmon et al. 1984), orchards in Europe (Pelz 2003) and to the wheat belt in Australia (Singleton et al. 2001). In many Asian countries, rodents are the principal pre-harvest pest in rice crops (Brown et al. 1999), causing 5-10% loss in production in traditional rice farming systems (Singleton 2003a). In Indonesia, the rice field rat, Rattus argentiventer, is ranked the number one pest (Leung et al, 1999), causing pre-harvest losses of approximately 17%, enough to feed 25 million Indonesians for one year (Singleton et al. 1999b).

In the Philippines, R. rattus complex (R. tanezumi), is the major rice pest species in the regions of Luzon and the Visayas, and may reduce rice yield by more than 10%, with localised reports by some farmers of 30-50% annual losses (Singleton 2003a). In municipalities such as Banaue, Ifugao, where rice is grown on a primarily subsistence basis, such yield loss could have a devastating consequence to the livelihood of families. Rice dependence stretches across the Philippines, which must import rice to meet the requirements of its population of 84 million, which is expected to reach 110 million by 2020.

Rodents are a particularly damaging pest because they can attack all stages of the rice crop (Jahn et al. 1999), unlike most invertebrate pests which are more specialised. Diet experiments on captive R. argentiventer (Goot 1951; Murakami et al. 1990) reveal that rice plants at the ripening stage are the most nutritious food for R. argentiventer. The level and intensity of rodent damage varies from year to year and is characteristically patchy. The severity and timing of damage, as well as a particular crop’s ability to compensate (re-grow) will govern the final impact on crop yields (Aplin et al. 2003). Typically, cereal crops, including rice tillers, are 70 capable of regrowth after being cut by a rodent. If cut before the maximum tillering stage, a tiller will be able to produce panicles and in turn rice grain. If cut after maximum tillering, when panicle initiation has started, a tiller will not be able to produce panicles. However, by redirecting resources into other panicles a rice plant may compensate for the damage (Aplin et al. 2003). Brown (2005) found that wheat can compensate for simulated mouse damage (tillers cut by scissors at different crop stages) in an Australian wheat crop. The crop compensated by increasing the number of tillers or survival of tillers remaining after simulated damage was imposed at the emergence stage. However, compensation did not take place when damage was simulated at the booting and ripening stages. Islam (2003) found that R. rattus damage during the reproductive stages of a rice crop, increased the compensation in tiller production. Yield loss was reduced by compensatory tiller production from 58.2 to 42.4% at booting and 47 to 46.8% at the ripening stage.

Cost effective control of damage caused by pests relies upon accurate assessment of pest impacts. It is therefore essential to calculate yield loss caused by rodents in order to quantify the cost-benefit of rodent control programs. Fan et al. (1999), explains that the cost of rodent control (materials and labor) should be less than the yield loss occurring when no rodent control is undertaken. Explaining rodent damage in terms of loss of yield or revenue, may also be a valuable tool in alerting Governments for the need to develop successful rodent control programs to ensure food security.

In Asia, rice is the staple food and in order to meet the needs of four billion people by 2025, Asia’s rice production will have to increase by 70% (Lampe 1993). Implementing effective rodent control programs to reduce current Asian yield loss, in the order of 10%, will make a substantial contribution to reaching these targets. Particularly when increasing yield through intensification of farming by planting rice varieties with short growing seasons, increased 71 cropping intensity, and improved water supply, may benefit rodent pests. Since intensifying rice crop production by 2-3 times per year in the 1990s, a serious rodent problem has developed in Vietnam. Doubling the rice production in the Mekong and Red River Deltas has increased the amount of quality food and the period the food is available, leading to increased rodent reproduction.

In this chapter, I examine rodent damage and associated yield loss in the rain fed, single cropping, upland agricultural system of Banaue, assessing impacts from the booting to ripening stages of the rice cropping cycle. Based on the background information presented above, I test the following specific predictions about rodent impacts on rice.

I. Rodents damage/cut more rice tillers at the booting stage than at the ripening stage of the rice crop. II. Rice tillers are not capable of regenerating productive panicles when cut after the maximum tillering/booting stage of the rice crop III. Rice yield will be greater in areas where rodents have been excluded compared to areas where rodents are not excluded.

5.2 Methods 5.2.1 Crop Sampling Sampling for crop damage by rodents was undertaken on three different occasions in thirteen rice paddies at each site (Liwang and Poitan). Paddies sampled were allocated to one of three levels of rodent damage based on visual assessment. low < 10% damage (5 paddies) medium 10-25% damage (4 paddies) high > 25% damage (4 paddies)

Low intensity damaged paddies did not show any visual evidence of rodent damage. Medium paddies had visible damage, typically represented by small, fragmented clusters of cut tillers. High intensity paddies had large continuous patches of cut tillers.

A transect was set along the longest axis of each paddy. At 5m intervals, five samples (every fifth hill in a row) perpendicular to each side of a transect, were taken (ten in total), recording total tillers, % cut tillers and % regenerating tillers.

30m

10m

Figure 5.1 Crop sampling methodology, where •= sample taken at every 5th hill along a row at each 5m distance across the longest axis of a paddy. 73

The number of hills assessed was different in each paddy due to the irregularity of paddy size.

Spatial and temporal variation in % cut tillers was analysed using a generalised linear model with Poisson distribution using S-plus. An initial visual inspection of the data revealed it was more Poisson than normal due the occurrence of many zeros in the data set.

5.2.2 Total Percentage Damage Estimate

In order to provide an approximate estimate of total damage to the rice crop at a site to help guide management decisions, a visual estimate of rodent damage of each whole site (area of cropped land in each valley) also was recorded at the time of each crop sampling event. This was determined by visually assessing each paddy as low, medium or high crop damage (as defined above) and using a Geographical Positioning System (GPS) to quantify the area of each paddy in relation to the whole site.

A total percentage damage estimate for both sites was calculated at the booting and ripening stages through combining the data at the plot level (quantitative measure of crop damage) with the visual percentage estimates at a landscape level for low, medium and high damaged areas (qualitative measure of crop damage).

Total Damage Estimate (%) = observed visual damage of site x crop sampling data.

5.2.3 Yield measurements

Fenced plots that excluded rodents were used to estimate maximum potential yield of the rice crop. Five 4 m² rat exclusion plots were erected in Liwang (only) at the booting stage of the rice crop. The fences were constructed out of clear plastic and bamboo stakes. Each fence was dug 30 cm into the paddy mud around the entire perimeter, leaving approximately 1 m of fence above the paddy 74

water line. The stakes were erected on the inside of the plastic. The 2 x 2 m fenced areas were free of rat damage at the time they were built.

At the end of the ripening stage, only the central 1 m² of crop within each plot (to minimize fence effects on rice yield) was harvested, weighed and weights standardized for 14% moisture content. These data were used to estimate the potential yield per hectare. Moisture readings of the grain from each sample were taken to adjust weight measurements:

adjusted weight = ((100 - % moisture)/(100 – 14)) x weight at harvest

To estimate yield in rodent affected areas, 100 m² random sample areas were harvested, weighed (moisture reading taken) and the yield per hectare calculated (= actual yield). Large, 100 m² areas were chosen in order to overcome problems associated with the patchiness of rodent damage to rice crops. It was not always possible to harvest 10 x 10 m random sample areas on each occasion due to the small size of some paddies; on those occasions 1 m² samples were measured (Liwang: 7 x 100 m², 3 x 1 m²; Poitan: 5 x 100 m²).

A t-test between actual and maximum potential yield was performed using JMP statistical software.

*Note: Access to paddies to undertake crop damage assessments, erect exclusion fences and take yield measurements was not allowed by some rice farmers. This reduced the amount of samples able to be taken, and did not allow for the erection of exclusion fences in Poitan. Many Ifugao farmers’ pagan beliefs do not allow other people to work in their fields and they understandably were nervous about their crops being inadvertently damaged during the study.

Figure 5.2 Rat exclusion fences, Liwang, Banaue.

Figure 5.3 Cut rice tiller, typical rodent damage. 76

5.3 Results

5.3.1 Crop Sampling

There were more cut tillers in areas that were considered to have more intense levels of rodent damage based on a visual assessment. Damage ranged from 0- 18% of tillers cut in any one paddy and damage was patchy. High damage occurred in the middle of a paddy, leaving a border of undamaged hills around the outside, producing a stadium effect. There was no significant difference in cut tillers between sites, nor any interaction between site and intensity of damage and cropping stage (Table 5.1). However, there was a significantly higher percentage of tillers cut at the booting stage in high damaged paddies. In the low damaged paddies, the percentage of cut tillers was significantly higher at the ripening stage (Figure 5.4)

Table 5.1 Results of the generalised linear model on % cut tillers, using S-Plus. DF F Ratio Prob > F Site 1 2.59 0.12 Intensity 2 27.57 < 0.001 Cropping stage 1 4.99 0.037 Site*Intensity 2 7.50 0.004 Intensity*Cropping stage 2 21.06 < 0.001 Site*Cropping stage 1 0.42 0.523 Paddy (Site*Intensity) 20 5.16 < 0.001

Figure 5.4 Percentage of rice tillers cut at the booting and ripening stage of the cropping cycle, in paddies with low <10%, medium 10-25% and high >25% visual rodent damage.

Liwang Poitan

ripening 21% ripening 33%

booting 67% booting 79%

Figure 5.5 The proportion of the total damage rodents caused to the rice crop at booting and ripening in Liwang and Poitan. Combining the two sites, 73% of damage occurred up to booting and 27% at ripening.

5.3.2 Total Percentage Damage Estimate

Cut tiller (fresh damage) and regenerating tillers (older damage) were combined to calculate the percentage damage estimate (Table 5.2). The percentage damage at the ripening stage is an accumulative figure, incorporating the damage which occurred throughout the cropping cycle up to the ripening stage. Given this, a greater amount of rodent damage occurred at to the booting stage than at the ripening stage at both Liwang and Poitan (Figure 5.5). For example at Liwang, damage at booting = 12.15%, and at ripening = 18.15 – 12.15 = 6% (Table 5.2).

5.3.3 Yield Measurements

Yield varied considerably amongst individual paddies and was strongly negatively related to the number of hills included in the sample (linear regression, r2=0.74). This was largely because the three 1 x 1 m random samples had a greater yield per hectare than the 10 x 10 m samples. This can be attributed to the 1 x 1m samples being in small paddies where damage was typically of low intensity, whereas the larger quadrates were taken where rodent damage was higher. The actual yield for the 2004 rice cropping season at Liwang, was 43% lower than the maximum potential yield calculated from the rodent exclusion plots (Table 5.3).

One of the exclusion plots had a comparatively low yield of 1665.03 kg/ha and had more than twice the amount of hills than the other samples (Table 5.3).

The accumulated damage estimate at Liwang (18.15%, Table 5.2) is around half the percentage yield loss (43%). The value of cut tiller damage at the ripening stage (6%), requires a multiplier of approximately 7 for an estimate of yield loss (43%).

Table 5.2 Percentage estimate of rodent damage to the rice crop up to the booting and at the ripening stages at two study sites in Banaue.

Crop Damage (cut + Visual % damage % Damage regenerating tillers) of Paddies at Site Estimate a b a x b = c Liwang - Booting >25% damage 0.255 30 7.65 10-25% damage 0.100 30 3 <10% damage 0.038 40 1.5 Total = 12.15 Liwang - Ripening >25% damage 0.307 35 10.75 10-25% damage 0.123 35 4.3 <10% damage 0.103 30 3.1 Total = 18.15 Poitan - Booting >25% damage 0.305 40 12.2 10-25% damage 0.133 25 3.33 <10% damage 0.035 35 1.23 Total = 16.76 Poitan - Ripening >25% damage 0.327 40 13.08 10-25% damage 0.153 35 5.35 <10% damage 0.080 25 2 Total = 20.43

Table 5.3 Actual yield (random samples) and maximum potential yield (exclusion fences) calculations for the 2004 rice cropping season at Liwang, Banaue.

Sample Area Number of Hills Yield per Hectare (kg)

Random Samples 1 x 1m 39 4326.62 1 x 1m 35 4387.29 1 x 1m 35 4228.33 10 x 10m 400 1069.53 10 x 10m 361 168.28 10 x 10m 240 2492.59 10 x 10m 238 2006.87 10 x 10m 225 2002.96 10 x 10m 210 1125.43 10 x 10m 272 3365.31 Mean 2797.02 kg/ha

Exclusion Fences 1 x 1m 25 5070.00 1 x 1m 25 8037.00 1 x 1m 56 1655.03 1 x 1m 25 7552.97 1 x 1m 25 2344.47 Mean 4933.89 kg/ha

At Poitan, only three 10 x 10m random samples were taken, with an average actual yield of 881.91 kg/ha.

5.3.4 Photo-points

Photo-points set up to visually assess changes in rodent damage to rice crops in the two study sites revealed substantial rodent damage to rice crops. Photos were taken on four different occasions at each site from the booting to stubble stages of the crop.

a b c

c d

Figure 5.6 Liwang photo-points a booting, b flowering, c ripening, and d stubble.

Rodent damage appears brown when tillers are recently cut in a, the damaged areas regenerate in b, c and d appearing green. The regenerating tillers do not produce panicles (grain) because rodent damage occurred after maximum tillering. 82

a b

c d

Figure 5.7 Poitan photo-points a booting, b flowering, c ripening, and d stubble

As in Liwang, tillers that have been cut by rodents, regenerate, however, do not produce panicles. Plate 4.4 clearly illustrates the “stadium effect” produced when tillers are cut in the middle of the paddy and undamaged tillers remain around the edge.

5.4 Discussion

5.4.1 Crop Damage and Yield Assessment

In the 2004 rice crop at Banaue, there was generally a greater amount of rodent damage at the booting than at the ripening stage; this supported Prediction I. However, in the low intensity damaged paddies there was higher damage at ripening. Typically, low intensity damaged paddies were much smaller in size (fewer replicates) than the medium and high intensity paddies, thus a small amount of cut tillers would show a proportionally higher percentage of damage in low intensity than medium and high intensity. With greater replication of low intensity paddies, this difference may not have occurred. Alternatively, given that low intensity paddies were selected visually by having no obvious damage just prior to booting, then any damage at ripening, in most instances is going to be greater than at booting.

Similarly, studies also have shown rodent damage to rice (Islam & Hossain 2003) and wheat crops (Brown 2005a) is greater during the earlier plant reproductive phases. A possible explanation may be due to the high nutritional value of panicles at the ripening stage (Goot 1951; Murakami et al. 1990), enabling rodents to cut fewer tillers to reach their dietary requirements. One exception is Bandicota bangalensis in Bangladesh and Mynmar, where it causes highest damage to the rice crop at the ripening stage. This species hordes grain in its burrows and often does not cause much damage to the crop until two weeks prior to harvest; it will then carry rice heads to burrows (G. R. Singleton personal communication).

Rice yield was significantly greater in areas where rodents were excluded after maximum tillering, compared to areas where rodents were not excluded, supporting Prediction II. Actual yield was 43% lower than maximum potential yield, highlighting the extreme negative impact rodent pests have on the livelihood of subsistence rice farmers in Banaue. Photo-points at both the Liwang and Poitan study sites, indicate that tillers were not capable of regenerating 84 productive panicles when cut by rodents after the maximum tillering stage of the rice crop (Prediction III). Anecdotal information collected through discussions with farmers, suggested that rice plants may regenerate and produce grain if cut at the early tillering stage, however, do not compensate if cut after booting. Further research is required to identify whether rice plants in the upland environment of Banaue are capable of compensation prior to the booting stage. However, it is unlikely that any such compensation will conversely impact upon damage estimates in order of 15% and yield loss of 43% caused by rodent pests in Banaue.

The photo-points also illustrated the “stadium effect” within paddies of high intensity rodent damage. Similarly, rodent damage studies in lowland irrigated ecosystems in the Philippines (Fall 1977) and in Indonesia (Leung et al. 1999) have reported stadium characteristics, with damage occurring in the centre of rice paddies. Rodents may leave a perimeter of undamaged tillers around the outside of a paddy to act as cover from disturbances from the edge of a paddy, such as human traffic and animal predators. However, the reason for the stadium effect is unclear.

5.4.2 Cost : Benefit of Rodent Control

Having determined crop damage and yield loss in Banaue during 2004, a cost- benefit model for rodent control can be constructed. To ensure a cost effective program, the cost of rodent control should be less than the yield loss occurring when no rodent control is undertaken (Fan et al. 1999).

Cost of Control Yield Loss (M + L) x E x (1 – C) : RI x Y x V M = material pesos/ha RI = rat impact proportion L = labor pesos/ha Y = maximum yield / ha E = efficacy of rat control V = rice value pesos/kg C = compensation of rice plant 85

Based on successful examples in Vietnam (Brown et al. 1999) and Indonesia (Singleton et al. 1998; Singleton et al. 2005), a community rat control program could include the use of trap barrier systems (TBS) (1 per 10 hectares), and a community rat drive incorporating cage trapping around houses and fumigation of rat burrows. In Banaue, the materials for a 20x20m TBS with two spare traps costs 4000 Pesos. Labor cost for construction of a TBS is 600 Pesos and maintenance of 1 hour per day for 6 months, 1800 Pesos. A locally made fumigator costs 1500 Pesos and 10 cage traps another 1500 Pesos, giving a total first season cost, M+L = 3640 Pesos/ha (USD $86/ha). The efficacy of these rat control methods is unknown in Banaue and need to be trialed, however, for the purpose of this exercise E =1. Compensation of the rice crop following rat damage in Banaue is also unknown (C=0), rat impact was 43% in Liwang during 2004 (RI = 0.43); and maximum potential yield (Y) was 4933.89 kg/ha.

Using these factors for managing rodents in Banaue, we can estimate the cost benefit of two scenarios. Scenario 1, where V = 14 Pesos/kg, the lowest market price of rice, representing the minimum cost a farmer would outlay for rice to feed their family. Scenario 2, where V = 30 Pesos/kg, the high potential market value for traditional Ifugao rice.

Cost of Control Yield Loss

Scenario 1 3640 Pesos/ha 29, 702 Pesos/ha 1 : 8

Scenario 2 3640 Pesos/ha 63, 647 Pesos/ha 1 : 17

Given the above costs, a non-chemical rat control program incorporating TBS, fumigation and cage trapping, would be cost effective even if damage is as low as 5% (RI = 0.05). 86

This cost benefit analysis is based on best available information. Given 55% of farmers (72) completing questionnaires in the Barangay of the study sites considered yield loss in 2004 to be low compared to other years (Chapter 5), the RI value of 0.43 can be justified and may even be conservative. Material costs will reduce after year 1 since equipment can be re-used, with only negligible maintenance costs required. The cost of labor in this example is exaggerated, due to the fact many farmers operate on a subsistence basis, that is, they provide their own labor at no cost. These influences on RI, M and L, may compensate for potential increases in the cost of control by the efficacy and compensation multipliers.

Although the use of chemicals such as zinc phosphide may be more cost effective during year 1, the same amount of money must be outlaid each year (unlike non- chemical methods) and the model does not incorporate the potential long term negative effects zinc phosphide may have on non-target species and the environment and the health of the user.

R. tanezumi population growth in Banaue matches the timing of reproductive growth of rice (maximum tillering - ripening). Thus, the timing of rodent control needs to ensure few rodents exist when damage impacts are greatest during the booting stage. As suggested in Chapter 2, undertaking effective rodent control at the end of the R. tanezumi non-breeding season, shortly after transplanting, will ensure rodent numbers are low during the damage prone rice reproductive phases.

Further research is required to trial a range of rodent control methods in Banaue to best maximise cost effectiveness for Ifugao rice farmers. In chapter 6, I examine the knowledge, perceptions and beliefs of Ifugao farmers in relation to rodents and their management, to assist in identifying achievable community based rodent management techniques.

Chapter 6

Beliefs, Perceptions and Practices of Ifugao Rice Farmers.

6.1 Introduction

Technology availability is often not the most important factor for a successful rodent management program. Of equal or greater influence may be the culture of farmers and their socio-economic conditions (Sudarmaji et al. 2003).

Farmers and researchers may have very different perceptions of the natural environment and its interaction with human values. This can create huge setbacks for rodent research, development and extension projects if misunderstandings block exchange of knowledge and ideas between projects partners (Frost & King 2003). To combat this, researchers have emphasised the need to examine the practices, knowledge and beliefs of indigenous farmers in order to assist with the development of rodent management programs (Frost & King 2003; Sudarmaji et al. 2003). In addition, gathering data on the amount of money and time used to control rats aids the analyses of benefits and costs (Tuan et al. 2003) of rat control programs.

The indigenous Ifugao people of Banaue have a culture based on their traditional rice growing practices. Their extensive knowledge of the agricultural and natural environment of Banaue is valuable for any agricultural project because it has been developed in a local context, is generated through experience over time and by trial and error, and it identifies the ideas and constraints of the people who will ultimately use the technologies specific to a project. Frost (2003) lists additional benefits from gathering indigenous knowledge: (1) development of trust towards researchers; (2) providing a platform to express what farmers know can give them confidence to take part in community discussions; (3) integrating farmers’ knowledge into programs can give them the feeling of empowerment; and (4) discussion of knowledge assists farmers to communicate new ideas and may lead to eagerness to test them in the field.

The Philippine Rice Research Institute (PhilRice) conducted a farmers survey (150) relating to pest management in Banaue, Hungduan and Mayoyao 89 municipalities of Ifugao in 1998. In this survey rodents were ranked the number two non-insect pest behind the giant earthworm which causes erosion of the terrace walls. The survey also revealed farmers had limited knowledge of new rice technologies and integrated pest management (Joshi et al. 2000).

In this chapter the perceptions, knowledge and beliefs of 360 Ifugao rice farmers from Banaue Municipality are examined. To expand on the findings of the 1998 PhilRice farmers’ survey, questions were specifically targeted towards rodents.

6.2. Methods

A questionnaire was designed to capture the knowledge, attitude and practice of Ifugao rice farmers in Banaue, Philippines (6.3). Specifically, questions related to rodent damage, yield loss, rodent control methods and farmer perceptions of rodents and their management (6.3).

Three hundred and sixty farmers from five Barangays (=village) in Banaue Municipio participated in the questionnaire, from October to December 2004. The sample size for each Barangay was determined to ensure the total household population was represented with a ±10% precision. Household statistics for each Barangay were provided by Banaue Municipal Hall.

One on one interviews were conducted in the local Ifugao language and lasted 15-30 minutes. To ensure consistency in questioning, only two local interviewers were recruited to complete the questionnaires (Figure 6.1). The interviewers cooperatively translated the material from English to Ifugao. The resident Banaue interviewers and barangay officials played an essential role in encouraging local farmers to participate in the questionnaire. The mix of male and female farmers interviewed was random and not targeted.

The Barangays were pooled in two groups for the examination of some data. Barangays of Bocos, Poitan and View Point (Group 1) apply single cropping rice practices, are located close to the Poblacion (municipal centre), have close 90

proximity to roads and are supplied with electricity. Batad and Cambulo (Group 2), conversely have double cropping rice systems, are remotely located with no vehicular access, do not have electricity and in general follow the traditional Ifugao culture and rice growing practices more closely.

Note: The two study sites for rodent research (Liwang and Poitan) are located in the barangay of Poitan.

Figure 6.1 Jocelyn Lamuton (centre) and Romeo Heppog (right), interviewing a Batad rice farmer.

6.3 Farmer Survey

Name of Respondent: …………………………………………………………………….. Date of Interview: ………………………….Interviewer:…………………………………

I. Farmer Profile 1. Name:……………………………………...………… 2. Age:………………………… 3. Sex: M F 4. Civil Status: Single Married Widow/er Seperated 5. Highest Education Attainment: …………………………………………………………. 6. Main Occupation………………………………………………………………………… 7. Farming Experience (in years): …………………………………………………………. 8. Tenure Status: a. owner b. amortizing owner c. mortgage owner d. renter/lessee e. tenant/shareholder f. other:………………………...

II. Household Profile 1. Household size:………………. 2. Type of Household: Nuclear Extended 3. Number of household members helping in rice farming: ……………………………….

III. Rice Farm and Farming Profile 1. Farm size: ………………………... 2. Cropping pattern: ……………………………… 3. Yield: 2004……………………cav/ha (………kg/ha) 2003……………………cav/ha (………kg/ha) 4. Do you belong to any farm-related organizations? Yes No If YES, what organization?......

IV. Rat Damage History and Characteristics 1. During this years (2004) rice cropping season, was rat damage in your fields low average or high in comparison to other years? 2. Did you observe a significant reduction in yield due to rat damage in your fields this year? Yes No If yes, estimate percent yield reduction…………………………………%

3. At what stage of the 2004 cropping cycle did most rat damage occur? seeding transplanting tillering booting flowering ripening

4. In the past, which years if any, has your crop experienced high rat damage (to help, try and relate it to a significant year in the family’s history)? ………………………………

5. In comparison to nearby paddies, have paddies where you have observed high rat damage mostly been: i. a. small b. average c. large, or d. any size? ii. located a. on the edge (outside) of the terraces b. in the middle of the terraces, or c. in either location? iii. located a. directly adjacent to a major irrigation channel b. away from a major irrigation channel, or c. in either location? iv. located at the a. top b. middle c. bottom, or d. any location (elevation) in the valley?

4. Does rat damage mostly occur in a. the middle b. the edge, or c. in any location within a rice paddy?

5. In your observations have a. early, or b. late developing crops been more susceptible to rat damage?

93 V. Rodent Management Practices 1. What did you do to control rats in your rice fields this year?

Rat Where Method of No. of Hours Money Reasons for Stage of the Rank Management learned (b) Implementation times done Spent Spent using (d) crop (e) Effectiveness Practice (a) (c) last season

(a) 1 trapping 2 bank clearing 3 rodenticides 4 fumigation 5 digging 6 other, specify…………………………………………………………. (b) 1 self experience 2 family 3 neighbour/co-farmer 4 chemical dealer/agent 5 extension and LGU staff 6 training/seminar 7 magazine/leaflets 8 TV/Radio 9 other, specify (c) 1 alone 2 group 3 both (d) 1 high efficiency 2 cheap cost 3 easy to do 4 additional food source 5 environmentally friendly 6 labor saving/use less labor 7 others, specify……………………………………………………………………………………………………………………………………………………. (e) 1 seeding 2 transplanting 3 tillering 4 booting 5 flowering 6 milking 7 ripening

2. If chemicals were used, please fill out the table Name Quantity Unit Cost per unit Total Cost

3. Has rat damaged still occurred when you have undertaken these practices? Yes No 3. Would you prefer to use chemical or non-chemical means of controlling rats? ……………………………………… 4. Would you be willing to participate in community rodent control programmes? Yes No 94

VI. Farmers Beliefs in relation to Rodent Management

For each of the statements below, please indicate the extent of your agreement or disagreement by placing a tick in the appropriate box.

Definitel In most May be In most Always Belief Statement y not cases not true (3) cases true (5) true (1) true (2) true (4) 1. Every type of rat eats palay. 2. Rat control must be done in rice growing areas 3. To maintain rice yield, a farmer must control rats. 4. Because rats are clever, they can never be controlled 5. Rats can cause severe yield loss, if not controlled. 6. Rats can only be controlled if farmers work together with other farmers. 7. Rats can be controlled by individual farmers working independently. 8. The cost of a rat control method can be reduced if farmers work together with other farmers. 9. Rats can be effectively controlled only by the use of chemicals. 10. Using chemical baits to control rats will not harm farmers’ water source. 11. It does not matter whether using chemicals to control rats will harm the environment, just as long as the rats are killed. 12. The effectiveness of a rat control method is more important than its cost. 13. During a severe rat infestation, the cost of rat control methods does not matter to farmers. 95

6.4 Results & Discussion

6.4.1 Farmer and Household Profile

The age of respondents ranged from 18 to 81 years. The higher female representation in the survey is reflective of the greater amount of females who work the rice fields on a daily basis. Farmers’ education level ranged from never attending school to fourth year at college. Household size varied from 1 to 14.

A greater proportion of people in Bocos, Poitan and View Point had an alternative and/or additional primary occupation to farming. These occupations included wood carving, weaving, knitting, driving, non-farm labor, carpentry, tour guide and teaching.

The principal farmers’ organisation of respondents was the BPKI farmers association (80%). Many farmers from the two study sites at Liwang and Poitan belonged to BPKI.

Respondents were generally unable to quantify the size of their rice fields in metric terms, however, explained size in terms of number of paddies and bundles harvested (Table 6.1).

Table 6.1 Summary of Farmer and Household Profile responses from the 2004 Banaue Farmers’ Survey.

Bocos, Poitan & Batad & Cambulo View Point

Number of farmers to 211 149 complete questionnaire

Average age 49 49

Sex 62% female 66% female

Average education level Grade 6 Grade 4-5

Primary occupation 74% farming 96% farming

Average no. of years rice 16 26 farming.

Member of farmers’ 17% <1% organisation

Average household size 6 7

Average no. of household 2.4 2 members who work on rice farm.

Tenure status 49% owner 69% owner 51% tenant 13% tenant 18% owner +tenant

Cropping pattern (yearly) Single double

6.4.2 Rice Yield

The rice yield comparison between 2003 and 2004 varied amongst barangays, some having an overall average increase and others having a decrease in production (Table 6.2). When asked whether rat damage during the 2004 cropping season was low, average or high compared to other years, respondents answers varied greatly within and between barangays (Table 6.3). These results suggest rodent crop damage in Banaue is patchy, where one farmers’ fields may be damaged severely, while a neighbours’ fields may be unaffected.

Table 6.2 Farmers’ response Comparison of yield between the 2003 and 2004 rice cropping season in Banaue.

Bocos Poitan View Pt Batad Cambulo

(68) (72) (71) (77) (72)

2003 rice yield 116 129 106 58 60

2004 rice yield 108 116 95 63 63 (mean bundles per farmer) 2004 % -7% -10% -10% +8% +5% comparison p<0.01 p=0.01 P<0.01 P<0.01 P<0.01 chi²=24.74 chi²=9.92 chi²=46.94 chi²=32.06 chi²=70.22

Table 6.3 Intensity of rat damage during the 2004 cropping season compared to other years, % of respondents.

Rat Damage Bocos Poitan View Pt Batad Cambulo in 2004 (68) (72) (71) (77) (72)

Low 47% 50% 23% 55% 7%

Average 11% 23% 12% 36% 72%

High 42% 27% 65% 9% 21% 98

6.4.3 Rodent Damage Characteristics

Farmers showed a distinct response to the size of paddies most susceptible to rat damage (Figure 6.2) and considered that small paddies were more at risk than large paddies. A large majority of farmers also identified that rat damage occurs in the middle of a paddy (Figure 6.3), supporting “stadium effect” observations in Chapter 5. The farmers’ responses thought that paddies far from a major irrigation channel was a determining feature for the occurrence of high rat damage (Figure 6.4). Paddies positioned in the middle elevation of a terraced valley, were also identified by farmers as most susceptible to high rat damage, compared to the top and bottom of a valley (Figure 6.5). A large majority of farmers acknowledged that crops transplanted late in the cropping season are more susceptible to rodent damage than early transplanted crops (p=1.86E-37, chi²=163.58). This will occur due to an increased rodent density later in the breeding season, and emphasises the need to synchronise cropping to limit the breeding potential of R. tanezumi (Chapter 3).

any location small 22% any size 30% 34%

edge 8%

middle large 70% 10% average 26%

Figure 6.2 Size of paddy most Figure 6.3 Location within a paddy susceptible to rat damage where rat damage occurs. p<0.001, chi²=51.95 (n=1) p<0.001, chi²=223.5 (n=1)

any top any elevation 5% location 16% 25% adjacent 30% bottom 8%

middle far 71% 45%

Figure 6.4 Location of high damaged Figure 6.5 Location of high damaged paddies to major irrigation paddies within a terraced channel. valley. P<0.001, chi²=20.5 (n=1) p<0.001, chi²=491.8 (n=1)

100

6.4.4 Rodent Management Practices

Almost all farmers clear vegetation from the terrace walls around their paddies at different times between the seedling and ripening stages. This clearing is undertaken to reduce the habitat in which rats may harbor close to the rice fields. Fumigation by lighting fires at the base of terrace walls is undertaken mostly in the barangays of Batad and Cambulo. Terrace walls in these barangays are made of stone which are more conducive to forming noticeable crevices rats may use. Few farmers still use traditional Ifugao rat traps, a greater amount apply chemicals as a control method.

57% of farmers applying chemicals used zinc phosphide, 38% of farmers did not know the chemical they used and 14 farmers in Cambulo had applied racumin. Many Cambulo farmers explained that the Municipal Agricultural Officer had provided them with chemicals free of charge. Zinc phosphide was distributed in a plastic sachet without instructions for use. Zinc phosphide has an acute oral toxicity to mammals (including humans), birds, and freshwater fish, and persists under normal environmental conditions for two weeks (ETN 2007). The use of zinc phosphide by farmers in Banaue, is therefore a major environmental and human safety concern.

In Batad and Cambulo 97% of farmers said rat damage still occurs after applying chemicals. 55% of all farmers would prefer to use non-chemical control methods, 5% chemicals and 40% a combination of both.

The timing of application of rodent control methods by Banaue rice famers is widespread throughout the R. tanezumi breeding season, and often undertaken when damage has already occurred. These efforts would be better concentrated at the end of the non-breeding season, just prior to transplanting (Chapter 3).

The major monetary cost of rat control for Banaue farmers was hire of labor for bank cleaning and the purchase of chemicals. 101

Considering the hours and money farmers already commit to rodent control practices, there is a great potential for community rat control programs to be developed in Banaue. The mean 142 Pesos spent per farmer per year (Table 6.4) could contribute to the cost of community trap barrier systems (TBS), fumigators and traps. The initial first season cost of such a program of 3640 Pesos/ha (Chapter 5) could be met by 25 farmers per hectare, or fewer farmers if labor costs are covered by the mean 25 hours per year already committed to rodent control by farmers (Table 6.4). If a community control program is proven to be effective, farmers may be willing to contribute more money, considering few costs are required for subsequent years after initial set up in year 1.

Table 6.4 Rodent management practices of 360 Banaue rice farmers.

Bocos, Poitan & Batad & View Point Cambulo

% of farmers undertaking:

Trapping 1% 13%

Vegetation clearing on bank/terrace 90% 97%

Chemicals 10% 24%

Fumigation 1% 20%

Average time spent in 2004 applying 19 hours 31 hours rodent control measures.

Average amount spent in 2004 282 Pesos 4 Pesos applying rodent control measures.

Willingness to participate in 77% 95% community rat control programs.

102

6.4.5 Farmers’ Beliefs

Table 6.5 The beliefs of 360 Banaue rice farmers in relation to rodents and their management.

% positive % unsure % negative response response response

Every type of rat eats palay (rice). 75 16 9

Rat control must be done in rice 86 6 8 growing areas.

To maintain rice yield, a farmer must 94 6 <1 control rats

Because rats are clever they can never 63 43 9 be controlled.

Rats can cause severe yield loss if not 95 5 <1 controlled.

Rats can only be controlled if farmers 73 23 4 work together with other farmers.

Rats can be controlled by individual 32 6 62 farmers working independently.

The cost of a rat control method can be 60 38 2 reduced if farmers work together with other farmers.

Rats can effectively be controlled only 23 29 48 by the use of chemicals.

Using chemical baits to control rats will 53 20 27 not harm farmers’ water source.

The effectiveness of a rat control 87 12 1 method is more important than its cost.

103

Farmers in all five barangays strongly believe in the need to control rats to increase rice yield as well as the need to work as a community in terms of cost reduction and effectiveness (Table 6.5). This willingness to work together presents the opportunity to facilitate community control actions, such as required for use of TBS technology.

Most farmers believe that all types of rats are pests and many continue to use chemicals even though they consider them to be ineffective. This suggests a need to educate the farming community on rodent ecology and effective non-chemical control methods, including government officials who continue to distribute free chemicals to farmers.

104

Chapter 7

Discussion

105

7.1 Key Results of Study

• R. rattus is the major rice pest rodent species in Banaue. • There is a strong relationship between rice cropping and the reproductive activity of female R. tanezumi. The breeding season corresponds with periods of food availability from the transplanted to ripening stages of the rice crop. The non-breeding season is from the fallow to seedling stages. • R. tanezumi has the same distinct breeding and non-breeding season in all three macro-habitats in which it occurs, rice field, village and scrub. • R. tanezumi were found to move from village and scrub habitats to the rice field during the breeding season. • R. tanezumi still persist in the rice field during the non-breeding season, however, some animals may move out of the rice field after harvest. • The Banaue agro-ecosystem does not show a clear source-sink dynamic for R. tanazumi. • A greater amount of rodent damage occurred at the booting than at the ripening stage of the rice crop. • Rice yield was significantly greater in areas where rodents were excluded compared to areas where rodents were not excluded. • Actual potential rice yield was 43% lower than maximum potential yield in Banaue, 2004. • The cost of undertaking a non-chemical rodent control program in Banaue, is beneficial if rodent damage is 5% or higher. • Farmers believe to increase rice yield rodents need to be controlled, and working as a community will reduce costs and ensure control effectiveness. • Most farmers believe all types of rodents are pests. • Many farmers continue to use chemicals to control rats even though they believe them to be ineffective. 106

7.2 Implications for Other Rice Agricultural Systems

It is hoped that the results from this study will be very useful in the management of pest rodent impact on rice grown in upland environments of south-east Asia, but the implications of this study to other rice systems in the Philippines and south-east Asia are somewhat limited. R. tanezumi in Banaue has a distinct breeding and non-breeding season, unlike R. tanezumi populations 100 km south in the lowlands of Nueva Ecija, where breeding continues all year round in multiple cropping, unsynchronised, irrigated rice systems (pers com. Joshi 2005). Similarly, however, in these rice systems and others (Islam & Hossain 2003) (Khokhar et al. 1993) (Salvioni 1991) (Brown et al. 1999) (Singleton et al. 2005), rodent breeding directly relies on availability of rice crops as food, explaining why breeding activity differs depending on the cropping pattern of an area.

The role of adjacent habitats in rodent damage in the Banaue rice system has also been shown for R. rattus Complex in rice systems in the uplands of Laos (Aplin et al. 2003), macadamia orchards in Australia (White et al. 1997) (Horskins et al. 1998), and small fields dispersed between fallow lands in Tanzania have shown greater rodent damage than large crop monocultures (Mullymaki 1997). These adjacent habitats act as refuges or movement corridors, increasing accessibility to and attractiveness of the crop fields (Fenn et al. 1987) (Brown et al. 2001). In many lowland areas, where rice crops do not have this mosaic of adjacent habitats, a source sink dynamic may exist, where rodents must travel long distances from population sources in order to access the crop during reproductive stages.

The severity of the crop damage in Banaue in the characteristic “stadium effect” pattern is comparable to that reported by R. tanezumi damage in the lowland of the Philippines (Fall 1977), and to R. argentiventer in rice cropping systems Indonesia (Leung et al. 1999). The reasons for such a pattern remains enigmatic. And in southern Laos, reports suggest R. rattus Complex dislikes entering water, 107 such that damage only occurs around the edges of flooded fields, with damage occurring throughout all areas of dried fields (Aplin et al. 2003). Such variability in the spatial aspects of rodent damage, hampers easy predictions of potential yield loss to unstudied areas.

The Banaue results therefore emphasise how the demographics and habitat use of a species varies under different ecological systems and highlights the need for local knowledge in basic research management, supporting the concept of ecologically based rodent management.

7.3 Where to from here?

7.3.1 Management Focus

The key results of this study highlight the need to develop and implement rodent control methods that will not only limit R. tanezumi numbers but which are practicable and financially viable for Banaue rice farmers. I suggest four beneficial areas for further community extension programs which address the most important issues; 1. the differences between rodent species of Banaue (pest and non-pest), 2. the distinct breeding an non-breeding season of R. tanezumi, 3. the optimum time to undertake community rodent control at the end of the non- breeding season (prior to transplanting), and 4. the introduction of available rodent control technologies (such as TBS) and associated cost benefit when applied at a community level.

Fortunately, many of the recommended measures required to limit R. tanezumi numbers, such as synchronising cropping and undertaking community level programs are not unfamiliar in Banaue culture. Traditionally, cropping was strictly synchronised, under the command of the local Chieftain and today many community agricultural programs are developed at the Baranguay level and through local farmers’ associations. 108

Importantly, key figures in the community such as the Municipal Agricultural Officer and Baranguay Captains need to join the ecologically-based rodent management “band-wagon”, to ensure whole of community participation, which is a requirement for successful rodent control programs. Such leaders also need to reassess the free distribution of non-specific chemicals to rice farmers for rodent control, considering the ineffectiveness of these chemicals, their impact on non-target species, the environmental health implications and the general desire of Banaue farmers to use non-chemical control measures (Chapter 6).

Banaue Municipality has received funding and assistance from many foreign and Filipino agricultural aid programs in the past. An apparent skepticism is shown by many farmers who feel that the technologies and benefits of these programs do not reach them or are short lived. Direct beneficiaries of these programs are often families in influential political or government positions. Other programs cease as soon as the aid agency pulls out or financial incentives have dried up. Considering this skepticism, an extension program targeting the wider community is required, with preferably no financial incentives in place, just a clear conveyance of ecologically based rodent management and the economic benefits of applying rodent control at a community level.

7.3.2 Further Research

In order to manage the “whole” rodent population of Banaue, further research is required to understand the diets, competitive interactions and potential facilitating interactions of all rodent species throughout the rice cropping season.

The native rodent species of Banaue probably have a net positive impact on the agro-ecosystem because they prey upon the golden apple snail and giant earthworms, which are both serious pests to rice production. Native species also have the potential to limit the range of R. tanezumi into forest habitats through competitive interactions (Stokes 2006) and may play an important ecological role 109

in forest ecosystems (Dickman 1999). Overlap of habitat use has been shown between R. rattus and Orzomys argentatus in Florida (Goodyear 1992) and between R. rattus and Nesoryzomys swarthii in the Galapagas (Harris et al. 2006), where a decrease in native rodents has been linked to high R. rattus densities. A recent experimental study in Australia by Stokes (2006) showed reducing R. rattus numbers in a native forest resulted in rapid immigration of native Rattus fuscipes matching the densities of R. rattus removed. R. fuscipes then prohibited re-establishment of R. rattus after removal. These potential positive influences of native rodents, highlights the need to research the competitive interactions between all rodent species and to investigate pest species specific rodent control practices, to prevent the non-target killing of native rodents.

The ecological implications of removing R. tanezumi from the Banaue agro- ecosystem also needs to be investigated. R. tanezumi is a predator of the golden apple snail, and if removed from the system, snail numbers may increase. Native rodents could respond to R.rattus removal by increasing their foraging activity in the rice fields due to reduced competitive interactions with R. tanezumi (although my study based on localised removals found no strong evidence to support this hypothesis). Other predator-prey interactions in the agro-ecosystem of Banaue relating to the diet of R. tanezumi, may be unbalanced after removal. It is also possible that R. tanezumi benifit other native flora and fauna species through facilitating interactions. Future work should therefore aim to ultimately include these ecological impacts within a cost-benefit framework when evaluating the total impact of R.rattus control.

110

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