Keywords

3.1 Setting the Scene

Rice agriculture is a staple for over half of the world’s population (Muthayya et al. 2014) and provides wetlands and complex habitats supporting biodiversity. The report from the RAMSAR Convention on Wetlands (RAMSAR 2018) highlighted that 35% of wetlands have been lost since 1970. However, since the 1960s, wetlands associated with rice agriculture have increased by 32% and now form nearly 12% of wetlands globally, indicating the increased urgency for research on existing agricultural wetland systems. Finding a balance, where human population requirements for food, shelter, and health are met without degrading the natural environment, is critical to the health of smallholder agricultural communities (Duru et al. 2015; Tilman et al. 2011).

The current UN Sustainable Development Goals (SDGs)Footnote 1 highlight the need to ensure sustainable food production systems that enable the maintenance of functional ecosystems (Goal 2) (United Nations 2015). Our approach has been to set our sights beyond SDG 2 that focuses on ending hunger and achieving food security via the promotion of sustainable agriculture. Often agricultural scientists are so motivated to achieve food security that they pay insufficient attention to the need to have a living, healthy, and dynamic agroecosystem that promotes floral and faunal biodiversity. Given the documented loss in global biodiversity, especially in tropical zones where most of the world’s rice is grown, we set our sights on achieving both SDGs 2 and 15. Goal 15 emphasizes the need to promote sustainable use of terrestrial ecosystems and halt biodiversity loss (see Barlow et al. 2018). The tropics cover 40% of the world’s landmass and are home to 91% of terrestrial birds and more than 75% of amphibians and terrestrial mammals. Conversely, ecologists, who address SDG 15 in terrestrial agricultural systems, need also to balance their efforts so that delivery of SDG 2 is not compromised.

In this chapter, we review interdisciplinary research over the past decade supported by CORIGAP that focused on assessing the biodiversity of wildlife living in and around irrigated rice lands. We report on research on amphibians, bats, birds, and rodents. Human-wildlife research in agricultural systems has often focused on conflicts between the human and natural world and less is understood regarding the ecosystem services that wildlife provide within the context of agroecology. For example, Tancoigne et al. (2014) found few socio-agroecosystem studies that integrate these linkages with wildlife. Several studies have identified the need for such human-wildlife integration, especially in agricultural systems outside of the developed world (Luo et al. 2014; Stafford et al. 2010). Most of the studies in this chapter identify potential positive ecosystem services provided by wildlife to rice-cropping systems that lead to more sustainable and healthier rice production. In general, this research was conducted in parallel with field trials that applied best management practices for lowland-rice production (see Stuart et al. 2018a, b, Chapters 2.3 and 2.5). The unifying theme of this chapter is to present research supported by CORIGAP that addresses SDG 15 in combination with SDG 2 and to outline a future strategy for mainstreaming biodiversity into rice-based production landscapes.

3.2 Amphibians

3.2.1 Introduction

Amphibians provide several regulatory services including reducing human-insect vector populations and consuming agricultural crop pests (Hocking and Babbitt 2014; Shuman-Goodier et al. 2019; Khatiwada et al. 2016). Because their early life stage is aquatic, they also function as bio-monitors for developmental problems associated with chemical contamination. Recently, studies have determined that the addition of frogs to rice fields can increase yields (Teng et al. 2016; Fang et al. 2021) and may even reduce greenhouse gas emissions (Fang et al. 2019). Over the course of 5 years, we conducted a series of studies on amphibians at the International Rice Research Institute (IRRI) farm near Los Baños, Philippines. Our research involved transdisciplinary investigations that included agronomic, sociological, ecological, biochemical, environmental physiological, and genomic studies. Our results demonstrate that wetlands created as part of rice agricultural systems form a powerful model for understanding how humans interact with modified environments and how sustainable agricultural practices can integrate both human and wildlife needs.

3.2.2 Case Study 1: Differences in Diversity and Abundance of Amphibians Between Conventionally Farmed (Higher Pesticide Use) and Improved-Management (Lower Pesticide Use) Rice Fields

Seven species of amphibians (Fig. 3.1) were observed to inhabit irrigated rice fields at the IRRI experimental farm. These included three native species: Luzon wart frog (Fejervarya vittigera), common tree frog (Polypedates leucomystax), and puddle frog (Occidozyga laevis); and four non-native species: cane toad (Rhinella marina), banded bullfrog (Kaloula pulchra), Chinese bullfrog (Hoplobatrachus rugulosus), and paddy frog (Hylarana erythraea). We undertook surveys to evaluate whether there were differences in diversity and abundance of these species between conventionally farmed (higher pesticide use) and improved-management (lower or no pesticide use) fields at IRRI. The number of adult individuals across all species was higher in the improved-management fields than in the conventional ones with R. marina representing 70% of the observations in the improved-management vs. 30% in the conventional fields (Table 3.1). Surprisingly, diversity was higher in the conventional compared to the improved-management fields (Simpson Index: p = 0.02), However, this outcome may have been a result of us noting that neighboring farmers were hunting frogs for food, including F. vittigera and H. rugulosus, species in the improved-management fields at night.

Fig. 3.1
A photo of 7 different species of frogs. Some of them are Hoplobatrachus rugulosus, Hylarana erythrea, Kaloula pulchra, and Fejervaya vittigera.

Compilation of amphibian species, to scale in reference to each other, observed in rice fields at IRRI’s experimental farm in Laguna, Philippines (photos by Phoebe Shuman-Goodier)

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Table 3.1 Number of adult individuals observed for each anuran species in improved-management (low-pesticide use) and conventional (high-pesticide use) fields at the Zeigler Experimental Farm of the International Rice Reserarch Institute farm, Philippines, in June and July, 2014
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Once we identified the frogs in the rice fields, we determined whether two species, F. vittgera and R. marina, have species-dependent diets with the potential to impact overall pest-control ecosystem services (Shuman-Goodier et al. 2019). The native frog, F. vittigera, ate a high proportion of rice pests, demonstrating that this species has the potential to provide regulatory ecosystem services. However, the diet of the invasive cane toad (R. marina) was replete with the predators of rice pests. These results suggest that F. vittigera may provide pest-control services, while the larger numbers of R. marina individuals in rice fields, throughout many of the islands of the Philippines, may lead to increased numbers of rice pests resulting from lower predator availability. While this outcome was surprising, it suggests that working with farmers to integrate conservation practices in parallel with their economic and food-resource needs may simultaneously provide benefits to both the farmers and the rice agroecosystem.

3.2.3 Case Study 2: Tadpoles as Bio-Indicators for Effects of Current-Use Pesticides on Vertebrate Physiology, Behavior, and Species Interactions

Environmental contaminants, including pesticides, have been identified as a contributing factor in global amphibian declines (Blaustein et al. 2003, 2011; Hayes et al. 2010). Several studies have identified effects relevant to rice ecosystems (Nataraj and Krishnamurthy 2020; Thammachoti et al. 2013; Shojaei et al. 2021). Because amphibians that live in rice ecosystems are exposed to herbicides and insecticides during sensitive life stages, such as development and reproduction (Fig. 3.2), they can be studied to identify chemicals that cause adverse physiological effects. In addition, because vertebrate endocrine systems and the physiological mechanisms that underlie development are highly conserved, these effects may translate to potential harbingers for human health.

Fig. 3.2
4 photographs. First. There are 2 light-shaded eggs hidden inside the young rice plants. Third. There are several tadpoles that are swimming in a flooded area. Fourth. There is a Hylarana erythraea in the wet paddy field.

Examples of the amphibian life stages observed in irrigated rice fields, which include eggs, larvae, metamorphs, subadults, and adults. Top left: two foam nests on a rice field bund that contain eggs produced by Polypedates leucomystax. Top right: Fejervarya sp. egg mass attached to a submerged rice plant leaf. Bottom left: Rhinella marina tadpoles swimming in a flooded rice field. Bottom right: an adult Hylarana erythraea documented the morning after a night-time breeding chorus (photos by Molly Shuman-Goodier)

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Through a series of experiments and surveys conducted at the IRRI farm in the Philippines, we demonstrated that wild amphibian tadpoles can be used to screen for effects of current-use pesticides on vertebrate physiology, behavior, and species interactions (Shuman-Goodier et al. 2017, 2021). Specifically, we found that a commercial herbicide formulation of Butachlor, Machete EC, can cause endocrine disruption at an environmentally relevant concentration (0.002 mg/L) and alter competitive interactions between invasive (cane toad, R. marina) and native (Luzon wart frog, F. vittigera) species. We also propose that the cane toad is an ideal candidate for monitoring pesticide exposure in rice in rice-growing countries where it has been previously introduced. The species is abundant, sensitive to chemical exposure, and has extensive reference resources (e.g., annotated genome).

3.2.4 Case Study 3: Knowledge, Attitudes, and Practices of Farmers with Regard to Amphibians That They Find in Their Fields

Throughout the centuries, amphibians have provided human populations with important ecosystem services relating to food, economic, and even cultural resources (Crump 2015). In 2014, we surveyed and interviewed 22 farmer owners, managers, laborers, and tenants regarding their knowledge, attitudes, and practices of the amphibians that they found in their fields (Propper et al. 2020). We found that nearly half of the surveyed farmers thought there was a decline in amphibian populations and two-thirds believed that pesticides have a negative effect on individual animals. Farmers mentioned seeing dead and fewer frogs in the fields after spraying and some lamented that, in recent years, there are fewer frogs in the fields to use as a food resource. One farmer worried that neighbors may be catching animals contaminated with pesticides and selling them at local markets. These results suggest that farmers are aware of the impact of pesticide exposure on the frogs in their fields while simultaneously demonstrating that frogs are both an economic and provisioning resource.

Farmers also expressed other perceptions of the potential ecosystem services the frogs in their fields provide. Many of the farmers agreed that the frogs eat the insects in their fields and that these animals provide pest-control services. Some farmers also mentioned that there has been a reduction of frogs calling in their fields and that they miss the “singing,” indicating that there are some cultural services provided by the animals. Another potential service the farmers noted was the belief that the tadpoles deliver nutrients to the soil.

3.2.5 Integration of Key Findings on Amphibians

Rice agroecosystems around the globe may play a key role in maintaining local amphibian populations that provide ecosystem services to the environment and to the farmers managing their fields. Our research at IRRI supports the hypothesis that frogs in this tropical-farming system provide regulatory, provisioning, and cultural resources to farmers. Recent other studies in China demonstrate the potential for complex-scaled interactions between frogs and the rice ecosystem. Fang et al. (2021) found that higher frog abundances in rice fields indirectly reduce methane gases emanating from rice fields by increasing both rice root porosity and oxygen secretion. Together, our studies and others demonstrate that amphibian conservation practices combined with optimizing farmers’ needs for economic, food, and health security may lead to the development of a shared-goals approach for more sustainable rice production.

3.3 Bats in Rice Ecosystems

3.3.1 Introduction

Rice-growing landscapes offer foraging opportunities to bats and ecosystem services to people; however, unsustainable practices within and outside rice-growing areas, such as cave disturbance and limestone quarrying, habitat loss, pesticide and herbicide use, and hunting, threaten this mutualistic relationship and contribute to the decline of bat populations (Kingston 2010; Voigt and Kingston 2015; Furey et al. 2016; Toffoli and Rughetti 2017; Costantini et al. 2019). If we are to maintain this mutually beneficial relationship with bats, we must learn to identify the precise role of our key bat collaborators and adopt management practices that allow them to thrive.

3.3.2 Case Study 1: Bat and Insect Activity at IRRI

Despite the potential benefits of and threats to bats, information on the species utilizing rice-dominated landscapes as a foraging habitat in Southeast Asia is sparse. To begin filling this gap, between 2014 and 2016, we sampled bat activity acoustically and through mist-netting and roost searches within, and in the vicinity of, the IRRI farm (Sedlock et al. 2019). The Makiling Forest Reserve lies adjacent to the farm and is one of the most studied bat assemblages in the country (Sedlock 2001; Ingle 1992) that provides baseline information on species present in the area and an echolocation call library for identifying passively recorded calls (Sedlock 2001). We assessed the extent to which bats were tracking aerial-insect abundance on the farm by simultaneously sampling bats and insects. Insects were sampled using large hoop nets mounted on a truck that was driven along transects (Fig. 3.3A). We acoustically monitored bat activity simultaneously over early and late tillering growth stages to reveal whether bats were tracking early colonizers, such as aquatic-emergents (e.g., midges, mosquitoes) or herbivores (e.g., planthoppers, stemborers) that arrive at later crop stages. Finally, we acoustically monitored bats from 50-m radio towers on the farm to compare the diversity and activity levels of bats immediately above the rice to that at higher altitudes (Sedlock et al. 2019).

Fig. 3.3
a to e. 5 photographs present a bat on the top of a four-wheeler and 4 different species of bat. f. and g. 2 scatter plots and a line graph plot S q r t versus 1700 H to 0500 H. It plots a curved line that initially rises, falls, and then increases again. The values are plotted along the line.

Bat and arthropod sampling on the Zeigler Experimental Farm of the International Rice Research Institute, Philippines. Nets mounted on a pickup truck passively sampled aerial arthropods along a driven transect (A). Representative bats captured within the farm and acoustically sampled, include Myotis rufopictus (B), Miniopterus australis (C), Taphozous melanopogon (D), and Scotophilus kuhlii (E). Relative abundance of insects captured (F) and bat calls recorded (G) during each of four driving transects across the night (Photos by Jodi Sedlock)

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3.3.2.1 Key Findings

We documented 11 bat species on the farm; the most abundant species living and foraging within the farm were the Asian house bat (Scotophilus kuhlii) (Fig. 3.3E), the Javan pipistrelle (Pipistrellus javanicus), and the black-bearded tomb bat (Taphozous melanopogan) (Fig. 3.3D). Conspicuously absent was the wrinkled-lipped bat (Chaerophon plicatus), an ecologically and economically important consumer of brown planthoppers in Thailand (Srilopan et al. 2018). Nevertheless, our data provide evidence of a rich bat community supported by the rice ecosystem and the surrounding landscape and potentially serving as natural enemies to rice-associated pests.

Our simultaneous bat and insect sampling, while not definitive, provides strong evidence of prey tracking by bats on the farm (Fig. 3.3) and echoes the pattern of bat and insect activity documented with Lidar technology over a Chinese rice paddy (Malmqvist et al. 2018). Moreover, most of the insect species we captured were decomposers (70%) during part of their life cycle, over 90% of these were flies (including biting midges, mosquitoes, etc.); 22% of captures were herbivores (including important rice pests such as planthoppers and leafhoppers (nearly 10% of captured herbivores); and the remaining 8% of captures included parasitoid and predatory insects and spiders. Additionally, over two rainy seasons of acoustically sampling bats simultaneously in early and late tillering fields, we found that the most recorded species, the Asian house bat and the Javan pipistrelle, foraged more over early tillering than late tillering fields when rice herbivores are most abundant (Fig. 3.4) (Sedlock et al. 2019). Therefore, the most conspicuous and abundant bats foraging immediately over irrigated paddies at IRRI are potentially critical in their consumption of disease vectors (mosquitoes). Molecular analysis of bat diets in a rice-growing region of Spain confirmed the consumption of dipterans (Puig-Montserrat et al. 2020), which underscores bats’ role as natural enemies in rice agroecosystems worldwide.

Fig. 3.4
2 photographs present rows of young plants in the wet field, which is labeled early tilering, and a crop field labeled late tilering. A scatter plot and a line graph of bat passes from 0 to 300 versus 1800 H to 0500 H. It plots 2 curved lines and vertical scatter spots throughout the x-axis.

Acoustic activity of aerial-hawking bats over paired early and late tillering plots at the Zeigler Experimental Farm of the International Rice Research Institute, Philippines. Each data point represents total bat passes during a 1-h sampling period in August 2016

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Bat species whose flight morphology and echolocation call design allow them to forage closer to vegetation, such as Myotis rufopictus (Fig. 3.3B) and Rhinolophus macrotis, were active throughout the night and over all sampled rice-growth stages. Lacking a dusk and dawn peak in activity that is apparent for the Asian house bats that track the nightly activity pattern of aerial insects—these bats may be more important as consumers of moth pests, such as stem borers and armyworm moths that alight on vegetation. Adept at flying and detecting prey near and on vegetation, these species may exploit eared noctuid (armyworm), pyrallid (stem borer), and arctiid moth pests that evade most bats by flying close to vegetation and that respond to rapidly approaching bats with evasive maneuvers and, in some cases, ultrasonic clicks of their own (Hofstede and Ratcliffe 2016). In Thailand, Myotis horsefieldii, a species that is present in the IRRI area and similar to M. rufopictus, was the most commonly recorded bat at ground level in a rice-dominated area of central Thailand (Nguyen et al. 2019).

3.3.3 Case Study II: Free-Range Bat Guano Farming in Cambodia

Insectivorous bats produce nutrient-rich guano that is highly valued as a plant fertilizer by farmers in Southeast Asia (Thi et al. 2014; Furey et al. 2016). The guano is typically sun-dried in places where it accumulates beneath the roost sites, then collected and sold. Monthly incomes for farmers employing traditional roost structures (Fig. 3.5) in the Kandal and Takeo provinces of Cambodia range between US$6–22 per roost with numbers of roost per farm ranging from 1 to 20 (Chhay 2012), whereas farmers employing stilt-house roost structures in Soc Trang province in Vietnam (Fig. 3.5C) earn between US$130–215 per roost (Neil Furey, unpubl. data). This farming practice provides a valuable source of income for smallholders in both countries. In addition to the environmentally friendly and nutrient-rich fertilizer provided by the bats (Thi et al. 2014), they undoubtedly help to protect rice crops in the surrounding landscapes by suppressing insect pests (Wanger et al. 2014; Kemp et al. 2019; Puig-Montserrat et al. 2020). It is also possible that this service may contribute to reducing the need for pesticides, although this has yet to be studied in Southeast Asia. To investigate the role that free-range bat guano farms in Cambodia play toward biological pest control in rice agroecosystems, a study was conducted by researchers from the Royal University of Phnom Penh that aimed to quantify bat activity over rice fields surrounding bat farms and evaluate threats to bat populations in this area (Pisey 2017).

Fig. 3.5
3 photographs of a row of tall trees, a composite structure, and a stilt house, respectively.

Roost structures employed by free-range bat guano farms in Cambodia and southern Vietnam. (A) traditional roost structure, Kandal province, Cambodia (photo by Neil Furey), (B) composite structure, Kampong Cham province, Cambodia (photo by Julia Guillebaud), and (C) stilt-house structure, Soc Trang province, Vietnam (Photo by Neil Furey)

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3.3.3.1 Key Findings

Results from interviews with bat and rice farmers in the study landscape suggest that bat populations had declined within the study area over the previous 10 years, with loss of palm tree roosts, hunting of bats for consumption, and high-pesticide use identified as possible causes. However, initial results from acoustic analysis revealed that free-range farming of lesser Asian house bats enhanced bat activity over nearby rice fields compared to those further away (Pisey 2017). These findings suggest that, in addition to supporting local bat populations through increased roost availability, the bat farms likely benefit nearby rice farmers. Efforts to address anthropogenic threats to bats, such as high-pesticide use, are clearly needed (Stechert et al. 2014) to ensure the sustainability of bat farms and avoid further declines in Cambodian bat populations and the ecosystem services they provide.

3.4 Birds

3.4.1 Introduction

Birds provide a great opportunity to study the interaction between biodiversity and agriculture. They are relatively easy to survey, identify, and record, and are wide-ranging and can respond rapidly to changing ecological factors. Recent attention has been given to studying the occurrence of bird species within rice fields, but these are often disproportionately represented by studies from Europe or the USA (Elphick et al. 2010a). Asia produces the largest quantity of rice in the world, but studies on birds in rice landscapes within Asia are within their infancy (e.g., Bourdin et al. 2015) and generally concentrate either on single species ecology or in the pursuit of reduced food damage during production (Lane et al. 1998; Borad et al. 2001; Takahashi and Ohkawara 2007; Smedley 2017).

There is a clear need to expand current knowledge about the avian biodiversity that uses rice fields (e.g., Bourdin et al. 2015). Long-term assessments of bird populations within lowland irrigated rice fields can provide an important foundation to identify general trends and establish a baseline that can be used to measure changes over time. The case study presented below covers two seasons and provides an indication of how changes in cropping systems in lowland irrigated rice systems can influence avian biodiversity in one of the dominant agroecological landscapes in the Philippines.

3.4.2 Case Study: Four Versus Five Crops Over 2 Years

Consisting of over 7,000 islands, the Philippines is one of the most avian-diverse countries in the world and has been identified as a biodiversity hotspot of conservation importance (Balmford and Long 1994; Myers et al. 2000). In 2020, the Philippines produced 19 million t of rice (FAOSTAT 2022), but currently relies on imports to supply the demand for its population. To avoid further loss of natural wetlands to agriculture, methods of producing more rice per unit area of existing agricultural land might be one solution to supply the increase in food demand, while maintaining uncultivated land to support local biodiversity.

In the Philippines, lowland irrigated rice fields typically produce two rice crops annually although this is dependent upon location and available water supply (GRiSP 2013). In 2012, the Philippines government encouraged farmers to intensify their production of lowland irrigated rice. Large-scale trials of crop intensification were conducted using selectively bred rice varieties that have a shorter maturation period, enabling smallholder farmers to grow five rather than four crops every 2 years.

Studies from countries that adopt a single annual-cropping practice, such as Europe and the USA, have shown that, with careful management of the fallow period (time between cropping seasons), rice fields can support an impressive range of bird species (Elphick et al. 2010b; Stafford et al. 2010). In the Philippines, this fallow time is already reduced but with further intensification, what would be the impact on bird species that are currently found within this agricultural landscape? As part of a broader research program on avian diversity of rice fields within the Philippines (Smedley 2017), avian biodiversity was monitored in rice fields, trialing the intensified system of five rice crops over a 2-year period (5-in-2) and compared to the traditional four crop model (4-in-2). Surveys commenced once the crop stage became unsynchronized, as the intensified “5-in-2” sites were harvested but the traditional “4-in-2” were still at the maturity stage. The study was conducted in Isabela province, northern Luzon, where this intensified method of farming had been adopted for the first time. Monthly bird surveys to record the diversity and abundance of species seen and heard were conducted at all sites to provide direct comparisons between the two cropping practices (Table 3.2). Two rice fields, each approximately 10 × 50 m in size, were surveyed at each site with results pooled during analysis, further details of which can be found in Smedley (2017).

Table 3.2 Diversity of bird species and mean number of individuals recorded per site per species during the 15 months of data collection between an intensified cropping system (5-in-2) and a traditional cropping (4-in-2) one. Surveys were conducted at two replicate sites per cropping method. Cumulative number of individuals recorded over the 15 months is given in parentheses. Sixty surveys were conducted per site. Common names which end with “(sp.)” represent records that were identified to the family level only. Species are from the Checklist of the Birds of the Philippines (Jensen et al. 2019)
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3.4.2.1 Key Findings

Over the whole survey period, more individual birds were observed within the 5-in-2 fields (n = 5,419) than in the 4-in-2 fields (n = 4,263). This was mainly due to the larger number of Eurasian tree sparrows recorded (5-in-2: n = 1,594, 4-in-2: n = 839), which is likely due to the increase in the amount of time that the rice fields have available grain (i.e., food for Eurasian tree sparrows), both while the crop is maturing and via grain spilled during harvest. In contrast, the total number of water bird individuals recorded in the 5-in-2 fields (mean = 356, range = 335–377) was substantially lower than in the 4-in-2 fields (mean = 546, range = 511–581). This outcome is most likely due to the shortened interval between planting and harvest in the 5-in-2 fields, compared to the 4-in-2 fields, which reduced the duration of preferential wet conditions and vegetation cover per cropping season. Generally, a similar number of species was observed in the two cropping systems (Table 3.3), which suggests that the change from 4-in-2 to 5-in-2 had little effect on the overall avian diversity during the survey period.

Table 3.3 Mean number of species recorded between an intensified crop (5-in-2) and a traditional crop (4-in-2), across four fields at two sites per cropping method. Species categorization of all birds, including those only identified to family level, during the 15 months of data collection. Cumulative number of species recorded per site is given in parentheses. Sixty surveys were conducted per site
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These field results provide useful insight into the likely response of the avian fauna to the adoption of an intensified cropping system in the Philippines. If such intensification of rice cropping was adopted nationwide, then we predict a reduction of water bird populations but a substantial increase in the number of Eurasian tree sparrows. This, in turn, would require an increased need for measures to control Eurasian sparrow populations in 5-in-2 rice-cropping systems. The findings provide key insights into the potential major changes in avian biodiversity because of large-scale agricultural intensification and highlights the need for further studies to understand the long-term effects.

3.5 Rodents

3.5.1 Introduction

Rodents cause substantial losses to cereal production globally (Meerburg et al. 2009a) and are carriers of human diseases that have major health impacts in rural communities (Meerburg et al. 2009b). In Asia, losses caused by rats to rice production is a major economic burden to smallholder farmers (John 2014) and can lead to severe impacts on food security in years when regions encounter severe population outbreaks of rodents (Singleton et al. 2010; Htwe et al. 2013).

The pest species of rats and mice belong to the order Rodentia. Hence the term “rodents.” There are approximately 2,552 species of rodents, which constitute about 40% of known mammal species (Burgin et al. 2018). Rodents therefore play a crucial role at an ecosystem level (see Dickman 1999). Widespread use of poisons to control pest species of rodents in agricultural systems do not discriminate between pest and non-pest rodents. The positive ecosystem services provided by the latter can therefore be severely diluted. This is of major concern given that less than 10% of rodent species cause significant negative impacts to rice and other cereals in Asia, Africa, and other continents (Singleton et al. 2007). We need to take positive efforts to protect the other 90% of rodent species. In this section, we provide case studies of the potential benefits that native non-pest rodent species can provide to farmers in the Philippines.

Also, rodent pests have been identified as a key factor that can influence whether a farmer adopts certain best practices for rice production. As described in Chap. 4, the implementation by smallholder farmers of alternate wetting and drying (AWD) of their rice crop will substantially reduce methane gas emissions (Lampayan et al. 2015). Many farmers, however, are concerned that drying their crop mid-season will encourage rats to enter their crop and will lead to significant economic damage to their crop (Rica Flor, pers. comm.). We briefly summarize a study that examined whether famers in Indonesia and the Philippines have a legitimate concern of increased rodent damage associated with the adoption of AWD.

3.5.2 Case Study 1: Rodent Diversity in the Philippines

The Philippines is an oceanic archipelago that is recognized for its high rodent diversity and endemism with over 72 murid rodent species described (Heaney et al. 1998; Rickart et al. 2019). Of these, only six are considered pests. These are also non-native in origin and tend to thrive in habitats that have been heavily disturbed by humans, such as agricultural and urban habitats, whereas the native species live predominately in natural forest (Heaney et al. 2016). However, in diverse agricultural landscapes that are commonly found across the Philippines and include a mixture of habitats such as agroforest, grassland, riparian, rice and various other crops, both native and non-native rodent species coexist (Heaney et al. 2005; Stuart et al. 2008). On Luzon Island, these species commonly include the endemic non-pest species Rattus everetti (common Philippine forest rat) and Chrotomys spp. (striped shrew-rats) and the invasive pest species Rattus tanezumi and Rattus exulans.

Interactions of rodents with the ecosystem are diverse, often complex, and not always apparent. These interactions are often overlooked when applying control measures against rodent pests. To better understand the ecology of the native rodents in complex rice-based agricultural landscapes of the Philippines, two studies were conducted—one in the upland rice-based agroecosystems in the Ifugao Rice Terraces (IRT), northern Luzon (Stuart et al. 2007) and another in the lowland rice-based agroecosystems of the Sierra Madre Biodiversity Corridor (SMBC), northern Luzon (Stuart et al. 2008). In both studies, Chrotomys spp. were trapped within rice fields. Stomach-content analysis and spool-and-line tracking provided evidence to support previous suggestions that they prey on golden apple snails (Pomacea spp.), a major invasive pest of young rice seedlings. In addition, in the IRT, Chrotomys spp. were confirmed to feed on large non-native earthworms (Pheretima spp.), another major pest that causes water seepage and erosion due to their deep-burrowing activities through rice terrace walls (Joshi et al. 2004).

In both the upland and lowland sites, another native species, R. everetti, was trapped in high numbers in the forest and agroforest habitats adjacent—or in close proximity—to rice fields, but few were trapped in coconut groves or rice fields. On the other hand, the abundance of R. tanezumi, a non-native pest species, was substantially lower in forest and agroforest habitats than in the more disturbed rice field and coconut-grove habitats. Due to the close proximity of agroforests to rice fields and their similarity in habitat complexity to coconut groves, the findings suggest that R. everetti may inhibit R. tanezumi from establishing in forest and agroforest habitats.

To further examine this, we conducted a 6-month experiment that involved monthly trapping and removal of R. everetti individuals from two replicate agroforest grid sites over a 3-month period to study the effects on the R. tanezumi population ecology and habitat use (Stuart et al. 2016). The findings from this study indicated that R. everetti has a negative effect on the reproductive activity and survival of R. tanezumi and influences the microhabitat use of R. tanezumi through interference competition with the larger R. everetti competitively dominant over R. tanezumi. In addition, there was a significant difference in the use of canopy cover between these two species irrespective of the treatment. R. everetti selected a microhabitat with denser canopy whereas R. tanezumi selected a microhabitat with less canopy cover, which is indicative of a severely disturbed habitat with few trees.

3.5.2.1 Key Findings and Conclusion

The native species of rodents on Luzon Island, Philippines, provide important beneficial ecosystem services to rice-field ecosystems.

3.5.3 Case Study 2: Does AWD Increase the Risk of Rodent Losses?

Rice farmers in Vietnam (Rica Flor, pers. comm.) and the Philippines (Richard Smedley pers. comm.) expressed concern that intermittent drying of the fields will attract more rats to growing rice, thereby causing more damage to the crop. However, spatially and temporally replicated damage assessments done on AWD and control fields in Indonesia and the Philippines demonstrate that rodent-pest damage levels on standing rice crops were not affected by the water management scheme employed (Lorica et al. 2020). AWD assists the rice plant as it grows, as previous studies from Gambia, India, Thailand, and China indicate (Ceesay 2004; Gani et al. 2002; Mishra and Salokhe 2011; Pan et al. 2017), which may translate to better compensation in the event of rodent-pest depredation.

AWD also had no significant effect on the breeding performance and population dynamics of Rattus argentiventer in Indonesia and R. tanezumi in the Philippines (Lorica et al. 2020). Breeding of R. argentiventer is synchronized with the growth stages of rice (Brown et al. 1999; Jacob et al. 2003; Leung et al. 1999; Tristiani et al. 1998), while available resources dictate breeding by R. tanezumi (Htwe et al. 2012). Likewise, rodent activity and movement, examined using spool-and-line tracking, was not influenced by water level (Lorica et al. 2020). Both species tended to use the rice paddies over bunds regardless of water level indicating that something other than water affects their habitat use. We conclude that perceived risk of predation, not water, influences habitat use (Jones et al. 2017).

In the Philippines, a post-project survey of knowledge, attitudes, and practices (KAP) of farmers indicated that there was a significant shift from the pre-project belief that intermittent irrigation will attract more rats into the rice fields (Lorica 2019). After the farmers were presented with the findings of the study, they were less hesitant to implement AWD because of concerns that rats would be more active in their rice crops when water levels were low.

3.5.3.1 Key Findings and Conclusion

The population ecology, behavioral, and social science research on rodents and AWD generated encouraging outcomes given how important the application of AWD, or at least one mid-season drainage of rice fields, is to a substantial reduction of greenhouse gas emissions during the growing season of rice (Lampayan et al. 2015). In summary, the analyses of the population dynamics and spatial use of rodents indicate that AWD is not likely to increase rodent damage to the growing rice crop. In addition, pre- and post-social surveys indicate that farmers are prepared to change their beliefs on rodents and AWD when presented with field findings.

3.6 A Way Forward

Rice fields have the potential to support biodiversity across biological scales. From a conservation standpoint, rice fields should be managed in a way that supports biodiversity within these agricultural systems. The ecosystem services provided by species which inhabit rice field ecosystems, across many trophic levels, may provide feedback and support to the farming stakeholders to help promote and sustain biodiversity. Overall, the adoption of ecosystem service-promoting rice agricultural practices may benefit farmers and other stakeholders and improve rice-field biodiversity.

To maximize the role of rice landscapes in supporting biological diversity and maintaining thriving wetland habitats, we outline four key areas that future research and development projects should address: (1) build capacity of countries to scale-up use of proven practices that reduce rice farming’s ecological footprint and conserve biodiversity, (2) increase investment in biodiversity research in rice production landscapes, (3) promote “Green Rice Value Chains” and “Agri-input Markets,” and (4) monitor and evaluate the ecological benefits to biodiversity of broadscale promotion of sustainable rice production.

Smallholder farmers often lack access to knowledge and training on sustainable management and best management practices, which remains a major bottleneck to achieving wide-scale adoption. As highlighted in this chapter, the CORIGAP program has validated many solutions that can reduce agrochemical use in rice production and, in turn, maintain rice landscapes’ capacity to sustain life. Such solutions, which include agroecological practices, such as rice-fish culture, ecological engineering, Integrated Pest Management (IPM), site-specific nutrient management, and conservation agriculture, deliver the same or higher yields as unsustainable practices prevalent across tropical Asia (Stuart et al. 2018a, b; Hung et al. 2022). CORIGAP has also demonstrated that, provided the right enabling conditions are put in place, smallholder farmers are able to adopt best management practices at scale (Flor et al. 2021). CORIGAP countries have been particularly successful in deploying best management practices through enacting enabling policies, building local extension system capacity, and establishing public–private sector learning alliances (Flor et al. 2017). CORIGAP countries have also benefited through developing integrated best management practice capacity development packages, which promote a combination of practices and technologies as a combined system. This enterprise has helped to maximize benefits to farmers and increased adoption rates in comparison with traditional development programs that have often focused on promoting a single practice or technology in isolation (Flor et al. 2021). Future research and development programs should build on the lessons learned from CORIGAP and continue to invest in sharing knowledge and building capacity to deploy sustainable best management practices across Asia.

In addition to boosting capacity-building programs and biodiversity-research investment, CORIGAP countries should also aim to leverage markets and create enabling conditions that incentivize the adoption of sustainable practices. Countries can review, phase out, and remove public programs that encourage rice production practices that are harmful to biodiversity. Rice is currently a major recipient of Asian agriculture subsidies and accounts for 15% of fertilizer and 35% of freshwater use globally. Some CORIGAP countries are already greening their public subsidy programs, resulting in significant positive impact. For example, in Guangdong province, China, the provision of subsidized agricultural inputs to rice farmers is now linked to their adoption of sustainable management technologies, known locally as “Three Controls” technology. Over 320,000 rice farmers have reduced fertilizer and pesticide use, while increasing yields by up to 10% (Xuhua Zhong, pers. comm.; Chapter 2 of this book). Policymakers can expand such reforms to subsidies and eliminate harmful subsidies wherever possible.

CORIGAP countries can also review regulations for their agri-input markets to accelerate registration of safer alternatives for pest management, phase out highly hazardous pesticides that are detrimental to biodiversity, and increase investment in manufacturing capacity for biopesticides and biofertilizers. These changes would benefit agriculture as a whole and enhance the capacity of rice landscapes to sustain life. Countries can also work with the private sector to apply sustainability standards, such as the Sustainable Rice Platform (SRP) Standard, which explicitly includes requirements to maintain biodiversity. CORIGAP-supported research has shown that urban consumers in Asian countries, such as Vietnam, are increasingly aware of the importance of sustainability and are willing to pay a premium for sustainably sourced rice (My et al. 2018). The SRP standard can embed sustainability across rice value chains and deliver sustainably certified rice products to consumers. Asian countries may consider establishing SRP national chapters and partnering with supply chain actors to adopt the SRP standard.

Finally, we recommend that future research and development programs should invest in monitoring and evaluation (M&E) to fully quantify and understand the ecological benefits to biodiversity of broadscale promotion of sustainable rice production. Collection of data to quantify benefits at both the farm and the landscape level will be highly beneficial for a number of reasons. First, better data will allow agricultural scientists and ecologists to further enhance and improve the design of best management practices to minimize trade-offs between achieving food security and preserving biodiversity. Second, M&E systems will provide capacity-building programs with better evidence upon which to evaluate and continually enhance their programs. And finally, the data generated through M&E can also help to build the investment case and help to unlock greater amounts of sustainable finance and private-sector investment in sustainable rice landscapes.