2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS'2012) Oct. 13-14, 2012 Bali (Indonesia)

Environmentally Sound Agro-practice, Biodiversity and Indicator in Rice Paddies

Takatoshi Ueno

received growing attention because it plays a significant role in Abstract—Rice paddies occupy the largest cultivated area in agro-ecosystem function [2], [4]–[6]. agricultural land and provide the habitats for many organisms. Thus, Beneficial organisms such as natural enemies of pests and rice paddies are a key ecosystem in agricultural land that sustains a pollinators serve agro-ecosystem function [7]–[9]. In high level of agro-biodiversity. Natural enemies have an important agricultural fields where pesticide use is minimized, crop function for crop production as agents of ‘ecosystem services’ because they play a major role in suppressing pests. The diversity and production commonly depends on natural control provided by abundance of natural enemies can be a good index reflecting the natural enemies; they can have a great impact on pest ‘healthiness’ of agro-ecosystem services in rice paddies. In the present populations. Their importance is highlighted when biological study, a survey was made to investigate the abundance and control, i.e., active use of natural enemies, works well or when biodiversity of natural enemies in rice paddies where chemical inputs, the resurgence of pests takes place [3], [10]–[11]. i.e., insecticide use, were different. The reduction of chemical inputs Indiscriminate use of agro-chemicals such as insecticides led to an increase in species richness or diversity of natural enemies like parasitoids and . Then, it was analyzed to explore suitable harms natural enemies and causes the loss of biodiversity of indicator species to assess environmental soundness of agricultural such beneficial organisms [10]–[11]. practice and biodiversity in rice paddies. Seven spotted ladybird The biodiversity of beneficial natural enemies may be a key beetle, Coccinella septempunctata, (Coleoptera: Coccinellidae) and a resource to improve the productivity and sustainability in web-constructing araneid , adianta, (Araneae: agriculture [3], [6], [12]. Conservation of the biodiversity Araneidae) were among the commonest species of predators detected should then be an important approach for sustainable in paddy fields, and were tested to examine whether the density of the two could reflect the levels of chemical input and biodiversity. The agriculture. To do this, it is required to monitor and evaluate the density of the ladybird did not respond both to pesticide use and to diversity of beneficial organisms. The problem is that biodiversity, indicating that this species was not suitable as an monitoring the whole community or biodiversity is highly time indicator. In contrast, the araneid spider increased both with a and labor consuming. It is thus ideal to select indicator reduction of pesticide use and with an increase of biodiversity. organisms that directly or indirectly relate to the level of Neoscona adianta was hence a good candidate of natural enemies to biodiversity and to use them for monitoring the biodiversity of assess agricultural practice and biodiversity in rice paddies. Thus, it is possible to select species that are ideal bioindicators for monitoring beneficial and other neutral organisms [1], [4], [5]. both environmental soundness and biodiversity in agriculture. Being ‘ecological’ is on strong demand in agriculture Usefulness of indicator species in rice paddies is discussed. nowadays. Large-scale use of agro-chemicals cannot be an option of farming practices due to public concern for Keywords— Functional biodiversity, agro-ecosystem, pest environment and health issues. However, so called ecologically management, environmental monitoring. or environmentally friendly agriculture is mostly desired in terms of the production of safe food for humans with minimum I. INTRODUCTION use of agro-chemicals; its impact on conservation of GRICULTURAL LAND is the habitat for many biodiversity is often neglected. In Japan, eco-friendly Aorganisms, including pest, beneficial and neutral species, agriculture are widely applied in many crop production all of which exist together in both time and space. They systems, including rice paddies, but its consequent impact on constitute a ‘community’, which contains a wide variety of organisms is usually unclear [13]. species that differ in their functions, representing biological Environmentally sound agriculture should now be linked to diversity in agricultural land [1]–[3]. In other word, agricultural biodiversity in order to meet recently growing demand that land supports, at least in part, biological diversity. Biological organism communities in agriculture land should be conserved diversity (hereafter, biodiversity) in agricultural land has as possible though this idea has many conflicting aspects. By focusing the impact on biodiversity, environmentally sound agriculture would meet the demand by consumers (i.e. safe Takatoshi Ueno is with the Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (phone: food) as well as the demand from a point of view of sustainable +81-92-642-3036; fax: +81-92-642-3040; e-mail: [email protected]). production [13].

20 2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS'2012) Oct. 13-14, 2012 Bali (Indonesia)

Rice is the primary food in Asia, where wet paddy pests. In many fields (but not all the fields), herbicides were cultivation is traditionally used for rice production. Rice applied once after transplanting rice. Around the flowering paddies occupy the largest cultivated area in Japan and other stage of rice, farmers applied Dinotefuran (a systemic Asian countries, which support one of the largest insecticide) twice to control leafhoppers, planthoppers and communities among agricultural systems [15], [16]. To practice green bugs but not all farmers applied such insecticides during environmentally sound rice production, the community of the growing stage of rice. Thus, rice paddies studied were beneficial natural enemies should be studied because without placed in three types; (1) organic fields (without any pesticide), this knowledge it is difficult to evaluate which management and (2) fields with insecticides only once during the seeding methods could be least influential to the biodiversity. Basic stage or (3) three times (once in seedling and twice during biology of beneficials in the community should also be growing stages). In my study, I mainly focused on maturing investigated [9], [14]. In addition, it is needed to establish stage of rice because all chemical inputs were terminated in this laboratory systems for testing the effects of agrochemicals like growth stage, which was suitable for the purpose of the study. insecticides and herbicides on beneficial insects [9], [14]. The maturing stage of Hinohikari was between September and Given that rice paddies provide habitats for hundreds of October. neutral and beneficial arthropod species [15], [16], all of these Arthropod natural enemies were sampled in 44 farmer’s organisms would be difficult to be involved in the fields. In 2008, general survey was first made to know the above-mentioned studies. Accordingly, it is crucial to select species composition of natural enemies found in the area of particular species or groups as indicator organisms for Nijyo-machi Town. For this purpose, sweeping with an insect extensive studies [1], [4], [13]. At least, candidate organisms net and visual collection were performed to obtain specimens, should be: widely distributed, commonly found, readily and the list of natural enemies was prepared. In 2009, data recognized or sampled, sensitive to agricultural practices and collection for analyzing biodiversity and exploring candidate easily reared in the laboratory [4], [5]. It is also ideal if indicator organism were made. To do this, inspection of the entire plant organisms reflect the biodiversity in agricultural land. was made to search natural enemies to obtain the data. In the present study, I focus only on arthropod natural Sampling was made by walking 5 m along 3 lows of rice plants. enemies, i.e., insects and spiders; birds, reptiles and amphibians Each field was sampled at two sites. This sampling was are not the targets of the study. This is because are repeated twice in different days for each field. The numbers of the major group of organisms recorded from rice paddies natural enemies were counted, and the species were recorded. [14]–[16]. Natural enemies are placed in three groups; When necessary, specimens were collected for exact predators, parasitoids and pathogens [8], [11], and the former identification to species. The results reported here were based two are among the arthropods. Parasitoids and predators are on the data collected from September to October, 2009. therefore the focus of my study here. I first examine the relationship between farming practices (pesticide use) and B. Data Analyses biodiversity of natural enemies, and, then, explore candidates as bioindicators in rice paddy ecosystems. Basing on the The data were analyzed with the aid of JMP (SAS, 2008). In results, I will discuss usefulness of bioindicators and my study, the diversity of natural enemies, i.e., parasitoids and conservation of beneficial natural enemies in the context of predators, was estimated by Shannon’s Index (= environmentally friendly agriculture. Shannon-Wiener Index), which allows the measurement of biodiversity. This index is commonly used because it has an advantage to take into account the number of species and the II. METHODS evenness of the species, both of which are important concept of biodiversity. A. Field Survey

Agricultural biodiversity on relatively small-scale farms was III. RESULTS surveyed in the present study Field survey was conducted in 2008 and 2009. Study sites are located at Nijyo-machi Town, The relationship between insecticide inputs and species Fukouoka Prefecture, lowland areas in northern Kyushu main richness (= number of species recorded per 5m in 3 lows) of island of Japan. Rice variety chosen for the study was natural enemies was then assessed with a generalized linear Hinohikari, which was the most popular in northern Kyushu. In model (=GLM).Overall, species richness and biodiversity the study sites, rice was an annual crop, and the variety increased with a reduction of insecticide use. Insecticide use Hinohikari was transplanted from late June to early July. significantly influenced the species richness (GLM; link 2 = 23.6, P < 0.0001 for Harvest was made mostly in early October. Rice paddies function for poisson; df =2, x parasitoids; df =2, x2 = 19.1, P < 0.0001 for predators). As selected for the present study included both organic farming expected, the highest levels of species richness for parasitoids fields and conventional farmer’s fields. In conventional fields, and predators were observed in rice paddies where no farmers exclusively used Imidacloprid, a systemic insecticide insecticides had been used (Fig. 1). acting as an insect neurotoxin, during the seeding stage before transplanting as the chemical control tool to manage insect

21 2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS'2012) Oct. 13-14, 2012 Bali (Indonesia)

Next, statistical analyses were made to examine whether some natural enemies species could reflect agricultural practice and biodiversity in rice paddies. Two species of predacious arthropods were chosen, namely, seven spotted ladybird beetle, Coccinella septempunctata,(Coleoptera: Coccinellidae) and an araneid spider Neoscona adianta (Araneidae). These two predators were selected because they were very common in agricultural fields and because they had a wide range of the distribution across the country. In fact, these two species were frequently observed in rice paddies in the study fields. The effects of insecticide applications on the ladybird and spider were first analyzed. Curiously, ANOVAs revealed that the two predacious species responded differently to insecticide use; the density of the spider N. adianta significantly differed among rice paddies with different applications of insecticides (ANOVA; df = 2, F = 4.97, P = 0.011), and the abundance was lowest in rice fields where insecticides had been applied three times (Fig. 3 left). However, the density of seven spotted ladybird was not influenced by chemical applications (F = 1.21, P = 0.31) though it was most abundant in rice paddies with no insecticide use (Fig. 3 right). The relationship between the density of the spider and the diversity of natural enemies was then examined. A generalized linear model (GLM) was constructed for this purpose. A significant model was obtained (GLM, link function = poisson; df = 1, x2 = 4.85, P = 0.027), and there was a positive relationship between the density of N. adianta and the diversity Fig. 1. Relationships between insecticide use (measured as the of natural enemies (Fig. 4). count of applications) and species richness (mean number of total species detected) of natural enemies in rice paddies (Data were shown as means ± SE) IV. DISCUSSION A large share of the total land area in Asian countries is Based on the data collected in 2009, the biological diversity occupied by agricultural land where many species of of natural enemies was calculated with Shannon-Wiener Index. and insects are observed. Thus, agricultural land should play a The biodiversity of natural enemies, including parasitoids and key role in supporting biodiversity of semi-natural predators, was strongly affected by insecticide inputs environments. Intensification of agriculture causes the loss of (ANOVA; df = 2, F = 26.7, P < 0.0001) and was greatest in rice biodiversity and should hence weaken the function of paddies without insecticide application (Fig. 2). Both species agro-ecosystem service [6], [12]. Intensified use of richness and biodiversity were notable low when insecticides agro-chemicals can increase the agricultural production but had been used three times during the growing season (Fig. 1 & should harm biodiversity in agricultural land [12], [13]. In the 2). present study, I have focused on the biodiversity of arthropod natural enemies as a representative agent of ecosystem service and shown that an increase of insecticide use leads to the reduction of species richness and biodiversity of predators and parasitoids of rice pests (Figs. 1 & 2). In recent years, chemical inputs have been largely reduced in rice production of Japan [13]; in fact, the count of pesticide use was only 3 at maximum in the study area. Nevertheless, the results have given evidence that insecticide use harms beneficial natural enemies, reducing the abundance and species richness. Reduction of insecticides as possible, preferably once or twice, would help conserving the community of natural enemies in rice paddies and allow avoiding disruption of native ecosystems and agro-ecosystems.

Fig. 2. Relationship between insecticide use and biodiversity (measured with Shannon’s index (Data were shown as means ± SE)

22 2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS'2012) Oct. 13-14, 2012 Bali (Indonesia)

within the range of distribution. Also they may strongly respond to micro-environments around and within agricultural fields, and environmental factors other than agricultural practices may largely determine the abundance of such rare species. Rare species hence may not necessarily reflect farming practices like pesticide use, and would thus be unsuitable as bioindicators widely used across the large area of the country. Among predacious species detected in the present study, I selected two species of natural enemies to illustrate the process of selecting indicator species. Seven spotted ladybird beetle, Coccinella septempunctata, is a very common insect that is familiar to general public in the country. Seven spotted ladybird beetle is a widespread predator of aphids including several pest species. Another predator selected is the araneid spider Neoscona adianta which is also among the commonest species of predators in the country. Both species of predators were detected widely in the study fields. These two species were tested to examine whether the density of the two could reflect the levels of chemical input and biodiversity. Strikingly, two species were shown to have a distinctly different response to farming practices. The spider responded to an increase of insecticide applications by reducing its number or density whereas the ladybird appeared insensitive to chemical use (Fig. 3). At least, these data suggest that N. adianta is more sensitive to pesticide applications or farming practices. Thus, the present study has demonstrated that not all species of natural enemies are equally Fig. 3. Effects of pesticide use on the density of two predacious affected by the degree of environmental friendship of species. The mean density of spiders significantly differed among the agriculture. By comparing the response to agricultural groups while the ladybird did not significantly respond to pesticide use. practices, candidate species should be selected to explore Data were shown as means ± SE suitable organisms for assessing whether a given practice is

benign to natural enemies and environment. The diversity of beneficial species such as natural enemies of pests represents functional biodiversity in agricultural fields [4], [5]. As demonstrated in the present study, functional biodiversity must be damaged by improper use of chemicals including pesticides. Therefore, environmentally sound agriculture, which is often desired in terms of the production of safe food for humans, should be linked to conservation of the biodiversity with minimizing use of chemicals. The present study has also indicated that the biodiversity of natural enemies can reflect the degree of environmental soundness of such agricultural practices (Fig. 2). Then it is possible to assess what extent a given practice is friendly to the environment, on the basis of the diversity of natural enemies. The assessment of biodiversity in a given agricultural field is not easy because it is time and labor consuming. Instead, it is ideal to select indicator Fig. 4. Relationship between the density of N. adianta and biodiversity species that reflect the level of biodiversity and environmental of natural enemies. A linear estimated with GLM (link function: soundness [13]. poisson) is fitted In the present study, I have mainly focused on common species that are widely distributed in the country. This is In addition, the present study has examined whether a primarily because bioindicators should be widely observed in given species of natural enemies could reflect the biodiversity agricultural land across the country. The study of biodiversity of natural enemies in rice paddies. The results have provided often focuses on protection and conservation of endangered evidence that the density of the spider N. adianta positively species and habitats. However, endangered rare species may correlates to the biodiversity (Fig. 4). Thus, by monitoring the simply be absent in a given area simply because the area is not presence and abundance of this spider, it will be possible to

23 2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS'2012) Oct. 13-14, 2012 Bali (Indonesia) indirectly evaluate the biodiversity of natural enemies. Because biodiversity, and natural pest control,” Proc. R. Soc. B., vol. 273, pp. N. adianta is a web-constructing, relatively large and visibly 1715–1727, 2006. [13] T. Ueno, “Biodiversity in Rice Paddies and Use of Indicator Species to conspicuous species, monitoring of this spider should be easily Assess Environmental Friendship of Agricultural Practices,” done even for farmers. Readiness of recognition would be an International AFAS Joint Symposium Between Korea and Japan, vol. 7, important component as indicator species [13]. The spider N. pp. 126–132, 2010. [14] T. Ueno, Parasitoid life history. In: Biological Control of Agricultural adianta therefore is a good candidate of indicators in rice Pests in Asia: Theory and Practice, Institute of Biological Control, paddies. Kyushu Univ., pp. 15-25, 2004. Here, two species of arthropod predators were tested for the [15] K. Yano, Insect Fauna in Paddy Field. Tokyo, Tokai Univ. Press, (in Japanese), 2002. suitability as indicator organisms among natural enemies. [16] K. Kiritani, A Comprehensive List of Organisms Associated with Paddy Insect parasitoids are also a diversified group of natural Ecosystems in Japan. Saga, Daido Printing Co. Ltd., 2009. enemies [8], [14] and may contain good candidates of [17] D. A. Landis, M. M. Gardiner, W. van der Werf and S. M. Swinton, “Increasing corn for biofuel production reduces biocontrol services in bioindicators. Parasitoids are among important beneficial agricultural landscapes,” Proc. Natl Acad. Sci. USA, vol. 105, pp. organisms in rice paddies, and many parasitoids have been 20552–20557, 2008. recorded from rice paddies as natural enemies of lepidopteran [18] K. Yasumatsu and C. Watanabe, A Tentative Catalogue of Insect Natural and homopteran pests [16], [18], [19]. Thus, at least several Enemies of Injurious Insects in Japan. Part 2. Host Parasite-Predator Catalogue. Fukuoka, Entomol. Lab., Fac. Agric., Kyushu Univ. Press, species or groups of parasitoids should be tested for their 1965. suitability as indicator organisms in future study. Although [19] T. Nishida and T. Torii, Rice Stem-Bores and their Natural Enemies. IBP birds, mammals, frogs and other higher animals were not in the Handbook no. 14. The International Biological Program, Oxford, Blackwell Scientific Publication, 1970. scope of the present study, some of them should also be important as natural enemies of pest organisms. Currently, the suitability of such animals as indicators species is also under evaluation.

ACKNOWLEDGMENT This work was supported by grants from the Ministry of Agriculture, Forestry and Fisheries of Japan (Research Project: Selection of functional biodiversity indicators and development of assessment methods) and by Grant-in-Aid for Basic Research (C), Japan Society for the Promotion of Science (Research Project Number: 24580079).

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