CHAPTER 8 Species Structure and Abundance of Invertebrate Natural Enemies in Sustainable Agroecosystems Hiroshi Amano CONTENTS Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 Nature of Species Structure and Abundance of Predacious Phytoseiid Mites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 Geographical and Climatic Factor . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 Food Habits and Co-occurring Prey Species . . . . . . . . . . . . . . . . . . . 171 Physical and Chemical Factors of Host Plant. . . . . . . . . . . . . . . . . . . 171 General Pattern of Dominancy in Phytoseiid Fauna. . . . . . . . . . . . . 173 Attributes of Mite Species Commonly Found in Agroecosystems and Factors Affecting their Abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175 Phytoseiid Fauna in North American Apple Orchards . . . . . . . . . . 176 Pesticide Application as Ultimate and Proximate Factors . . . . . . . . 178 Cultural Practice as Ultimate and Proximate Factors . . . . . . . . . . . . 179 Change in Prey Fauna as a Proximate Factor. . . . . . . . . . . . . . . . . . . 179 Competitive Interaction as an Ultimate Factor . . . . . . . . . . . . . . . . . 180 Use of Natural Enemies in Sustainable Agroecosystems as Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181 INTRODUCTION Recent expansion of the integrated pest management (IPM) system has revolutionized the whole concept of crop protection not only in Japan but 167 0-8493-0904-2/01/$0.00+$.50 © 2001 by CRC Press LLC 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 167 168 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Table 8.1 Major Natural Enemies of Spider Mites in Agroecosystems of Japan Class Order Family Genus & Species Insecta Coleoptera Coccinellidae Stethorus japonicus Staphylinidae Oligota kashmirica benefica Oligota yasumatsui Diptera Cecidomyiidae Feltiella sp. Hemiptera Anthocoridae Orius minutus Orius nagaii Orius sauteri Neuroptera Chrysopidae Chrysopa pallens Tysanoptera Thripidae Scolothrips takahashii Arachnida Acari Phytoseiidae Amblyseius californicus Amblyseius eharai Amblyseius womersleyi Typhlodromus vulgaris others Stigmaeidae Agistemus exsertus Agistemus terminalis also in other areas of the world. Consequently, applied entomologists and fundamental ecologists enjoy unexpected favor at all levels, not only to boost crop yield but also to preserve nature. For a long time, the nature of biotic interactions has been undiscovered and hidden in agricultural lands by heavy use of agrochemicals. Japan, one of the leading producers of these chemicals, unfortunately has taken the lead in throwing them into various facets of agroecosystems, where a rich biotic fauna of the temperate zone was originally established. A unique problematic example showing this process is a fauna of natural enemies of notorious pest mites. It is a well-known fact that spider mites were not of primary importance in pest management prior to the intensive intro- duction of synthetic agrochemicals in the 1960s. Mites had been well under control by a complex of natural enemies, paradoxically proven by many observations in which cessation of using pesticides and acaricides quickly recovered natural enemies resulting in suppression of the mite population at low levels. Due to persistent use of many chemicals, however, potential nat- ural enemy fauna, especially in the 1960s and 1970s, was undiscovered com- pletely, and it remained obscured until today. An overall picture of natural enemy fauna for spider mites is composed of predacious insects and mites (Table 8.1). These two taxa often co-occur in the field and together play an important role in depressing prey population. Although there are some dif- ferences in their predacious and habitat characteristics (Table 8.2), both groups share a common weakness against most agrochemicals. Under these circumstances, few long-tem studies on their dynamics in sustainable as well 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 168 SPECIES STRUCTURE AND ABUNDANCE OF INVERTEBRATE NATURAL ENEMIES 169 Table 8.2 Biological Characteristics of Natural Enemies of Spider Mites Common in Japan Thripidae Parameters Phytoseiidae Cecidomyiidae Staphylinidae Coccinellidae Chrysopidae Body size Small Large Abundance High Low Predation rate Low High of individual Developmental Fast Slow rate Prey requirement Small Large of individual Stability in prey High Low colony 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 169 as conventional agroecosystems are available, and analysis of factors respon- sible for their abundance is lacking. With the increasing emphasis on biological control as a core component in IPM, there is an urgent need to understand biocontrol agents with respect to the prevailing agroecosystem. This chapter focuses on the species structure and abundance of predacious mites of the family Phytoseiidae in Japan, fol- lowed by investigation into possible factors that determine their existence in the field. Given results and hypotheses may be helpful in understanding and predicting the behavior of natural enemies in upcoming sustainable agro- ecosystems. NATURE OF SPECIES STRUCTURE AND ABUNDANCE OF PREDACIOUS PHYTOSEIID MITES As mentioned briefly in the previous section, members of the family Phytoseiidae show a remarkable ability to depress spider mite population by their good numerical response and high stability in prey colony. Their body size (about 0.4 mm for the largest adult female) is as small as prey mites, but they are able to attack all stages of spider mites, although details of their bio- logical attributes are species-specific (e.g., McMurtry et al., 1970). About 1600 species are known to occur in the world (Chant and McMurtry, 1994). Recently, Ehara and Amano (1998) reviewed Japanese phytoseiid fauna and nominated, in total, 77 species with short remarks on their biology. They also categorized phytoseiid fauna into several groups after a close investigation of their association with different food habits and habitat. In reference to the basic picture presented by these authors, factors that may influence phyto- seiid distribution and survival, especially in natural ecosystems, are described in the following section. Certainly, these factors act simultaneously in the field, but for clarification are explained separately below. Geographical and Climatic Factor The climatic conditions in Japan are somewhat hostile for the establish- ment of beneficial phytoseiid species of tropical or subtropical origin, which include members in the genus Phytoseiulus. Moreover, no Galendromus and Metaseiulus species have been found. These two genera are of major taxa in the subfamily Typhlodrominae in the New World (Chant and McMurtry, 1994; Ehara and Amano, 1998). Looking at domestic phytoseiids, two species with similar ecological niches show contradictory distribution: Amblyseius finlandicus is well distributed in northern or elevated areas of Japan, whereas A. sojaensis is normally found in southern Japan. Some geographical and associated climatic conditions must have played an important role in their survival and establishment, and species seen in agroecosystems are not exceptional in this matter. 170 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 170 Food Habits and Co-occurring Prey Species No species have exactly the same food requirement and prey preference, and thus it is understandable that prey availability and distribution may determine establishment of predacious mites. Even on the same host plant, different fauna of phytoseiid mites will become dominant if prey species are changed with some reasons. One of the important factors in this regard is webbings produced by spider mites. Heavy web structures constructed by Tetranychus spp., in particular, easily eliminate certain phytoseiid species from the field, and often simplified their fauna (discussed in later sections). Table 8.3 shows a general scheme of four phytoseiid genera adapting to dif- ferent food types. It seems that there is a trend of increasing dependability on animal food along the genus line of Phytoseius-Typhlodromus-Amblyseius- Phytoseiulus. Of course, exceptional species can be found among various genus. In agroecosystems, abrupt turnover of prey species complex is often caused by human manipulations such as spray application. Physical and Chemical Factors of Host Plant The use of the term host plant for natural enemies is misleading because it is not purely phytophagous, but, for convenience, this word is used throughout this chapter for the plant on which the mites are collected. The physical structure on plant surfaces unexpectedly influences the successful colonization of phytoseiid mites. Leaf structure may includes roughness, pubescence, vein structure, domatium, and others (e.g., Collyer, 1976; Walter and O’Dowd, 1992). It is also suggested that volatile chemicals of host plants sometimes play a key role in the trophic triangle of host plant-prey mite- predacious mite (e.g., Dicke et al., 1990). Physical and chemical factors of host plants may also affect food prefer- ence and colonization of spider mites, and thus it is sometimes difficult to identify the ultimate reasons, between changes in prey species and host plants, for turnover of phytoseiid fauna. Nevertheless, Table 8.4 summarizes dominant phytoseiid species, which attack the population of a spider mite, Tetranychus kanzawai, in Japan for each host plant separately. Among these plants, basic fauna of predators is similar, but the predominant species on each plant (shown in the order of their abundance in the table) show some differences. For example, A. womersleyi commonly dominates on tea and Kudzu vine, but it is replaced by A. eharai on hydrangea and Glory-Bower. Distribution of predacious mites shows subtle differences even on the same tree. In 1988, mites were collected throughout seasons from water sprouts of Japanese pear trees in a small experimental orchard, and species were identified (Table 8.5). Due to unsprayed conditions for more than 10 years, a rust mite, Eriophyes chibaensis, is the only prey source for predators on both leaves and twigs of the sprouts. These phytoseiid species lived under the same climatic conditions and associated with the same prey, but they SPECIES STRUCTURE AND ABUNDANCE OF INVERTEBRATE NATURAL ENEMIES 171 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 171 172 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Table 8.3 Generalized Food Types and Biological Characteristics of Four Phytoseiid Genera Parameters Food Types Light Webbing Heavy Webbing Plant Juice Pollen Rust mite Spider Mite Spider Mite Phytoseius Typhlodromus Amblyseius Phytoseiulus Developmental rate Low High Predation rate Low High Oviposition rate Low High Stability of population High Low 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 172 showed some discrepancies in species abundance between leaves and twigs on the same sprouts. It was assumed at least that certain plant morphology and physiology might have affected microhabitat selection of each species in the field. General Pattern of Dominancy in Phytoseiid Fauna Is there any general pattern in phytoseiid fauna under relatively undis- turbed environments? This question is a topic in the present section and includes information useful when sustainable agroecosystems are once established. In Table 8.6, species structures of phytoseiid mites are shown as percentages for several natural or seminatural ecosystems. Three dominant species on each host plant occupied 67 to 99% of all specimens, and in two cases two dominant species accounted for over 90% (Kudzu vine and cherry in Matsudo). These values suggest that in undisturbed conditions, two or three species co-occupy the habitat and share resources in the single season. SPECIES STRUCTURE AND ABUNDANCE OF INVERTEBRATE NATURAL ENEMIES 173 Table 8.4 Dominant Phytoseiid Species in Japan Attacking Tetranychus kanzawai on Different Host Plants Host Plant Phytoseiid Species Japanese pear Amblyseius californicus, Amblyseius womersleyi Te a Amblyseius womersleyi, Amblyseius californicus Hydrangea Amblyseius eharai, Amblyseius womersleyi Kudzu vine Amblyseius womersleyi, Amblyseius eharai, Amblyseius sojaensis Glory-Bower Amblyseius eharai, Amblyseius womersleyi, Amblyseius orientalis Species are arranged in the order of their abundance. Table 8.5 Species Structure and Abundance of Phytoseiid Mites on Water Sprouts of Nonsprayed Japanese Pear Trees Species (no. of adult females and % in parentheses) On Leaves (n ؍ 145) On Twigs (n ؍ 41) 1. Amblyseius sojaensis 74(51) 1.Typhlodromus serrulatus 18(44) 2. Typhlodromus vulgaris 29(20) 2. Typhlodromus vulgaris 9(22) 3. Amblyseius okinawanus 19(13) 3. Amblyseiulella amanoi 4(10) 4. Amblyseiulella amanoi 13(9) 4. Amblyseius sojaensis 3(7) 5. Amblyseius tsugawai 7(5) 4. Amblyseius okinawanus 3(7) 6. Amblyseius eharai 3(2) 6. Amblyseius orientalis 2(5) 7. Amblyseius tsugawai 1(2) 7. Amblyseius makuwa 1(2) Surveys were conducted on 20 sampling dates in 1988 in an unsprayed small experimental orchard in Chiba Prefecture, central Japan. Predacious mites on different parts of water sprouts were separately collected and identified. 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 173 174 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Table 8.6 Percentage Occupancy of Dominant Phytoseiid Species in Natural or Seminatural Ecosystems in Japan Host Plant (date & place) n Percentage Occupancy of Dominant 3 Species Kudzu vine (1984 in Matsudo, Chiba) 96 Amblyseius womersleyi (49), Phytoseius nipponicus (42), Amblyseius tsugawai (6) Kudzu vine (1987–89 in Togane, Chiba) 240 Amblyseius okinawanus (63), Phytoseius nipponicus (12), Amblyseius tsugawai (11) Glory-Bower (1998 in Togane, Chiba) 267 Amblyseius orientalis (40), Amblyseius okinawanus (39), Amblyseius eharai (13) Cherry (1994 in Matsudo, Chiba) 229 Typhlodromus vulgaris (50), Amblyseius sojaensis (44), Typhlodromus serrulatus (5) Japanese pear (1988 in Togane, Chiba) 307 Amblyseius soajaensis (44) Amblyseius okinawanus (22), Typhlodromus vulgaris (14) Japanese pear (1995, in Kuki, Saitama) 68 Amblyseius okinawanus (26), Amblyseius californicus (25), Amblyseius paraki (16) In all surveys, samplings were carried out weekly or fortnightly. All host plants were in unsprayed condition. 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 174 In other words, this pattern could be an attribute that belongs to the phyto- seiid community in common. The species structure and abundance shown in Table 8.6 calculations were based on all specimens collected on the host plants during the survey season, and, thus, in some cases a seasonal discrepancy in abundance did not appear. The dominant phytoseiid species was dramatically changed on cherry in spite of year-round occurrence of the prey mite Tet. viennensis (Figure 8.1). Factors responsible for this seasonal change are not fully under- stood, and therefore further investigation is necessary. ATTRIBUTES OF MITE SPECIES COMMONLY FOUND IN AGROECOSYSTEMS AND FACTORS AFFECTING THEIR ABUNDANCE Among 77 species recorded from Japan (Ehara and Amano, 1998), 14 species are relatively common in a variety of agroecosystems (Table 8.7). Under the present pest management system, chemical control dominates other tactics of crop protection. Phytoseiid species, which successfully sur- vive in such conditions, have some potential of pesticide tolerance. Furthermore, pest mites of the genera Tetranychus and Panonychus usually increase their numbers by resurgence, and thus predators in close relation to SPECIES STRUCTURE AND ABUNDANCE OF INVERTEBRATE NATURAL ENEMIES 175 Figure 8.1 Seasonal population dynamics of two dominant phytoseiid species on cherry trees in Matsudo, Chiba, Japan in 1994. They were closely asso- ciated with a prey mite, Tetranychus viennensis. 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 175 these prey may have advantages. As pointed out earlier, ability of phytoseiid species to be generous with spider mite webbing is a precious talent to increase their population in available prey resources, especially against genus Tetranychus. All species of Phytoseius and Typhlodromus and many species of Amblyseius listed in Table 8.7 lack at least one of these abilities. Japan, extending north to south, is a country with extreme variations in climate, and climatic conditions in the northern area are supposed to be severe for the survival of most species. Cold tolerance and overwintering ability are important characteristics for species survival as shown for A. wom- ersleyi by Kishimoto and Takafuji (1994 and 1997). They showed that popula- tions from the north had higher diapausing capacity than the southern population but at the expense of a narrower temperature range in which they could display their full reproductive ability. In the following section, details of factors that affect the abundance of phtyoseiid mites in agroecosystems are described. Phytoseiid Fauna in North American Apple Orchards Surveys on apple trees in the “apple belt” of North America are by far the most complete among any studies for phytoseiid fauna on a single host plant. Those from the 1960s and 1970s are especially useful because few exotic species were experimentally introduced into the areas in those eras. Table 8.8 shows dominant species in the eastern, central, and western regions of the apple belt for sprayed and unsprayed orchards separately. In commercial sprayed orchards, A. fallacis predominated in 14 states and provinces of east- ern and central regions, whereas in five western states and provinces Typhlodromus occidentalis predominated. When crop protection practices including sprays were discontinued, more species were observed in the orchards, and this trend was common in all apple orchard regions of North America. In the eastern to central regions, T. pomi became most abundant and widely distributed. Phytoseius macropilis seems to have a second position in this context. In the west, however, T. caudiglans and T. pyri (in British Columbia) or T. flumenis (in Utah), for example, dominated in the orchards, and T. pomi was never as numerous as in other regions. 176 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Table 8.7 Phytoseiid Species Commonly Found in Japanese Agroecosystems Genus No. of Species Species Name Phytoseius 2 capitatus, nipponicus Typhlodromus 2 serrulatus, vulgaris Amblyseius 10 californicus, eharai, finlandicus, koyamanus, makuwa, okinawanus, orientalis, sojaensis, tsugawai, womersleyi Species were collected from agricultural crops and/or groundcovers. 920103_CRC20_0904_CH08 1/13/01 10:56 AM Page 176 [...]... Saitama (n= 68) Chiba, Chiba (n=144) Species structure (% occupied) of phytoseiid species in Japanese pear orchards with different prey mites in dominance Main prey mites and observation years are as follows: Eriophyes chibaensis in 1 988 (Togane), Tetranychus kanzawai in 1995 (Kuki), and Panonychus citri in 1996 (Chiba) 920103_CRC20_0904_CH 08 180 1/13/01 10:56 AM Page 180 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS... 920103_CRC20_0904_CH 08 182 1/13/01 10:56 AM Page 182 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Chant, D A and McMurtry, J A., 1994 A review of the subfamilies Phytoseiinae and Typhlodrominae (Acari: Phytoseiidae) Int J Acarol., 20:223–310 Collyer, E., 1976 Integrated control of apple pests in New Zealand 6 Incidence of European red mite, Panonychus ulmi (Koch), and its predators N... in phytoseiid fauna in the field 920103_CRC20_0904_CH 08 1 78 1/13/01 10:56 AM Page 1 78 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT important in this context, as will be mentioned later Details of these factors are discussed in the following sections Pesticide Application as Ultimate and Proximate Factors Many studies suggested drastic changes in species structure and abundance of phytoseiid... agricultural lands, and we are now facing a serious problem in the names of resurgence and environmental pollution Ecologically speaking, frequent chemical applications introduced never-ending instability into agroecosystems, and natural enemies of spider mites suffered a great reduction in numbers It is obvious that not only spider mites are the major pests in the field, but a complex of hazardous invertebrates... on the ground level in winter, and, if weed control in orchards is light throughout seasons, their populations are maintained at high levels and predators often climb on the trees Amblyseius tsugawai is one of those species, and it is frequently observed in sod-cultured orchards Different cultural practices undoubtedly affect many dimensions and components in the agricultural land, and thus it is usually... 40:331–390 Penman, D R., Wearing, C H., Collyer, E and Thomas, W P., 1979 The role of insecticide-resistant phytoseiids in integrated mite control in New Zealand Recent Adv in Acarology, 1:59 –69 Specht, H B., 19 68 Phytoseiidae (Acarina: Mesostigmata) in the New Jersey apple orchard environment with descriptions of spermathecae and three new species Can Entomol., 100:673 –692 Walter, D E and O’Dowd, D J., 1992... influential factor in the field either directly (killing predators) or indirectly (killing certain prey species) Cultural practice of crops, such as weed management, also determines abundance of predators directly or indirectly In contrast, competitive interaction among predators is not well understood, but it is probably Figure 8. 2 Diagrammatic representation showing factors responsible for change in phytoseiid... Long-term investigation of the program is now under execution Since 324 BC in China, when ancient Chinese farmers were reported to foster ants in order to control caterpillars and beetles on citrus trees (after DeBach and Rosen, 1991), there has been pessimism about development in our technology of biocontrol and related philosophy on pest management However, an assignment recently given to us in the... ultimate and/ or proximate factors could not be fully excluded 9 17 83 A tsugawai A womersleyi A californicus 19 29 81 Figure 8. 5 91 71 Species structure (% occupied) of phytoseiid species in 4 neighboring pear orchards under similar cultural conditions Survey was conducted on Aug 28, 1997 at Katori, Chiba 920103_CRC20_0904_CH 08 1/13/01 10:56 AM Page 181 SPECIES STRUCTURE AND ABUNDANCE OF INVERTEBRATE... H., and de Groot, A E., 1990 Isolation and identification of volatile kairomone that affects acarine predator-prey interactions J Chem Ecol., 16: 381 –396 Ehara, S and Amano, H., 19 98 A revision of the mite family Phytoseiidae in Japan (Acari, Gamasina), with remarks on its biology Species Diversity, 3:25–73 Hill, T A and Foster, R E., 19 98 Influence of selective insecticides on population dynamics of . not only in Japan but 167 0 -8 49 3-0 90 4-2 /01/$0.00+$.50 © 2001 by CRC Press LLC 920103_CRC20_0904_CH 08 1/13/01 10:56 AM Page 167 1 68 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT Table. important role in their survival and establishment, and species seen in agroecosystems are not exceptional in this matter. 170 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT 920103_CRC20_0904_CH 08. be fully excluded. 180 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT 17 19 83 81 71 91 9 29 A. californicus A. womersleyi A. tsugawai Figure 8. 5 Species structure (% occupied)