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parameters that can effect this process. MEASURE OF COMBUSTION RATE AVAILABLE TECHNIQUES- The paper presented is intended as a contribution to our understanding of cycle to cycle variations in the combustion event in spark ignition engines. To enable
Effects of Intercropping on the Life Cycle of the Turnip Root Fly (Delia floralis) Behaviour, Natural Enemies and Host Plant Quality
Maria Björkman Faculty of Natural Resources and Agricultural Sciences Department of Crop Production Ecology Uppsala
Doctoral thesis Swedish University of Agricultural Sciences Uppsala 2007 1
Abstract Björkman, M. 2007. Effects of Intercropping on the Life Cycle of the Turnip Root Fly (Delia floralis) – Behaviour, Natural Enemies and Host Plant Quality. ISSN: 1652-6880, ISBN: 978-91-85913-24-4 The turnip root fly (Delia floralis) is a pest insect in the northern temperate regions of the world. If uncontrolled, it can cause severe problems in the production of brassica crops. This thesis examines how intercropping of cabbage (Brassica oleracea) and red clover (Trifolium pratense) affects the different life cycle stages of D. floralis. Such knowledge about the mechanisms involved is needed for developing intercropping systems with optimal pest reduction. A field trial was performed in Umeå, northern Sweden (63º45’N; 20º15’E), to study the effects of intercropping on D. floralis oviposition behaviour, and the impact of predators and parasitoids on D. floralis in the field. Intercropping was found to reduce D. floralis oviposition compared with monoculture. Furthermore, analysis of the spatial distribution of eggs within plots showed that the difference in egg numbers was greatest close to the border between the cultivation systems. This indicates that the effect of intercropping can be enhanced if D. floralis is provided with an alternative oviposition site. Natural enemies, in this case mainly predators, significantly reduced the final pupal numbers of D. floralis but this effect did not differ between the cultivation systems. However, the study showed that it is possible to retain the predation pressure in intercropped systems despite lower predator activity-densities and D. floralis egg numbers. A greenhouse experiment was performed to investigate effects of intercropping on development of D. floralis at different larval and intercropping densities and to analyse different aspects of host plant quality in the same system. It was found that D. floralis pupal weight decreased in response to both intercropping and larval density. This impaired larval development is likely to be explained by changes in host plant quality, which included decreased biomass, lower root nitrogen levels, higher root fibre content and altered glucosinolate concentrations. Information on plant responses to herbivory in competitive plant systems can be valuable in identifying quality aspects that are negative for insect development, which may further improve pest insect regulation in these systems. Keywords: Oviposition, border effect, predation, parasitization, glucosinolates, NDF, lignin, induced response. Author´s address: Maria Björkman, Department of Crop Production Ecology. SLU, Box 7043, SE-750 07 UPPSALA, Sweden. E-mail: [email protected]
Effekter av samodling mellan vitkål och rödklöver på den stora kålflugan (Delia floralis) Beteende, naturliga fiender och värdväxtkvalité Den stora kålflugan (Delia floralis) är en skadegörare på kålväxter som t.ex. vitkål, broccoli och blomkål. Flugan lägger sina ägg i jorden intill plantan, och larverna äter sedan av rötterna, vilket kan hämma plantans tillväxt eller leda till att den dör. Ekologiska grönsaksodlare i Sverige har identifierat en pålitlig och effektiv bekämpning av skadegörare som en viktig del i utveckling av den ekologiska trädgårdsodlingen. Det finns därför ett behov att hitta nya metoder för att minska skador orsakade av D. floralis. Samodling mellan växter kan vara en metod för att minska angrepp av skadegörare i en odling. I den här avhandlingen har jag undersökt hur samodling mellan vitkål och rödklöver påverkar äggläggningen hos D. floralis, samt hur effekten av dess naturliga fiender som predatorer och parasitoider som angriper flugans ägg, larver och puppor, påverkas av odlingssystemet. Studierna av äggläggningsbeteende och naturliga fiender gjordes i ett fältförsök på Röbäcksdalen i Umeå. Jag fann att samodling kraftigt minskade äggläggningen av den stora kålflugan jämfört med vitkål odlad i monokultur. Effekten av samodling var störst nära gränsen till monokulturen, och denna ’gränseffekt’ sträckte sig ett par meter in i båda odlingssystemen. Det visar att det är möjligt att ytterligare förbättra effekten av samodling om D. floralis har tillgång till en bättre äggläggningsplats. Att kombinera samodling och monokultur kan vara en strategi i utvecklingen av odlingssystem med hög reglering av skadegörare. Naturliga fiender, i det här fallet främst predatorer, hade en god reducerande effekt i fältet, och denna effekt var lika hög i båda odlingssystemen. Försöket visade att det är möjligt att bibehålla en effekt av naturliga fiender trots att både färre predatorer och kålflugeägg återfanns i samodlingen. I ett växthusförsök undersökte jag hur en ökad klöverdensitet, samt en ökad grad av rotskada orsakad av D. floralis larver, påverkar vitkålens kvalité som födoresurs för kålflugan. Kålflugans utveckling hämmades då vitkålen var samodlad med klöver, samt vid konkurrens med andra kålflugelarver. Denna effekt kan förklaras av förändringar i vitkålens kvalité vilket inkluderade en lägre kåltillväxt, lägre näringsinnehåll, ökat fiberinnehåll samt förändrade nivåer av sekundära ämnen, s.k. glukosinolater. Information om vilka växtfaktorer som hämmar insekters utveckling är värdefull för att långsiktigt kunna dämpa tillväxten i en insektpopulation. Sådan kunskap, tillsammans med kunskap om insekters beteende och deras samspel med naturliga fiender, ökar möjligheten att utveckla samodlingssystem med en optimerad effekt på skadeinsekter.
Contents Introduction, 7 Aims of thesis, 7 Theoretical background, 8 Intercropping theory, 8 Definition of intercropping, 8 Effects on pest insects in intercropping systems, 9
The turnip root fly - Delia floralis, 11 Biology, 11 Behaviour, 12 Natural enemies, 14 Development and food quality, 14
Materials and methods, 15 Field trial, 15 Greenhouse experiment, 17 Statistical analyses, 18 Results and discussion, 19 Behavioural effects, 19 Quantity and distribution of eggs, 19
Effects on and of natural enemies, 22 Effects on natural enemy activity-densities, 22 Predation and parasitization, 23 Survival of D. floralis in the field, 25
Host plant quality and D. floralis development, 25 Cabbage N, C, NDF and lignin, 25 Glucosinolate concentrations, 26 Development of D. floralis, 29
Conclusions and applications, 31 References, 33 Acknowledgements/Tack, 41
Appendix Papers I-IV This thesis is based on the following papers, which are referred to in the text by their Roman numerals: I.
Björkman, M., Hambäck, P.A. & Rämert, B. 2007. Neighbouring monocultures enhance the effect of intercropping on the turnip root fly (Delia floralis). Entomologia Experimentalis et Applicata 124, 319-326. Björkman, M., Hambäck, P.A., Hopkins, R.J. & Rämert, B. Evaluating the Enemies hypothesis in an intercropping system – effects of generalist and specialist natural enemies on the turnip root fly (Delia floralis). (Submitted to Agricultural and Forest Entomology). Björkman, M., Hopkins, R.J., Hambäck, P.A. & Rämert, B. Effects of intercropping and herbivore density on the development of the turnip root fly (Delia floralis) mediated by host plant quality (Submitted to Entomologia Experimentalis et Applicata). Björkman, M., Hopkins, R.J. & Rämert, B. Combined effect of intercropping and turnip root fly (Delia floralis) larval feeding on the glucosinolate concentrations in cabbage roots and foliage (Submitted to Journal of Chemical Ecology).
Paper I is reprinted with kind permission from the publisher.
Introduction The turnip root fly, Delia floralis Fall. (Diptera: Anthomyiidae), is a specialist pest insect of Brassica crops, such as cabbage, cauliflower and broccoli. If uncontrolled, D. floralis can cause substantial yield losses in vegetable production. In a recent survey, organic vegetable growers in Sweden identified efficient and reliable pest control as one key factor for the development of organic vegetable production systems (Nilsson, 2007). At present, methods for adequate control of D. floralis in organic vegetable production are scarce. There is therefore a need to develop alternative methods for pest control, in order to meet the demands of sustainable and reliable vegetable production. Increased attention has been given to the potential benefits of enhanced withinfield plant diversity as a strategy for pest insect control (Risch, 1983; Vandermeer, 1989). Intercropping is one way to add diversity to a cropping system, and there are many examples where these systems have been shown to suffer from lower yield losses due to insect damage compared with monocultures (Theunissen, Booij & Lotz, 1995; Rämert & Ekbom, 1996). However, the variability in responses by insect herbivores to plant diversification (Andow, 1991) shows that there is a need for better understanding of the mechanisms affecting insect herbivores in diverse systems. The work in this thesis formed part of the project Ecology of the Cultivation System – Green Manure as a Multifunctional tool in Vegetable Production, the aims of which were to develop locally adapted organic vegetable production systems in which green manure use is optimised for integrated management of plant nutrients, pests and product quality, and to evaluate the agronomic and economic performance of vegetable production systems.
Aims of thesis The main aim of this thesis was to examine different aspects of the effects of intercropping cabbage with red clover on the life cycle of D. floralis and to gain knowledge about the mechanisms involved, which is needed for developing intercropping systems with optimised pest reduction. The project was divided into two parts. In a field trial, the pest reduction capacity of intercropping for D. floralis was examined. This was done by: (1) Studies of the oviposition behaviour of the flies; and (2) examination of the effect of natural enemies as predators and parasitoids. Studying both these in the same field experiment gave the opportunity to evaluate the importance of each mechanism for pest reduction. In addition, a greenhouse experiment was performed to: (3) Investigate effects on development of D. floralis at different larval and intercropping densities; and (4) study the response of the host plants in the same system by analysing the effects on growth and content of nitrogen and carbon, fibre (neutral detergent fibre and lignin) and secondary compounds (glucosinolates).
Intercropping cabbage with clover was expected to affect the oviposition behaviour of the turnip root fly, the predation and parasitization by natural enemies, and the development of the flies through altered host plant quality. This thesis is based on the following questions: •
Is the oviposition behaviour of D. floralis disrupted by the presence of a clover intercrop?
Does the distance from the adjoining treatment affect the distribution of eggs within the monocultured and intercropped experimental plots?
Do natural enemies, such as carabids and staphylinids, respond with higher activity-densities in the diverse intercropped treatment?
Does intercropping lead to higher predation and parasitization rates of D. floralis, and does the predation pressure change during the season?
Is the quality of cabbage (growth, C and N, and fibre) affected by intercropping and herbivore pressure, and is the development of D. floralis affected by these changes?
Is the content of glucosinolates in cabbage foliage and roots affected by intercropping and herbivore pressure, and are there any implications for D. floralis development?
Theoretical background Intercropping theory Definition of intercropping Intercropping can be defined as the cultivation of two (or more) plant species simultaneously in the same field. The plant species do not necessarily have to be sown at the same time, and their harvest times may differ, but they should be grown simultaneously for a substantial part of their growth periods (Andrews & Kassan, 1976). There are several different modes of intercropping, ranging from very regular arrangements to situations where the different plant species are intermingled. In mixed intercropping, the plants are not arranged in distinct rows, whilst in row intercropping, two or more species are cultivated together, but in separate rows. With strip intercropping, several rows of one species are alternated with several rows of another species. Finally, in relay intercropping, two or more species are grown together during at least part of their life cycles (Andrews & Kassan, 1976). An intercropping system can either contain two or more economically important crops, or a marketable crop combined with a plant species included to improve the productivity of the system. This could for example be a 8
nitrogen fixing species that at least in a longer perspective may contribute nutrients to the system and act as a soil improver, and also presumably lower infestations of pest insects. Besides the term intercropping, it should be acknowledged that diverse plant systems also may be referred to in terms such as polycultures, mixed cropping, undersowing, living-mulch and companion planting (Tukahirwa & Coaker, 1982; Andow, 1991; Finch, Billiald & Collier, 2003; Dixon et al., 2004; Hooks & Johnson, 2006).
Effects on pest insects in intercropping systems Vandermeer (1989) divided the mechanisms that might lead to reduced insect attack in intercropping systems into three hypotheses: The Disruptive Crop Hypothesis (1) (which is closely linked to Root´s (1973) Resource concentration hypothesis), in which the intercrop disrupts a specialised herbivorous insect pest from attacking its host; while The Trap Crop Hypothesis (2) states that reduced insect damage can be achieved if the insects are more attracted by an alternative host (Hokkanen, 1991). The third mechanism proposed by Vandermeer (1989) is the Enemies Hypothesis (3), originally developed by Elton (1958) and Root (1973), in which a diverse habitat is believed to attract and retain more enemies of insect pests. Compared with a monoculture, adding more plant species to a system affects herbivores in two major ways. Firstly, the environment of the host plants, e.g. neighbouring plants and microclimatic conditions, is altered and secondly, host plant quality, e.g. morphology and chemical content, is altered (Langer, Kinane & Lyngkjær, 2007). The simultaneous effect on both environment and quality may complicate comparisons between systems, as several mechanisms affect herbivorous insects at the same time (Bukowinzky et al., 2004). Changes in environment and host plant quality lead to direct effects on the host plant searching behaviour of herbivorous insects, as well as indirect effects on their developmental rates and on interactions with natural enemies. The mechanisms behind the direct effects of intercropping have been investigated further by Finch & Collier (2000), who developed the theory of Appropriate/inappropriate landings. This theory states that when an herbivorous insect lands on an intercrop plant instead of a host plant, its behavioural sequence is disrupted (Finch & Collier, 2000). These authors suggest that insects use a three-link chain during host selection in which the initial link is governed by volatile host plant chemicals (Nottingham & Coaker, 1985), the central link by visual stimuli (Finch & Collier, 2000) and the final link by non-volatile chemicals (Simmonds et al., 1994). It is in the central link that disruption occurs, as insects are attracted to land on any green surface and avoid landing on bare soil (Kostal & Finch, 1994; Finch & Collier, 2000). When insects make an inappropriate landing, the behavioural sequence is disrupted and they have to ‘locate’ the host plant all over again. It has been suggested that the effect of intercropping on herbivore behaviour is exaggerated in small-scale experiments, as insects can move freely between the diverse treatments and the controls (Bergelson & Kareiva, 1987; Bommarco & Banks, 2003). The controls, often a pure stand of host plants, then function as a 9
trap crop, suffering higher herbivore densities and damage. The response to vegetation diversity varies for insect herbivores (Andow, 1991), and is most likely to be dependent on factors such as breadth of diet (Andow, 1991), insect search mode (Hambäck, Pettersson & Ericson, 2003; Bukowinszky et al., 2005) and life history aspects (Åsman & Ekbom, 2006). When evaluating the responses of a specific insect species to intercropping, one must consider both behavioural responses to intercropping per se, and responses to the design used in the particular experiment. The indirect consequences of intercropping include effects on the natural enemy community. Pest natural enemies, both parasitoids and generalist predators, have proved to be an important factor in biological control, and recent studies have also aimed to translate control efficiency into monetary values, with promising results (Östman, Ekbom & Bengtsson, 2003). Whether the effect of natural enemies is enhanced in diverse habitats is, however, debatable. The Enemies Hypothesis suggests that the effect of natural enemies is enhanced in mixed cropping systems, because these systems provide a variety of microhabitats and alternative prey (Root, 1973). However, The predictions of the Enemies Hypothesis are likely to vary between generalist and specialist natural enemies, as the latter are unlikely to benefit from the presence of alternative prey that should favour generalists. Specialists are expected to accumulate in simpler habitats, where their specific prey usually achieve higher densities and are easier to find (Sheenan, 1986). However, parasitoids utilising flower resources have benefited from more diversified systems (Lavandero et al., 2005). Examinations of the effect of plant diversity on generalist natural enemies have often shown an increased abundance in diverse systems (Booij, Noorlander & Theunissen, 1997; Denno, Finke & Langelotto, 2005). However, there are variations in the responses not only among predator species, but also within the same species when different studies are compared (Tukahirwa & Coaker, 1982; Rämert, 1996a; Armstrong & McKinlay, 1997), and these differences are likely to be explained by factors such as prey density (Bryan & Wratten, 1984), prey preference hierarchies of specific natural enemy species, and habitat preferences (Thiele, 1977). Besides an alteration in the host plant environment of intercropping systems directly affecting herbivore behaviour, crop plants in intercropping systems often compete with the intercrop for resources such as light, water and nutrients. These factors may have consequences for plant growth (Langer, 1996; Rämert, 1996b), morphology (Hooks & Johnson, 2001) and chemical composition (Stamp et al., 2004; Osier & Jennings, 2007), which in turn could affect host plant finding and acceptance by herbivores (den Belder, Elderson & Vereijken, 2000). Indirectly, this might also change the suitability of the crop plant as a food source for insect herbivores (Simpson & Raubenheimer, 1995), which could have consequences for their development rates (Bukowinszky et al., 2004; Osier & Jennings, 2007). Among plant quality traits found to affect herbivore development are their fibre and nutrient contents (Bethke et al., 1987; Hunt, Drury & Maw, 1992; Hochuli, 1993), which can both be affected by environmental conditions (Widdicombe & Thelen, 2002; Osier & Jennings, 2007), and might therefore be expected to vary between monocultured and intercropped plants. 10
Furthermore, plant competition in intercropped systems may affect the allocation of resources to either plant growth or to the maintenance of their defence mechanisms (Herms & Mattson, 1992). In cruciferous plants, the sulphur and nitrogen containing glucosinolates are considered to be an important part of their defence system against herbivores and pathogens (Mithen, 2001; Halkier & Gershenzon, 2006). When plant tissues are damaged, the glucosinolates are hydrolysed by plant myrosinase enzymes, and a wide range of volatile and nonvolatile compounds are produced, of which the isothiocyanates (mustard oils) are the best known (Mithen, 2001). These compounds are largely responsible for the characteristic flavours of crucifers and are toxic to generalist herbivores (Giamoustaris & Mithen, 1995; Kliebenstein et al., 2002). Specialised herbivores, on the other hand, use glucosinolates and isothiocyanates in their host plant finding and acceptance (Nottingham & Coaker, 1985; van Loon et al., 1992; Renwick, 2002). Glucosinolate concentrations change in response to herbivore damage (Koritsas, Lewis & Fenwick, 1991; Bartlet et al., 1999; van Dam & Raaijmakers, 2006), but also to environmental stress factors (Yusuf & Collins, 1998; Radovich, Kleinhenz & Streeter, 2005). As plants are rarely subjected to only competition or herbivory, there are likely to be interactive effects which may have consequences for plant quality aspects such as fibre, nutrients and the concentration of glucosinolates, and hence for the development of feeding herbivores.
The turnip root fly - Delia floralis Biology The turnip root fly (Fig. 1), Delia floralis Fallén (Diptera: Anthomyiidae), is considered to be an economically important pest on cruciferous crops in the north temperate region, including the countries of Fennoscandia: Sweden (Lundblad, 1933), Denmark (Jørgensen, 1957; Bromand, 1980), Norway (Andersen et al., 1983) and Finland (Varis, 1967), as well as Canada (Brooks, 1951), Scotland (Morison, 1939) and Russia (Vasina, 1927). The fly larvae feed on the root system of their host plant, which can lead to decreased plant growth, or death of the plant. Host plants of D. floralis include different varieties of Brassica oleracea L., e.g. cabbage, cauliflower, kale and broccoli, and Brassica napus L., e.g. swede and canola (oilseed rape) (Morison, 1939; Brooks, 1951; Broatch & Vernon, 1997). The turnip root fly shares many of its biological and behavioural traits with its close relative the cabbage root fly, Delia radicum L. (Varis, 1967; Baur et al., 1996a). The geographical distribution of these two species overlaps, but D. radicum has a more southerly distribution (Coaker & Finch, 1971). Where the two species occur together, the proportions of the two species in the total population vary between locations and years (Sundby & Taksdal, 1969; Paper II). When they occur together, the emergence of D. floralis seems to be some weeks later than that of D. radicum (Varis, 1967; personal observations by the author). The female turnip root fly lays small white oval eggs 1.10 ± 0.008 mm long (Varis, 1967). The eggs are laid close to the host plant, preferably in crevices in 11
the soil (Havukkala & Virtanen, 1985). Under laboratory conditions, female flies lay about 55 eggs in the first batch, after which the egg numbers decrease continuously in subsequent batches (Havukkala & Virtanen, 1984). Cage experiments have shown that after emerging from the pupae, the females begin to lay eggs after 8 days on average (Havukkala & Virtanen, 1984), and oviposition then lasts for about 3 weeks (Varis, 1967).
Fig. 1. A turnip root fly, Delia floralis, female.
The egg stage lasts about 8 days (Varis, 1967), and after hatching the neonate larvae burrow into the plant roots to feed. Larval development includes three stages. When the larvae are fully developed, after 5-7½ weeks (Varis, 1967), they move down into the soil and pupate at a depth of about 10 cm, but sometimes as deep as 23 cm, from the soil surface (Morison, 1939). The pupal stage is the stage in which the turnip root fly overwinters. Delia floralis is considered to be univoltine (Morison, 1939; Brooks, 1951), but in certain places in Denmark two generations have been encountered (Jørgensen, 1957), and in Finland there are reports of at least a partial second generation in warm years (Varis, 1967).
Behaviour The pre- and post-alightment behavioural process has been investigated for both root fly species (Havukkala & Virtanen, 1985; Kostal & Finch, 1994; Hopkins et al., 1996; Städler & Schöni, 1990) and their behaviours seem to be similar. During the host location process, which is completed through oviposition by female flies, a broad spectrum of stimulatory cues operates, and the relative importance of these different cues depends on the specific stage in the behavioural process. Gravid D. floralis females arrive in a brassica field through a series of short (2 m) flights, re-orientating towards the wind between landings (Havukkala, 1987). Volatile host plant compounds, such as the isothiocyanates, elicit up-wind movement of D. radicum (Havukkala, 1982; Nottingham & Coaker, 1985), and D. floralis has shown similar behaviour in the presence of host plant odour (Havukkala, 1987). In the vicinity of host plants, the importance of visual stimuli has been determined for D. radicum, which is attracted to land on green surfaces at a distance of 40-60 cm from the host plant (Prokopy, Collier & Finch, 1983). Havukkala (1987) also assumed that visual stimuli were important for D. floralis as the female flies flew directly towards green traps at close range. Leaf area seems to be of greater importance than leaf form in stimulating landing by D. radicum (Roessingh & Städler, 1990). Furthermore, plants that are grown on bare 12
soil are more attractive than undersown plants, probably because they are more visually conspicuous to the flies (Kostal & Finch, 1994). After a fly has landed on a host plant, it is suggested that volatile cues enhance its response to the host plant, even if these compounds alone do not induce oviposition (de Jong & Städler, 1999). In addition, contact cues have been shown to be important for the ensuing behaviour and final host acceptance (Simmonds et al., 1994). The non-volatile glucosinolates have long been considered to be the main contact cues for both D. floralis and D. radicum (Städler, 1978). More recent studies have found non-volatile compounds that are even more stimulating than the glucosinolates as conditioning cues for oviposition (Hurter et al., 1999; Hopkins et al., 1997). Cabbage Identification Factors or CIFs (thia-triazafluorene compounds), have been found on the leaf surface of crucifers in very low concentrations compared to the glucosinolates, which have been found in concentrations about 6 x 104 times higher than that of the CIF compounds (Roessingh et al., 1992; Roessingh et al., 1997). However, glucosinolates alone, for example glucobrassicin (Gouinguené & Städler, 2006), induce oviposition in both D. floralis and D. radicum. In addition, other factors such as leaf surface waxes may affect the ability of insects to detect oviposition stimulating compounds (Roessingh & Städler, 1990). Post-alightment behaviour includes a specific sequence of behavioural stages, culminating in oviposition at the base of the plant stem. Havukkala & Virtanen (1985) divided the post-alightment behavioural process for D. floralis into six stages: (1) landing, (2) extension of the proboscis and examination of the leaf surface, (3) walking over the leaf, (4) running down the stem, (5) walking on the ground at the base of the stem and (6) oviposition. After making the initial landing on a leaf, D. radicum performs short, so-called ‘spiral flights’ around the plant canopy as part of the exploration process (Kostal & Finch, 1994), and this behaviour has also been observed in D. floralis (personal observations by the author). Oviposition behaviour can be aborted at any of the stages described (Havukkala & Virtanen, 1985), but comparison of the behaviour on susceptible and resistant brassica plants has revealed that cues perceived immediately after landing on a leaf (the so-called leaf contact phase) are crucial for acceptance, or rejection, of the plant as a oviposition site (Hopkins et al., 1996, 1999). In the final stage before oviposition, flies also perceive cues emanating from the roots. Female D. radicum prefer to oviposit on plants where conspecific larvae have fed for 4-5 days (Baur et al., 1996b). The changes induced by larval feeding were not detected on the leaf surface, which indicates that contact or volatile cues at ground level are important for oviposition. In addition, specific egg-associated compounds, recently identified as CIF compounds, stimulate oviposition by conspecific females (Gouinguené, Poiger & Städler, 1996). These two mechanisms may explain the aggregated oviposition pattern found for D. radicum in the field (Mukerji & Harcourt, 1970).
Natural enemies Carabids are known to feed on immature stages of dipteran pests and have been widely studied for their potential in biological control (Coaker & Williams, 1963; van Dinther & Mensink, 1971; Finch & Elliot, 1992; Finch, 1996). The potential rate of egg consumption varies between species, and depends on factors such as body size. Laboratory experiments have revealed a positive linear relationship between the numbers of eggs eaten and carabid body size within the 2.7 to 10 mm size range. Species of Agonum, Amara, Bembidion and Harpalus were among those species that had a high consumption rate in relation to their body size (Finch, 1996). van Dinther and Mensink (1971) found that Bembidion spp. were dominant egg predators in cabbage fields, while other groups only consumed eggs occasionally. Larger species (>10 mm), such as Pterostichus melanarius, seem to have a low interest in Delia eggs (Finch & Elliot, 1994). Staphylinids have been studied less thoroughly for their ability to predate dipteran eggs, but two Aleochara species, A. bilineata Gyll. and A. bipustulata L. (Coleoptera; Staphylinidae), are known to attack root fly eggs (Coaker & Williams, 1963; Andersen et al., 1983). Aleochara adults have the capacity to eliminate a considerable quantity of D. radicum eggs, larvae and pupae. According to laboratory studies, individual A. bilineata beetles are capable of eating 25 D. radicum eggs per day (Langlet & Brunel, 1996) or about 600 eggs during their lifetime (Read, 1962). Aleochara bilineata also predates on later developmental stages (Hartfield & Finch, 2003). Both Aleochara species also function as parasitoids on root fly pupae, with A. bilineata as a specialist attacking mainly Delia species (Wishart, 1957; Maus, Mittman & Peschke, 1998), while A. bipustulata is considered to be more of a generalist (Maus, Mittman & Peschke, 1998). Trybliographa rapae Westw. (Hymenoptera; Cynipidae) is also a common parasitoid of Delia spp. It is a larval parasitoid that preferably attacks the early larval instars of its host (Wishart & Monteith, 1954).
Development and food quality The development of D. floralis and D. radicum has been reported to vary depending on host plant species, resulting in differences in the percentage pupating successfully and the final pupal weight (Finch & Ackley, 1977; Hopkins et al., 1995). The factors affecting D. floralis development are relatively unknown, but a high content of root neutral detergent fibre (NDF) may affect D. floralis larval growth negatively, leading to lower pupal weights (Hopkins et al., 1995). NDF includes cellulose, hemicellulose and lignin as major components (van Soest, Robertson & Lewis, 1991). Reports on the digestibility of NDF vary between species, but is usually considered to be low (Hochuli, Sanson & Roberts, 1993), and is generally associated with a decrease in host plant quality for herbivorous insects (Hochuli, 1996). The content of NDF is likely to vary between host plants (Hopkins et al., 1995) as is nutrient (Osier & Jennings, 2007) and glucosinolate concentration (Birch et al., 1992; Griffiths, Birch & MacFarlane-Smith, 1994). Although it has not been studied in D. floralis, a high nitrogen level is considered to be positive for herbivore development (Bethke et al., 1987; Hunt, Drury & 14
Maw, 1992). However, the effect of host plant glucosinolate concentrations on the development of crucifer specialists has not shown consistent patterns (Cole, 1997; Agrawal & Kurashige, 2003). Against this background of knowledge, the present study aimed to investigate how intercropping affects the different stages of the life cycle of D. floralis, with the emphasis on behaviour, natural enemies and host plant quality, in order to evaluate the potential of this strategy as a control method for D. floralis. A field trial was designed to investigate the relative impact of the effects on D. floralis oviposition behaviour and the effects on natural enemies in the same system. A separate experiment was performed to assess the effects of intercropping density and D. floralis egg density on host plant quality and the development of D. floralis.
Materials and Methods The thesis comprises of a field trial performed in two successive years and a greenhouse experiment.
Field trial The aim of the field trial was to study the effect of intercropping on D. floralis oviposition, as well as the effects of natural enemies on the fly population. The field trial was located at Röbäcksdalen in Umeå (63º45’N; 20º15’E) and consisted of alternating plots (15 m x 15 m) with cabbage monocultures (Brassica oleracea var. capitata genotype Castello) and plots with row intercropping of cabbage and red clover (Trifolium pratense genotype Betty) (Fig. 2). The red clover was sown in the whole field in the previous season and was incorporated into the field as green manure before the transplanting of the cabbage plants. Strips of red clover, 20 cm wide, were left running through the plots aimed for intercropping. The distance between cabbage rows was 70 cm in both treatments, and within row plant distance was 40 cm. The field trial in 2004 was performed at a distance of approximately 40 m from the field trial of the previous year. The effect on D. floralis oviposition and the effect on the natural enemy community were measured in both study years. In 2003, pilot studies of egg predation, total predation and parasitization were performed, and the methods were modified for the field season of 2004. In both 2003 and 2004, oviposition was examined throughout the oviposition period from early July to the middle of August. This was done with felt egg traps placed on the stem of the cabbage plants (Freuler & Fischer, 1982) and sampled two times a week for egg counts (Papers I & II).
= Oviposition transect
Fig. 2. The two different cultivation systems tested in the field trial at Röbäcksdalen in Umeå. Left, a cabbage monoculture and right, intercropping between cabbage and red clover. Underneath is the design of the field experiment.
During both seasons, the natural enemy community was monitored with pitfall traps. This method is far from problem-free, especially when comparing two treatments that differ in plant complexity (Greenslade, 1964), but no attempt was made here to measure absolute abundance. Thus, the aim was to measure the presence of different species and their activity-densities (Mitchell, 1963). Pitfall traps were emptied two times per week (Paper II) and species of Carabidae and Staphylinidae were counted and identified to species. In 2004, a study of egg predation was performed by placing D. floralis eggs in the field in a density comparable to a natural egg batch size (30 eggs). Eggs from a fly culture kept at Röbäcksdalen were placed in the field repeatedly during the oviposition period and were recollected in order to count the remaining eggs and examine them for predation marks (Paper II). Total predation was estimated by using predator exclusion barriers (Fig. 3). The resulting pupae inside and outside the barriers were sampled in early autumn (Paper II). Parasitization rates were estimated from pupal samples both in 2003 (40 per plot, presented only in this thesis) and in 2004 (35 per plot, Paper II). To summarise the overall survival of D. floralis in the field, comparisons of oviposition and final pupal numbers in both intercropping and monoculture are presented below.
Fig. 3. A predator exclusion barrier in the cabbage monoculture.
Greenhouse experiment A greenhouse experiment (Fig. 4) was performed to investigate the effects of intercropping and herbivore density on the development of D. floralis (Paper III), and the responses of plants with respect to growth and content of fibre, nutrients (Paper III) and glucosinolates (Paper IV). Cabbage plants were grown in monoculture (M) or in one of two clover densities (IC1 & IC2). Eggs of D. floralis eggs were inoculated onto 6-week-old plants at the 6-7 true leaf stage in four different densities (0, 10, 20 or 40 eggs), and the fly larvae were able to feed until pupation. After six weeks, the experiment was terminated. Cabbage plants were weighed (aerial parts and roots separately) and plant samples were taken for analyses of total nitrogen and carbon of cabbage roots and shoots, cabbage root NDF (neutral detergent fibre) and lignin (Paper III), as well as the glucosinolate concentrations of cabbage foliage and roots (Paper IV). The pupae were washed out from the soil, counted and weighed (Paper III).
Fig. 4. Overview of the greenhouse experiment.
Statistical analyses The effect of cultivation system on total oviposition (Paper I) was analysed with analysis of variance (ANOVA). To investigate the effects of adjoining treatments on the spatial distribution of eggs, an analysis of covariance was performed (ANCOVA). To examine the distance the border effect extended into the plots, a gliding window was used, analysing four distances at a time with an ANCOVA. When a threshold value was found, which indicated the extent of the border effect, the two cultivation systems were analysed separately with linear regressions to examine whether one or both treatments were causing the border effect. The effect of cultivation system on oviposition with edge effects excluded (Paper II) was analysed with a two-way ANOVA. The egg predation rates over time were first analysed with a nested ANOVA, and then with two-way ANOVAs for each sampling date as a planned comparison. The effects on total predation and parasitization rates were analysed with split plot ANOVAs and the likelihood of the presence of at least one pupa parasitized by T. rapae per plant was analysed with GLM (Paper II). The pitfall trap catches of groups of carabids and staphylinids were analysed with a two-way ANOVA (Paper II), and this analysis was repeated for Bembidion spp., A. bipustulata, ‘other carabids’ and ‘other staphylinids’ separately (Paper II). To compare the activity-densities of individual predators between cultivation systems, we used a blocked Multi-Response Permutation Procedure (MRPP, Zimmerman, Goetz & Mielke, 1985), and an indicator species analysis as a post-hoc test (Dufrene & Legendre, 1997) with the default number of randomisations (1 000) in PC-ORD 4.25 (McCune & Mefford, 1999). The MRPP analysis was only done for 2004 due to a lack of power in the 2003 data (Paper II). The effects of intercropping and egg density on cabbage growth, fibre and nutrient content and on D. floralis pupal weights were analysed with ANCOVAs (Paper III). For the glucosinolate analysis (Paper IV), separate MANOVAs were performed for foliage and root samples. GLM analyses were used to analyse individual glucosinolates, as well as the groups of aliphatic and indole glucosinolates and the total concentrations in cabbage roots and foliage. Correlation analyses were carried out to identify possible correlations between insect development and plant growth, NDF, lignin, carbon and nitrogen content (Paper III), as well as glucosinolate concentrations (presented only in this thesis). Transformation of data was performed when needed to fulfil assumptions on normality and equal variances. All analyses, except for the MRPP analysis (Paper II), were made using S-PLUS statistical software (Insightful Corp. Seattle, USA. S-PLUS® 6.0).
Results and discussion Behavioural effects Quantity and distribution of eggs Oviposition measurements in the field trial showed that oviposition by Delia floralis was reduced considerably in the intercropped plots compared with the monoculture plots in both study years (Papers I & II; Fig. 5). The overall reduction in oviposition in the intercropped plots, compared with the monoculture plots, was 42% in 2003 and 55% in 2004 (Paper I). The duration of the oviposition period extended from early July to the middle of August, with a peak in oviposition around July 20 in both years (Paper II). Furthermore, oviposition in 2004 was around 6 times greater than in 2003. Oviposition by Delia floralis Eggs / trap & day
25 20 15 10 5 0
27-Jul 06-Aug 16-Aug 27-Jun 07-Jul
27-Jul 06-Aug 16-Aug
Fig. 5. Oviposition by D. floralis during 2003 and 2004 in monoculture and intercropped plots (Paper II). Analysis of the distribution of eggs within the experimental plots showed a decreased oviposition in intercropped plots and an increased oviposition in monoculture plots close to the border between treatments (Paper I), although this effect was only statistically significant in 2004. Consequently, the difference in oviposition between the monoculture and intercropped plots was greatest close to the border. The difference in egg numbers decreased with distance from the border up to a distance of 3.5 m into the plots (Fig. 6). The mechanisms behind the reduced oviposition in the intercropped plots in both years are likely to be found in the behaviour of the gravid female flies (Finch & Kienegger, 1997), and in the specific cues used during their oviposition behavioural sequence (Prokopy, Collier & Finch, 1983; Simmonds et al., 1994). In many cases, initial colonisation of intercropped and monoculture treatments is similar, with for example D. radicum arriving to a cabbage-clover system (Tukahirwa & Coaker, 1982). Therefore, the odour of clover does not seem to interfere with the host location process pre-alightment, although this has been proposed for certain non-host plant odours (Nottingham, 1987). The main reason
for reduced oviposition in the intercropped plots is therefore likely to be factors operating after the flies arrive in the field. After flies have arrived in a field, the capacity of a specific plant-intercrop system to lower pest infestations is determined by both the behavioural and biological attributes of specific herbivores. It is suggested that the number of ‘appropriate’ landings an insect has to make during the behavioural sequence is a key factor determining the value of intercropping for pest control (Finch & Collier, 2000). The ability of a specific insect species to perceive and orientate towards visual and olfactory cues is crucial and may affect the probability of making landing ‘mistakes’. In the vicinity of a host plant, vision is the main stimulus eliciting landing on any green surface by D. radicum (Prokopy, Collier & Finch, 1983). As D. radicum has been shown to perform an average of four socalled ‘spiral flights’ during its oviposition behavioural sequence (Kostal & Finch, 1994), there is a high risk for behavioural disruption through ‘inappropriate landings’. Delia floralis females share the general pattern of their host selection behaviour with D. radicum (Hopkins et al., 1996; personal observations by the author), and the present study has demonstrated the disruptive capacity of intercropping for D. floralis (Papers I & II). The number of host plant contact phases required to achieve oviposition probably varies both between, as well as within, the same species. Thus, a host plant of low quality may need more ‘appropriate landings’ before being accepted (Finch & Collier, 2000). Furthermore, an insect’s pattern of movement in the vicinity of a host plant, and the specific intercropping system, will determine the number of interactions that occur between the insect and the intercrop, and thus influence the probability of making ‘inappropriate landings’. The pattern of movement is, in part, determined by the location of the oviposition site. For example, intercropping seems to have a large effect on insects that oviposit in the soil, such as the cabbage root fly and the turnip root fly (Finch & Kienegger, 1997; Papers I & II), the carrot fly (Psila rosae F.) (Rämert & Ekbom, 1996) and the onion fly (Delia antiqua Meigen) (Finch, Billiald & Collier, 2003). An important factor influencing the reduction in oviposition may be the interaction with the intercrop during the insect’s vertical movement from the host plant foliage down to the soil. This may be one of several factors explaining the reduced effect of intercropping on some leaf ovipositors such as the diamond back moth (Plutella xylostella L.) (Finch & Kienegger, 1997) and the leek moth (Acrolepiopsis assectella Z.) (Åsman, Ekbom & Rämert, 2001). An explanation of the greater difference in egg density near the border between the intercropped and monoculture plots (Fig. 6) may be that the flies in parts of the intercropped plots close to the border have a higher probability of entering the monoculture than flies in the centre. When flies enter the monoculture plots, they can oviposit without disruption from the clover. In addition, as the final choice to decide where to land is based on visual cues (Prokopy, Collier & Finch, 1983), the visual stimulus of a host plant growing with a background of bare soil (Kostal & Finch, 1994) might further motivate flies to stay in, or fly into, the monoculture.
The border effect was most pronounced in the intercropped plots (Paper I). The more homogeneous egg distribution in the monoculture is probably explained in part by increased mobility of the flies in this treatment. In an intercropping situation, D. radicum spends considerable periods of time inactive on non-host plant leaves (Morley, Finch & Collier, 2005). For D. floralis and D. radicum, the time spent on the foliage of a non-host plant (Morley, Finch & Collier, 2005) or a resistant plant (Hopkins et al. 1996, 1999) has been shown to be longer than the time spent on a host plant, and such inactive periods may contribute to the reduced oviposition by D. floralis in intercropping systems (Morley, Finch & Collier, 2005). However, the arresting effect of contact with non-host plants or resistant cultivars does not seem to be general for all species, as the cabbage moth (Mamestra brassicae L.) and the leaf mining fly (Liriomyza trifolii Burgess), for example, spend less time on non-preferred host plants or non-host plants compared with host plants (Bethke & Parella, 1985; Rojas, Wyatt & Birch, 2000). Effect of the border 700 600 Eggs
500 400 300 Border plant
Di stance from the border (m)
Fig. 6. The effect on D. floralis oviposition of distance from the border between intercropped and monoculture plots in 2004 (Paper I).
Besides behavioural factors, life history aspects such as the insect’s response to host plant deprivation may also influence the magnitude of the reduction in attack in intercropping systems. Insects deprived of a preferred resource may accept a previously unacceptable resource, as with ovipositing checkerspot butterflies (Euphydryas editha) (Singer, 1982). If insects become less discriminating in response to failed oviposition attempts and if deprived individuals have the ability to postpone oviposition, as shown for the leek moth (Åsman & Ekbom, 2006), the effect of plant diversity may decrease with time. Whether D. floralis becomes less discriminating with time is still unknown, but it is not unlikely that the border effect found in this field trial may have been enhanced because deprived females finally encountered a suitable host plant. Some caution is needed when interpreting results from studies of intercropping, as the cultivation system often leads to interspecific competition, which in turn can lead to physiological differences between intercropped and monocultured plants (Bukovinszky et al., 2004). For example, it has been shown that plant size can 21
have an effect on preference for D. radicum in a choice situation (Kostal & Finch, 1994) and that increased leaf area stimulates more landings (Prokopy, Collier & Finch, 1983). In the field trial reported here, the intercropped cabbage actually performed slightly better at the beginning of the oviposition period (Rämert et al., unpublished data). Hence, if D. floralis had been attracted to larger plants, this would rather have reduced the difference in oviposition between the treatments. At the beginning of August, the cabbage in the monoculture started to outgrow the intercropped cabbage. At this stage the main proportion of the eggs had already been laid, so the effect of plant size appears to have been less important in this experiment. Other aspects of host plant quality that may have importance for ovipositing females, such as morphological aspects or glucosinolate levels, were not measured during the oviposition period. Similarly to several other studies of intercropped systems, final crop yield suffered from reductions through competition with the intercrop, and cabbage yield was reduced by approximately 38% in the intercropped plots (Rämert et al., unpublished data). As the primary aim of this field trial was to examine the potential of intercropping for pest control, the measures for reducing competition were few (Papers I & II). For a practical use of intercropping systems, account must be taken of both the pest disruptive capacity of the cropping system and minimising competition with the main crop. These goals may both be achieved through careful consideration of choice of crop and intercrop species, as well as practical measures to prevent competition, e.g. through root pruning of the intercrop (Båth et al., submitted).
Effects on and of natural enemies Effects on natural enemy activity-densities The species caught in the pitfall traps were subdivided into four groups: Bembidion spp., Aleochara bipustulata, ‘other carabids’ and ‘other staphylinids’. This subdivision was based on their numbers and known potential as predators of root fly eggs (Coaker & Williams, 1963; van Dinther & Mensink, 1971; Andersen et al., 1983; Finch & Elliot, 1992; Finch, 1996; Langlet & Brunel, 1996). In both years, the activity-densities of carabid beetles were higher in the monoculture. This result was explained largely by species of the Bembidion family (mainly B. quadrimaculatum L., B. bruxullense Wesmael and B. lampros Herbst), which were caught predominantly in the monoculture plots. The effect of cultivation system on Bembidion spp. was somewhat stronger in 2003. The numbers of ‘other carabids’ caught did not differ between the cultivation systems. The distribution of other individual carabid species between cultivation systems was similar between the years, and the MRPP analysis of the 2004 data showed that only Pterostichus niger Scall. was caught more often in the intercropped plots than in the monoculture. In addition, species such as Calathus melanocephalus L., Trechus secalis Paykull and P. melanarius Ill. dominated the pitfall trap catches in the intercropped plots. Aleochara bipustulata was the dominant staphylinid species in both years and was captured almost exclusively in the monoculture (Paper II). Furthermore, the effect of cultivation system on A. bipustulata activity-densities 22
was stronger in 2004. The group of ‘other staphylinids’ responded with a higher activity-density in the intercropped plots in 2003, while trap catches for 2004 were similar in the two treatments. Similar patterns were observed in the species distribution of ‘other staphylinids’ between years. In 2004, Aloconota gregaria Er. and Anotylus rugosus F. were trapped more frequently in the monoculture plots. Only Oxypoda umbrata Gyll. and Mocyta orphana Er. had higher activitydensities in the intercropped plots, even though M. fungi Grav. tended to have a similar response. Even though the majority of studies have found increased predator densities in diversified systems (Andow, 1991), there is undoubtedly a large variation in the response of different carabids and staphylinids towards diversification (Tukahirwa & Coaker, 1982; McKinlay, 1993; Rämert, 1996a; Armstrong & McKinlay, 1997; Booij, Noorlander & Theunissen, 1997). The responses to increased vegetation diversity are probably based on the habitat preferences of different species (Thiele, 1977), but may also be influenced by the explicit design of the systems studied (Bommarco & Banks, 2003). Because the design of this field trial meant that different treatments were adjacent to one another, it is likely that the differences in activity-densities are a result of a redistribution of the natural enemy community at this site. Some insects may have inhabited both treatments, for example Pterostichus melanarius, which has been shown to forage in monocultures during the night but to remain in intercropped areas during the day (Chapman, Armstrong & McKinlay, 1999). The temporal dynamics of carabid and staphylinid activity-densities in 2004 showed that the increases in numbers of A. bipustulata and Bembidion spp. occurred mainly during the early part of the summer, while there were only small differences in the activity-densities of the remaining species throughout the season (Paper II). Bembidion spp. and A. bipustulata were treated separately in this study because of their high numbers and their potential as predators on Delia spp. As the responses of Bembidion spp. and A. bipustulata where most apparent early in the season when egg densities were fairly low and egg numbers where similar in both cultivation systems, it seems likely that the main effect on these species was a response to other habitat factors, and to a lesser extent to D. floralis egg densities. This conclusion is further supported by the strong respons in Bembidion spp. in 2003 when egg densities were relatively low (Paper II).
Predation and parasitization The specific studies of total predation and egg predation indicated that the predation pressure was similar in the two cultivation systems. If there was any trend at all, it was towards a higher predation pressure in the monoculture, which was especially apparent from the experiment using the predator exclusion barriers. Comparison of pupal numbers inside and outside the barriers gave an estimate of 41% mortality due to predation in the monoculture and 21% in the intercropped treatment (Paper II; Fig. 7). Pilot studies on egg predation in 2003 indicated that there was no difference between the cultivation systems in egg predation rates, and this was confirmed in the field trial in 2004. During 2004, there were no consistent 23
patterns in differences in predation levels between the two cultivation systems, or between predator activity-densities and egg predation rates during the season (Paper II). Overall, parasitization rates were low in both 2003 (monoculture 6.3%, intercropped 2.3%) and 2004 (monoculture 5.3%, intercropped 4.6%) and did not differ between the cultivation systems. Trybliographa rapae was the main species of parasitoid. A small number of pupae parasitized by Gnotus spp. or by Aleochara bipustulata were also found. In 2004, when pupal numbers were high, there was a density-dependent response between numbers of pupae per plant and the likelihood of at least one pupa being parasitized by T. rapae. This pattern was similar in both cultivation systems. Parasitization by A. bipustulata is likely to have been underestimated because a closer inspection of pupae suggested that A. bipustulata had already hatched at the time of sampling. Effect of barrier 100
Inside barrier Outside barrier
80 60 40 20 0
Fig. 7. Comparison of pupal numbers inside and outside barriers (mean ± SEM) in monoculture and intercropping (Paper II).
Predictions made by the Enemies Hypothesis of a greater effect of natural enemies in diverse systems (Root, 1973) have been both confirmed (Letourneau & Altieri, 1983) and contradicted (Andow & Risch, 1985), while in the present field trial the effects of both predators and parasitoids were similar (Paper II). Similarly, an earlier study using predator exclusion barriers did not reveal any differences in egg predation pressure due to vegetation diversity (Tukahirwa & Coaker, 1982), and our study suggests that this lack of effect persists into the pupal stage. For the predation studies, the lack of effect could be explained by comparable differences between systems in predator activity-densities and D. floralis egg numbers, creating similar predator:egg ratios. The applicability of the Enemies Hypothesis to specialist natural enemies has been questioned, as they are expected to accumulate where prey densities are higher (Sheenan, 1986). The low parasitization rates by T. rapae in this field trial did not show any densitydependent effects, although these were found previously by Jones & Hassell (1988) (Paper II). The similar parasitization rates in monoculture and intercropped plots confirm earlier studies, which found no effect of plant diversity on the host finding efficiency of T. rapae (Hartfield, Nethercleft & Finch, 1999).
Survival of D. floralis in the field Even though oviposition differed significantly between the two cultivation systems in both study years, pupal numbers differed only in 2004 (Table 1). The pupa:egg ratio, which may be regarded as a measure of survival, was similar between cultivation systems in 2004. This further confirms that there was similar predation pressure in both the monoculture and intercropped plots during this season. In 2003, survival seems to have differed between systems, as pupal numbers were similar. As they were not measured in 2003, differences in predation pressure between treatments cannot be excluded, and the stronger effect of treatment on Bembidion spp. in this year (Paper II) may have led to stronger predation pressure in the monoculture, which could have resulted in similar numbers of pupae in the two systems. However, this result also raises questions about the abiotic factors affecting survival rates in the two systems. The immature stages of D. floralis and D. radicum are sensitive to high temperatures and desiccation (Vodinskaya, 1928; Coaker & Finch, 1971; Mukerji, 1971), which is considered to contribute to their high overall mortality (Mukerji, 1971). The mean temperature during the period of peak oviposition was approximately 3 ºC higher in 2003 than in 2004, which may have led to higher survival in the intercropped plots as a result of a more stable microclimate in terms of temperature and humidity (Potts, 1990; Bodreau, 1993; Fininsa, 2001). Furthermore, even though both egg and pupal numbers are likely to have been underestimated in this study, the pupa:egg ratio indicates that only a minority of D. floralis eggs survive to the pupal stage. Table 1. Egg and pupal numbers sampled in 2003 and 2004 (mean ± SEM) and the pupa:egg ratio 2003 Eggs
76 ± 7
471 ± 13
51 ± 5
47 ± 8
246 ± 26
22 ± 3
Host plant quality and D. floralis development Cabbage N, C, NDF and lignin In the greenhouse experiment, there was a strong negative effect on the final weight of cabbage plants of competition through both increasing clover density and increasing egg number. This was reflected in both the aerial parts and the roots of the cabbage (Paper III). In addition, plant competition and larval feeding also resulted in higher levels of NDF (neutral detergent fibre) and lignin in the roots of the intercropped cabbage plants. There was also an interactive effect of intercropping and larval density on the lignin content, which was explained by an increase with larval density in the roots of intercropped plants, while the content was unchanged in roots of monocultured plants (Paper III; Fig. 8). The nitrogen content was higher in the roots of monoculture cabbage compared with 25
intercropped plants, while the amount of carbon was higher in the roots of intercropped cabbage. Both the nitrogen and carbon levels in cabbage roots increased with D. floralis egg density, while their content in the foliage was unaffected either by intercropping or feeding by root flies (Paper III). The negative effects of intercropping on the growth of cabbage and on the root:shoot ratio are predictable consequences of inter-specific plant competition for mutual resources such as light and nutrients (Theunissen, Booij & Lotz, 1995; Agele, Iremiren & Ojeniyi, 1999; Bonifas et al., 2005). The effects of nutrient availability were presumably more important in this study, considering the higher root:shoot ratio in intercropped cabbage plants (Bonifas et al., 2005). The higher nitrogen content of roots from the monoculture also points in this direction (Paper III), and the impaired cabbage growth due to larval feeding confirms the detrimental effect of root flies, especially on small brassica crop plants. The increase in the NDF and lignin contents of cabbage roots due to feeding by D. floralis corresponds to the response found in the roots of kale, rape and swede (Hopkins et al., 1995) and may be caused by two different processes: (1) D. floralis may choose to feed on the parts of roots that have a lower fibre content (Hopkins et al., 1995); or (2) the damage caused by feeding larvae may induce a plant response that increases the fibre content of the roots. Plants may respond by lignification when wounded or attacked by pathogens (Rittinger, Biggs & Pierson, 1987; Moerschbacher et al., 1990; Li et al., 2007), and an induced response to larval feeding damage may be one explanation for the pronounced increase in lignin content at high egg densities (Fig. 8). Root lignin
18 16 14 12 10 0
Fig. 8. Effects of intercropping density and Delia floralis egg density on the content of lignin in cabbage roots (% of root dry matter, DM) (M = monoculture, IC1 = low clover density, IC2 = high clover density).
Glucosinolate concentrations The analysis of glucosinolate content of the foliage and roots of the cabbage plants revealed a total of nine different glucosinolates, consisting of five aliphatic and four indole glucosinolates (Table 2). All were present in both the foliage and roots of cabbage plants in all treatments (Paper IV). Both intercropping and D. floralis 26
egg density affected the concentrations of glucosinolates in cabbage. Of the glucosinolates in the foliage, several decreased in concentration as a response to intercropping, and this resulted in a total decrease in the concentration of indole glucosinolates. The strongest responses in individual glucosinolates were for gluconapin, glucobrassicin and hydroxyglucobrassicin (Paper IV). The responses to insect root damage were less pronounced, with a slightly significant decrease in the concentration of the aliphatic glucosinolate progoitrin and the indole glucosinolate neoglucobrassicin. The total glucosinolate content of the cabbage foliage was not significantly affected by either clover competition or by the damage caused to the roots of the plants by D. floralis, even though there were strong tendencies towards a reduction (Paper IV; Fig. 9). Root glucosinolates responded more strongly to both intercropping and egg density and the responses of individual root glucosinolates were complex and, on occasions, non-linear. Most root glucosinolates decreased in response to clover competition, with the exception of the indole methoxyglucobrassicin, which increased, and neoglucobrassicin, which was unchanged. The total concentrations of indole glucosinolates in the roots increased in response to D. floralis damage. The aliphatic gluconsinolates decreased in damaged intercropped roots, but only at high egg densities. In monoculture roots, a decrease in concentration of aliphatic glucosinolates was only observed at low egg densities, which caused a non-linear response. However, there were exceptions to this pattern for individual glucosinolates within each group (Paper IV). Table 2. Different glucosinolates found in foliage and root samples of cabbage
The decreased concentrations of several glucosinolates in the cabbage foliage suggest that cabbage plants in competition with another species, and cabbage plants subjected to root herbivory, do not manage to allocate the same resources as unchallenged plants to sustain levels of leaf defence compounds. Lower concentrations of defence compounds have been shown previously in competing plants (Cipollini & Bergelson, 2001; Stamp et al., 2004), and may lead to increased herbivory on these plants (Cipollini & Bergelson, 2002). However, as several glucosinolates have been identified as oviposition and feeding stimulants (Roessingh et al., 1992; van Loon et al., 1992; Simmonds et al., 1994; 27
Gouinguené & Städler, 2006), a decrease in the concentration of these compounds as a result of plant competition could lead to less attractive host plants in intercropping systems, at least for crucifer specialists such as D. floralis.
μmol/ g FDM
The responses of root glucosinolate concentrations in this study correspond to responses identified in previous studies of damage-induced changes in glucosinolate concentrations. In previous studies, the concentration of indolebased glucosinolates in roots tended to increase in response to root herbivory (Birch et al., 1992, 1996; Griffiths, Birch & MacFarlane Smith, 1994; Hopkins et al., 1998; van Dam & Raajimakers, 2006), whilst a damage-induced change in the total amount of root glucosinolates seemed to depend on a balance between a relative increase in indole glucosinolates and a decrease in aliphatic glucosinolates (Birch et al., 1992; Hopkins et al., 1998). The additional stress provided by competition from the clover intercrop caused interactive effects on e.g. the total root glucosinolate level, which was reduced in intercropped treatments at higher egg densities, while the levels in monoculture treatments were fairly constant (Fig. 9). Thus, competition with clover appears to have impaired the ability of the cabbage plants to maintain root glucosinolate levels in the presence of high D. floralis infestations (Paper IV). Total foliage glucosinolates
Total root glucosinolates
Fig. 9. Changes in root aliphatic glucosinolates concentrations (μmol g-1 freeze-dried matter, FDM) in monoculture and in the two clover intercropping densities at an increasing D. floralis egg density (M = monoculture, IC1 = low clover density, IC2 = high clover density).
It is clear from the results of this study that individual glucosinolates may not respond uniformly to herbivory or plant competition, within the usual division of glucosinolates into aliphatic, aromatic and indole based glucosinolates. This was shown, for example, for the indole methoxyglucobrassicin, which was the only indole glucosinolate that increased in intercropped roots. In addition, the responses of a specific group of compounds based on chemical structure may be dominated by a few compounds, or sometimes a single compound. In this study, the sinigrin and glucobrassicin dominating in foliage and the sinigrin and neoglucobrassicin in roots had a major influence on the responses of their specific structural groups. As the responsiveness to specific glucosinolates can vary by several orders of magnitude for both D. floralis and D. radicum (Roessingh et al., 1992, Simmonds 28
et al., 1994), the dominant compound may not be the most stimulating one from the herbivore point of view. It is therefore relevant to consider these compounds on an individual level (Paper IV).
Development of D. floralis In the greenhouse experiment, the development of D. floralis was affected both by feeding on intercropped cabbage plants and by sharing their food source with conspecific larvae, which resulted in lower pupal weights (Fig. 10). Pupal weight
20 15 10 5 0 0
Fig. 10. Effects of intercropping density and D. floralis egg density on the final pupal weights (mg) of D. floralis (M = monoculture, IC1 = low clover density, IC2 = high clover density).
Evaluation of the factors resulting in reduced pupal weight is complicated, as all of the aspects of quality that were measured were changing at the same time, and due to two different causes; interspecific competition between the cabbage host plants and the clover intercrop, and feeding by D. floralis larvae. Reduced food availability for small intercropped roots or through competition with other larvae is one possible cause for reduced larval growth (Paper III). A previous study (Hopkins et al., 1993) showed that intraspecific competition between feeding D. floralis larvae led to reduced pupal weights. The positive correlation found here between pupal weight and root weight (Paper III) indicates that a limited food source is a possible cause for impaired larval development in the intercropped treatments. Other aspects of quality that may have affected larval growth include a high nitrogen concentration, which may have benefited D. floralis larvae feeding on the more nutrient-rich monoculture roots (Bethke et al., 1987; Hunt, Drury & Maw, 1992) (Paper III). In contrast, a higher NDF and lignin content in intercropped and insect-damaged roots may have reduced larval growth (Hopkins et al., 1995), as illustrated by the negative correlation between pupal weight and root NDF and lignin (Paper III). The aggregated oviposition pattern observed for species such as D. radicum and D. antiqua (Mukerji & Harcourt, 1970; Judd & Borden, 1992), suggests that their larvae may benefit from mutual feeding. Since D. radicum prefers to oviposit on 29
plants with moderate damage rather than undamaged or heavily infested plants (Baur, Kostal & Städler, 1996), there is a possibility that intra-specific interactions may lead to a survival advantage. However, an enhanced survival at high egg densities, expressed as the percentage of individuals forming pupae successfully, was not found in this experiment (Paper III).
Glucosinolates (μmol /g FDM)
There was a positive correlation between the concentration of aliphatic glucosinolates in the cabbage roots and pupal weight. This was because pupal weight was positively correlated with concentrations of the individual glucosinolates iberin, sinigrin and napin. This also resulted in a positive correlation between pupal weight and the total concentration of glucosinolates. Plants with high levels of glucosinolates at harvest produced heavier pupae. There was no correlation between pupal weight and the concentration of indole glucosinolates. Within the indole group, there were variable patterns of correlation between pupal weight and individual glucosinolate concentrations. Pupal weight was positively correlated with hydroglucobrassicin, but negatively correlated with methoxy-glucobrassicin (Fig. 11). Pupal weight vs methoxyglucobra ssicin
Pupal weight vs aliphatic glucosinolates
0,1 0 2.2
2 2.4 2.6 2.8 3.0 Pupal weight (loge mg)
2.4 2.6 2.8 3.0 Pupal weight (loge mg)
Fig. 11. Correlation results for pupal weights and methoxyglucobrassicin and the group of aliphatic glucosinolates.
The negative correlation between pupal weight and the concentration of methoxyglucobrassicin is the only indication that glucosinolates would provide a defence against feeding by D. floralis larvae. However, this needs to be investigated further, as the results of this experiment do not say anything about the glucosinolate profile or the concentration of individual glucosinolates during the larval feeding period, especially as glucosinolates seem to have both a fast induction response and turnover rate (Martin & Müller, 2007). In the Brassicaceae, the glucosinolate-myrosinase complex has been called the "mustard oil bomb" for its defence properties (Ratzka et al., 2002), but several specialist insects have evolved strategies for disarming this defence mechanism. The diamond back moth (P. xylostella) prevents the formation of toxic hydrolysis products arising from this plant defence system by producing an enzyme that desulphates glucosinolates in the gut of the feeding larva (Ratzka et al., 2002). The larva of the small white butterfly (Pieris rapae L.) redirects the glucosinolate hydrolysis reaction from the formation of toxic isothiocyanates to the formation of 30
harmless nitriles, through a specific gut protein (Wittstock et al., 2004). However, these disarming strategies do not always seem effective, since the glucosinolatemyrosinase system has also reduced feeding in cruciferous specialists such as P. xylostella and Phyllotreta cruciferae Goeze (Siemens & Mitchell-Olds, 1996) and decreased growth in P. rapae (Agrawal & Kurashige, 2003). However, it should be noted that other studies have found no such effect (Hopkins, Ekbom & Henkow, 1998; Traw & Dawson, 2002; Travers-Martin & Müller, 2007). It is not known whether, and how, D. floralis or D. radicum are affected specifically by the glucosinolates in their diet or their specific strategy used for coping with the glucosinolate-myrosinase system. The mechanisms for plant antibiotic resistance causing developmental differences on different crucifers (Finch & Ackley, 1977; Hopkins et al., 1995) most likely depend on both structural and chemical traits, in which the glucosinolate profile may play a significant role.
Conclusions and applications The development of intercropping as a pest management strategy must be based on knowledge of the behaviour and biology of the target pest. Based on this knowledge, there is increased potential for the successful development of locally adjusted intercropping systems for optimal pest reduction. This thesis shows that intercropping of cabbage and red clover has the potential to reduce oviposition by the turnip root fly, Delia floralis, compared with cabbage monoculture. In addition, the border effect found shows that the effect of intercropping can be enhanced if D. floralis is provided with an alternative oviposition site, in this case a monoculture that functions as a trap crop. This implies that a cropping design in which intercropping and monoculture are combined would be comparable to a push-pull strategy, where location of a resource is made difficult (push), whilst at the same time providing the pest with an attractive alternative (pull). This thesis further shows that natural enemies, in this case mainly predators, have the potential to reduce the population of D. floralis in the field. Even though the difference in effects of natural enemies was similar in both cultivation systems, this study nonetheless shows that there is potential to retain predation pressure in the intercropping system, despite lower predator activity-densities. As a combination of intercropping and monoculture may be a strategy to enhance the effect on D. floralis oviposition, it is promising that the effect of predation was comparable between cultivation systems. For the development of systems where diversity is used for pest reduction and spatial manipulation of attacks, it is probable that measures directed towards enhancing the natural enemies at farm level are more important than intercropping per se for enhancing the effect of natural enemies in the field.
A high level of clover competition not only reduced cabbage biomass, but also led to altered plant quality with respect to root fibre and root nitrogen content. In addition, competition altered the glucosinolate profile of both cabbage foliage and roots. Adding D. floralis herbivory to this system had further and sometimes interactive effects on cabbage growth, structure and chemical content, and these competition and herbivory induced changes had negative consequences for D. floralis development. Although the competitive conditions in this experiment far exceeded an acceptable field situation, the results provide further insight into plant responses in complex systems. Knowledge of plant responses to herbivory in these systems may be useful in identifying mechanisms that affect herbivores negatively. To conclude, intercropping and trap cropping are often seen as opposing strategies for pest control, but the results in this thesis show that a combination may lead to an enhanced effect on pest insect behaviour. This could provide the potential to protect a more susceptible crop through intercropping, while using a more tolerant plant species as a trap crop. Knowledge of insect responses in these systems is still needed, and a future challenge will be to integrate such knowledge in diversification strategies for pest reduction. Consideration must be given to choice of intercrop species for optimal disruption and the integration of a trap crop into the system for manipulation of attack distribution. Furthermore, long-term studies on effects on natural enemy populations in diverse agroecosystems are scarce, so further studies are essential for the development of diverse systems for optimal pest reduction of predators and parasitoids. Although effects of competition may be minimised in intercropping systems through choice of intercrop species or mechanical management, plant-plant interactions will occur and consequently affect herbivores in these systems, both in their host plant search, host plant acceptance and subsequent development. This may be important for the long-term effects on pest insect dynamics in these systems, but there are still questions to be answered regarding plant resistance mechanisms and the responses by herbivores to these.
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Acknowledgements/Tack Först och främst vill jag tacka min huvudhandledare Birgitta Rämert. Tack för ditt otroliga stöd och engagemang och för att du alltid hjälpt mig att se möjligheter istället för problem i svåra situationer! Ett stort tack också till mina biträdande handledare, Peter Hambäck och Richard Hopkins, för all hjälp och alla bra diskussioner. Tack också till Sven Hellqvist, min biträdande handledare under mina somrar i Umeå, för allt stöd angående fältförsök och vitkålsodling. Tack till alla trevliga medarbetare på EVP/VPE som hjälpt till att göra min tid som doktorand så trevlig som den har varit! Ett särskilt tack till ”trädgårdsgruppen”, för att ni tog hand om mig när jag kom till institutionen. Tack till Calle Åkerberg och Anita Pettersson för att ni ALLTID tagit er tid att hjälpa mig, i stort och smått, och Per Nyman för all hjälp med krånglande datorer. Jag vill också tacka mina doktorandkollegor; Sara, för att du är en så god vän, Anuschka, för att du alltid peppat mig, och Hanna, för allt stöd och trevliga samtal, men ett stort tack till ALLA doktorankollegor/vänner som gjort tiden både på och utanför jobbet så mycket roligare! Mina somrar hade inte varit lika trevliga om det inte varit för all personal på Institutionen för Norrländsk jordbruksvetenskap på Röbäcksdalen i Umeå. Ett särskilt tack till Ulla Bång, Malin Barrlund och hela växtskyddsgruppen. Jag vill också tacka alla de tappra som hjälpte mig räkna totalt 95 949 kålflugeägg! Tack till alla deltagare i ’gröngödslingsprojektet’ för all inspiration jag fått vid våra projektresor och gårdsbesök! Tack till Lennart Salomonsson för ditt engagemang i forskarskolan SWOFF och för alla kurser och seminarier du ordnat som fördjupat mina kunskaper om ekologisk odling. Tack också till min forskarskolegrupp som varit ett stöd genom min tid som doktorand med trevliga möten och mycket inspiration! Jag vill också tacka min familj och mina vänner; Min pappa och syster, tack för att ni alltid finns där! Anna, du är inte bara syster utan också min allra bästa vän. Jag vet inte vad jag skulle göra utan dig! Sofia, Cecilia och Maria, tack för ert tålamod med en inte alltid kontaktbar vän. Ni kommer att se mer av mig nu… Malin, du är inte bara den bästa fältassistent man kan önska sig, men också en väldigt god vän! Tack Markus för all kärlek och uppmuntran! Tack också till mina håriga vänner, Ville & Selma, för att ni påmint mig att ta en paus ibland, oftast genom att bokstavligen blockera skrivbord, artiklar, dator m.m.. I am also grateful to Rosemary Collier for comments on this thesis, and for the opportunity to spend my last months as a PhD student at Warwick HRI. It was inspiring to finish this thesis in a place where so much root fly research has been undertaken during the last century, and to get the opportunity to reveal some more of the ‘mysteries’ regarding root fly behaviour. Thank you! 41
Financial support by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas) and the Swedish University of Agricultural Sciences (SLU) is gratefully acknowledged!