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Challenges for integrated pest management of Dasineurabrassicae in oilseed rape

Challenges for integrated pest management of Dasineurabrassicae in oilseed rape The use of insecticides in flowering oilseed rape (Brassica napus L.) against pest insects such as the brassica pod midge (Dasineura brassicae W.) often conflicts with the protection of pollinating and beneficial insects. Dasineura brassicae is a major pest insect in European oilseed rape production. However, a comprehensive and sustainable pest control strategy within the framework of integrated pest management (IPM) does not exist, and little research on the insect has been published dur- ing the past two decades. This paper reviews the existing knowledge about D. brassicae along its life cycle and is intended to form the basis for further research activities on pod-damaging pest insects in oilseed rape. Important knowledge gaps are identified, regarding the significance of natural enemies, diapause induction, and predictions on damage potential, based on initial pest insect population. The short lifespan of the adults is particularly challenging in praxis. The implementation of IPM for D. brassicae is discussed on the basis of the four IPM steps (set an economic threshold, establish pest monitoring, preventive measures, and direct control measures) and remaining hurdles, as well as potential solutions for a better IPM, are identified. For D. brassicae, there is no science-based economic threshold and no applicable monitoring methods for farmers, which hinders a field-specific damage forecast and the precise timing of insecticide applications. Research into improved monitoring (e.g. selective attractants, real-time monitoring using remote-sensing technologies) appears to be a promising step towards an integrated pest management of D. brassicae. Keywords Insect pests · Monitoring · Pest control · Economic threshold Introduction monitoring is established, preventive measures are taken, and only as the last option, chemical control is used. Integrated pest management (IPM) is considered to be the Oilseed rape, Brassica napus L., (Brassicaceae) (OSR) is standard in modern agriculture (Dara 2019; European Com- one of the most important break crops in cereal-dominated mission 2020). It aims to establish sustainable crop manage- crop rotations in Europe (Lundin 2021; Zheng et al. 2020). ment systems, with effective regulation of pest organisms by Its seeds are processed into versatile oil for human nutri- natural antagonisms and environmentally friendly measures. tion, industry, and biodiesel, and its by-products are used There are various approaches how to implement IPM strat- as animal feed (Friedt and Snowdon 2009). A major chal- egies in practice, all covering the following four steps as lenge in the cultivation of OSR is the control of various core elements (Barzman et al. 2015; Ehler 2006; Hokkanen pest insects that cause average annual yield losses of 15% 2015). At first, an economic threshold is set, then a pest across Europe (Zheng et al. 2020). Substantial efforts have been made to develop IPM strategies in oilseed rape pro- duction, and extensive knowledge on pest insects has been published (Alford et al. 2003; Nilsson et al. 2015; Williams Handling Editor: Severin Hatt. 2010a). Nevertheless, there is still no IPM strategy for the * Johannes Hausmann brassica pod midge, Dasineura brassicae Winnertz (Diptera: johannes.hausmann@julius-kuehn.de Cecidomyiidae) and there has been little research on this insect during the last two decades. Dasineura brassicae is Julius Kühn Institute (JKI)–Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Field a major pest insect of OSR and widely spread throughout Crops and Grassland , Messeweg 11-12, 38104 Brunswick, all important growing areas in Europe and in parts of China Germany Vol.:(0123456789) 1 3 646 J. Hausmann (Alford et al. 2003; Zheng et al. 2020). During the ripening and decision support systems. The obstacles that currently period of seeds, the larval instars of D. brassicae feed on prevent the implementation of an effective IPM programme the inner pod walls and secrete enzymes, causing the pods against D. brassicae and how to overcome those shortcom- to turn yellowish, swell and deform (Meakin and Roberts ings, are described in third part of the review. 1991). Significant yield losses occur due to a decrease in This review elucidates that the management of D. bras- seed weight by up to 80% (Williams 2010b) and a premature sicae in agricultural praxis is difficult, because monitoring splitting of the pods, resulting in the loss of seeds (Meakin systems are not yet available and knowledge gaps in the and Roberts 1991). In traditional OSR growing areas, D. biology allow only vague predictions of pest insect popula- brassicae spawns two generations in winter OSR and a third tions and damage, which also prevents the establishment of generation develops in spring OSR (Williams et al. 1987a, sustainable thresholds. It is intended to provide a compre- b). To prevent damage from D. brassicae, farmers regularly hensive overview of the state of knowledge on D. brassicae spray insecticides during the bloom of OSR, which is critical and a basis for further research activities. for several reasons. Insecticides are often added to fungi- cide treatments for Sclerotinia sclerotiorum (Lib.) de Bary and, thus, usually miss the optimal timing aligned with the Current knowledge on the biology flight of the first generation of D. brassicae. Additionally, of Dasineura brassicae insecticide applications during the bloom of OSR have a particularly high risk to harm non-target organisms, such Emergence of the first generation as pollinators (Karise et al. 2017; Mänd et al. 2010) and many important parasitoids of OSR pest insects (Ulber et al. Dasineura brassicae hibernates as larva in a cocoon in fields 2010a). In line with the IPM objectives, pesticides should be where OSR was grown in previous years (Williams 2010b). applied only after economic thresholds have been exceeded After diapause, the larvae pupates inside the cocoons (Buhl and in a targeted manner. In case of D. brassicae, the size and Schütte 1964) and the pupa moves up to the soil sur- of single generations is highly fluctuating and cumulated face (Buhl 1960). The emergence of the first generation is larval densities of individual years can range from a few mainly driven by soil temperatures (Axelsen 1992b; Hansen −2 hundred to over 30.000 larvae m (Felsmann 2007; Haus- 1994; Kirchner 1966). For the development of the cocoons mann et al. 2019). Most studies found the second genera- in the soil, 141 day degrees above 8.1 °C after the first of tion to be the largest (Buhl 1960; Erichsen 1982; Fröhlich January are needed (Axelsen 1992b). The first generation 1956a). However, applications against the second generation of midges emerges when the soil temperature in 5 cm depth are not sensible, because OSR branches out during pod set exceeds 15 °C and air temperature is around 19 °C (Kirchner and late applications result in major plant damage along the 1966), which coincidences with the early flowering stage of driving alleys, among other problems. Consequently, the OSR in most years (Fröhlich 1956a; Williams et al. 1987a). second generation develops undisturbed and can only be Pupation itself is not influenced by soil moisture (Erichsen controlled indirectly by a reduction of the previous genera- 1982; Hughes 1998; Kirchner 1966). However, soil moisture tion. Thus, a thorough understanding of the factors driving affects the warming of the soil and the mechanical resistance D. brassiae population dynamics is absolutely necessary for for the movement of pupae to the soil surface (Blume et al. the successful management of this multivoltine pest insect, 2016). Consequently, the emergence of midges within one with only one application against the first generation early in field can vary due to small-scale differences in soil moisture the season. For targeted control, it is important to precisely and soil type and depends also on the depths at which the determine the time point at which a pest insect emerges and cocoons were located in the soil. The flight period of the first immigrates into the crop. Species-specific migration behav - generation lasts about 3–6 weeks (Williams et al. 1987a). iour has a major impact, on which fields, or areas within, Shifting temperatures can delay emergence, and often there will be infested. Knowledge about the maximum reproduc- is no constant flight, but several waves of migration. tion capacity of a single female is important for estimat- The emergence of D. brassicae occurs mainly in the ing the maximum possible population increase over several morning (Buhl 1960). At the emergence site, virgin females generations at a given pest insect density. These and other show a “calling behavior” and release a sex pheromone aspects are linked to biological traits in the life cycle of D. (Williams and Martin 1986) that is produced by glandular brassicae, which are addressed in the first part of this review. tissue in the epidermis of an intersegmental membrane in the To predict the occurrence of a pest insect and the related ovipositor (Isidoro et al. 1992). After mating, the females damage, the most important factors influencing its popula- immediately search for host plants, which is illustrated by tion dynamics have to be known. This is analysed in the sec- the curve of the flight activity at the emergence sites (Mur - ond part of this review. Together, this information can pro- chie et al. 2001). It was observed that the curve is unimodal vide the basis for the development of economic thresholds with a peak for males at 9:00 (searching for virgin females) 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 647 and time shifted at 11:00 for females (mated females search cuticula (Åhman 1986). On a potential host plant, females for suitable host plants). There is no flight activity at night can be observed walking along pods. Tactile and sensory time (Murchie et al. 2001) (Fig. 1). stimuli are perceived by the tarsi and antennae (Coutin 1964). In most cases, females lay their eggs in pods that were Finding and accepting host plants previously damaged (Åhman 1987). Potential oviposition sites are externally palpated with the maxillary palps and In general, the range of dissemination of D. brassicae is finally investigated by the insertion of the ovipositor which rather low. In search of new host plants, the females mainly is equipped with different types of sensory hairs at its tip fly downwind (Sylvén 1970). Just as they deflect the wind, (Hallberg and Åhman 1987). hedges, and other landscape elements can act as barriers or sluices for the dispersal of D. brassicae. Distances of up to Reproduction of Dasineura brassicae 500 m upwind were observed only at low wind speeds of −1 max. 4.5 m  s (Schütte 1964), which indicates an olfactory- Virgin females produce up to 140 eggs in their ovaries (Syl- mediated upwind anemotaxis. This was confirmed by olfac- vén (1949) cited by Axelsen 1992a); however, the average tometer bioassays in which mated females (but no males) number of eggs laid per female is estimated to be around 60 were attracted to leaves and pods of OSR (Pettersson 1976) (Buhl and Schütte 1971). Adult midges were observed lick- and crushed OSR leaves (Williams and Martin 1986). At a ing on plant sap (Fröhlich 1960), but no feeding behaviour shorter distance, males and females of D. brassicae respond of the adults was observed so far. Whether egg maturation in positively to the yellow colour of the flowers (Williams and D. brassicae is proovigenic, or whether additional eggs also Cook 2010). mature after eclosion, is not yet known. However, fecun- Host plants of D. brassicae are OSR, close relatives such dity is correlated with the body length of a female (Sylvén as turnip rape (Brassica rapa subsp. oleifera), cabbage (1949), cited by Åhman 1985), which indicates that all eggs (Brassica oleracera), and some cruciferous weeds. In gen- mature before eclosion. Environmental stimuli affect ovipo- eral, the survival on Brassica spp. is higher than on other sition as well. According to Fröhlich (1956a) temperatures cruciferous plants, which only serve as hosts to a limited above 19 °C are preferred for oviposition. Additionally, the extend (Åhman 1988; Speyer 1925). In choice tests between quality of a host plant influences the egg loads and at a later OSR and other crucifers, females did land more frequently stage, larval weights which are higher on suitable hosts, on OSR and the number of batches per ovipositing female compared to low-quality hosts (Åhman 1988). Females was higher (Åhman 1988). The initial host plant adaption lay their eggs in several batches, and there is evidence for behaviour is probably elicited by the wax composition of the monogeny of broods of a single midge (Murchie and Hume 2003). Regarding the overall sex ratio in D. brassicae, sev- eral authors described a slight bias towards females (Buhl 1960; Fröhlich 1956a; Murchie and Hume 2003). The development of the eggs and larvae depends on tem- perature (Axelsen 1992b; Hughes 1998). Eggs hatch after 3–4  days and the egg-larval stage of the first generation needs 134°DD above a developmental threshold of 6.7 °C, which lasts about 3–4 weeks in the field (Axelsen 1992b). At maturity, larvae leave the pods and drop down to the soil where they burrow in 0–5 cm depth (Buhl 1960; Fröhlich 1956a). According to Buhl (1960) about 5% of the first-generation larvae, but almost 80% of the second-generation larvae enter winter diapause. In contrast, Axelsen et al. (1997) found that the proportion of larvae that enter diapause varies within a season and between years and is not constantly increasing in every generation. The authors suggested that the cumula- Fig. 1 Female of Dasineura brassicae. The adults of D. brassicae are tive solar radiation perceived by the growing larvae trig- delicate with body length of 0.7–1.5  mm (♂) and 0.9–2.2  mm (♀), respectively (Kirk 1992). Males have stalked antennae with annular gers diapause. Still the specific factors that control diapause sensory hairs. Distinctive features of the female are the non-stalked induction remain unknown. Additional, not all diapausing antennae and the ovipositor. The three larval instars live gregariously larvae pupate in the following year, e.g. Schütte (1979) within the pods and grow up to 2 mm. The first larval instar is almost investigated that 13% of the overwintering larvae did not translucent, and older larvae are white coloured with yellow fat bod- ies emerge in spring following diapause. Diapausing larvae of 1 3 648 J. Hausmann D. brassicae can survive in the soil for up to 5 years (Buhl top gauze net. Each six cups (replicates) were placed in 1960; Nilsson et al. 2004), but there is a negative correlation climate chambers (RUMED®, P 210) at constant tempera- between the duration of the cocoon stage in the soil and the ture levels of 10 °C, 15 °C, 20 °C, and 25 °C. The experi- average lifespan of adults (Schütte 1979). ments started at 12 a.m., and the mortality of the midges was recorded every six hours for three days. Thereafter, Life expectancy of Dasineura brassicae assessments were made every 12 h. Data analysis was performed using R (version 3.6.1) In the field, a life expectancy of 1–3 days is assumed for (R Core Team 2019). A generalized linear model (glm) adult D. brassicae (Williams 2010b), though conclusive explaining the number of dead midges per cup by tem- reports on the lifespan of D. brassicae are missing. Hughes perature treatments and time was fitted. A binomial error (1998) demonstrated that the lifespan of D. brassicae is distribution was assumed. The effects of different variables temperature dependent; however, experiments were biased were tested via an analysis of deviance using the “Chi- because midges had no access to water and did not survive test”. For model diagnostics, the residuals were plotted longer than 48 h in any of the temperature regimes. against the predicted values and the explanatory variables To shed more light on this question, I have conducted and were checked visually. The LT values were calcu- an experiment in which larvae of the second genera- lated using the function dose.p from the MASS package tion were collected in the field in 2019 and were held (Venables and Ripley 2007). The effect of different tem - for almost one year in moist sand at 5 °C in the climate peratures on the mortality of midges over time was also chamber, before they were reared to adult midges. The analysed using Kaplan–Meier survival analysis. midges used for this experiment, emerged from the same As a result, 50% of female D. brassicae were alive for sample in the morning of the 16th June 2020. Groups of 35 h (SE ± 1.2) at 25 °C (max. 66 h) (Fig. 2). At a con- five females were transferred into transparent plastic cups stant temperature of 10 °C, the LT was 224 h (SE ± 6.8) (500 ml, height 16.5 cm), which had three openings (each and single females lived up to 17  days. Adult lifespan 4  cm ), covered with gauze to allow the circulation of air. was significantly dependent on temperature treatments A water saturated cube (3.5  cm ) of floral foam in each (Kaplan–Meier survival analysis, p < 0.001). This outcome cup supplied moisture to the midges. The foam cubes were confirmed that under humid conditions, adult lifespan is resupplied with drops of tap water every 12 h through the inversely related to temperature. Fig. 2 Calculated mortality with 95% confidence limits of Dasineura brassicae females over the time (hours). Midges were kept in plastic cups with a moist cube of floral foam at constant temperatures. Dashed lines indicate the time after which 50% of the midges have died (LT ). n = 30 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 649 quickly changing weather conditions during the flight Drivers of population dynamics period of the first and second generation, especially pre- cipitation, may kill adults and prevent successful oviposi- A distinction can be made between factors that have the tion. Strong winds may disperse the first-generation adults potential to promote population dynamics of D. brassicae and partly prevent colonization of suitable crops. and others that have negative effects (Fig.  3). As mentioned earlier, D. brassicae is reliant on damaged Regarding the life cycle, Axelsen (1992c) identified two pods for oviposition because the ovipositor is not suitable for critical life stages, in which the population of D. brassicae piercing or drilling of mature pod walls, as demonstrated by suffers larger losses, namely the pre-cocoon stage and the morphological studies (Hallberg and Åhman 1987; Stech- diapause during winter. The author calculated a generation mann and Schütte 1978). For this reason, the cabbage seed- survival of about 2–4% (Axelsen 1992c). During the pre- pod weevil, Ceutorhynchus obstrictus Marsham (Coleoptera: cocoon stage, which is the time period between the drop- Curculionidae), by injuring on the pods through its feeding ping of larvae from the pods until they spin a cocoon in and oviposition activity, is considered the most important the soil, losses may occur because of predation by carabids factor for a severe infestation of an OSR crop with D. bras- (Warner et al. 2000) and spiders (Felsmann 2007). In addi- sicae (Ferguson et al. 1995; Free et al. 1983; Speyer 1921). tion, dry weather conditions that lead to desiccation are Strong increases in the seed weevil population lead to a being discussed (Axelsen 1992c). The losses during dia- time shifted growth of the D. brassicae population (Schütte pause can be attributed to parasitism (Ferguson et al. 2004; 1979). In many cage trials on OSR, no oviposition of D. Murchie 1996), pathogens (Hokkanen et al. 2003), and brassicae could be observed without artificial injury of the adverse effects of tillage, e.g. ploughing (Axelsen 1992c). pods or the addition of C. obstrictus (Ankersmit 1955; Buhl There is still a need for research on all of these points. 1957; Doberitz 1973; Fröhlich 1956b; Hughes and Evans Weather conditions can affect the population dynam- 2003). In contrast, several authors described that D. bras- ics of D. brassicae in different ways. As described, many sicae can also independently oviposit in small and young physiological processes, like the emergence of the first pods up to a length of 40 mm (Axelsen 1992c; Fröhlich generation, egg laying, larval and pupal development, and 1956b; Hoßfeld 1963; Mühle 1951; Nietzke 1976). Thus, C. lifespan, are temperature dependent. Warmer tempera- obstrictus is probably more important for the development of tures reduce the developmental time of eggs, larvae, and the second than the first generation. Also, at low pest insect pupae, resulting in a faster generation turnover. Whether densities, the abundance of C. obstrictus is not limiting the diapause is induced by environmental conditions remains population size of D. brassicae (Axelsen 1992a; Fröhlich to be investigated. On the other hand, it seems likely that 1956b). This can be explained by the larvae of D. brassicae Fig. 3 The life cycle of Dasineura brassicae, modified after Buhl 1960 1 3 650 J. Hausmann living gregariously and more than one female using a suit- et al. 2004; Thiem 1970; Warner et al. 2000). In addition, the able pod for oviposition. For this reason, the average number proportion of damaged pods cannot be equated with yield of larvae within one pod can fluctuate considerably and is losses, since OSR compensates early pod losses up to 10% dependent on the availability of damaged pods for female by increasing grain weight (Diepenbrock 2000; Erichsen midges. In addition, other phytophagous insects, such as 1982; Williams and Free 1979), and also compensates early lygid bugs [Lygus spp. (Heteroptera: Miridae)] (Hughes pod losses at the main inflorescence on lateral shoots (Pinet and Evans 2003) or abiotic damages such as hail and wind et al. 2015). The plant’s ability to compensate, however, is (Winfield 1992), can provide suitable oviposition sites. Con- less pronounced for damage caused by the second genera- cluding, C. obstrictus is important for the economic damage tion of the midge. potential of D. brassicae within one year, but not a manda- Knowing the important driving factors of an insect’s tory prerequisite. population dynamics and their relation to potential damage, an economic action threshold can be derived. Presently, threshold values for direct control of D. brassicae do not Challenges for the implementation exist in most European countries. Most commonly, the eco- of integrated pest management nomic threshold for C. obstrictus, the alleged pioneer of the midge, is lowered from one weevil per plant to one weevil Defining economic thresholds per two plants, if both pest insect species occur together (Heimbach 2017; Ramsden et al. 2017). Older thresholds Dasineura brassicae is a typical r-strategist, with short for D. brassicae ranged between 0.25–1 midges per plant generation time and high reproductive capacity. The short (Heimbach 2017; Lauenstein 1993). Other approaches try lifespan of the adults is particularly challenging for farmers, to predict the damage potential from the overall population because the midges start egg laying immediately after their size of D. brassicae estimated from the number of D. bras- emergence in OSR, leaving little time for control measures. sicae cocoons that are washed out of soil samples. Buhl As stated above, it was shown that the abundance of the wee- and Schütte (1964) recommended to treat OSR fields in a vil C. obstrictus at full flowering promotes pod damage by region if the number of cocoons with living larvae in the soil D. brassicae later in the season. However, predation, parasit- exceeds the threshold of 40 per 100  cm . A similar method is ism, and weather conditions (especially temperature) seem used in several federal states in northeast Germany. Here, the to be additional important drivers of the midge’s population threshold for insecticide applications in the following year dynamics. Main losses during the life cycle occur during the against C. obstrictus is lowered if the average number of 25 winter diapause and the overall generation survival is low. cocoons per 100  cm (assessed after the harvest of OSR) Nevertheless, small numbers of individuals seem to be able is exceeded (Hahn, M pers. communication). However, it to build up a strong population over the season, if condi- should be stated that a scientic fi ally based and peer-reviewed tions are favourable. Hence, the shift from the first to the economic threshold does not exist. second generation should be the focal point for the overall reproduction capabilities and population size within one sea- Pest monitoring son. Altogether, it is difficult to make a prediction about the population dynamics of two generations, at the time when The establishment of an economic threshold requires moni- the decision for or against an active control has to be made. toring of the pest insect and represents the second stage in This challenge should be met by an economic threshold, the implementation of an IPM strategy. In case of D. bras- the creation of which is the first step of the IPM approach. sicae, the monitoring is challenging for several reasons, not Therefore, knowledge about the potential damage of a pest least because of the insect’s small size (Fig. 1). Adults of insect and the tolerance of a host plant towards a pest insect D. brassicae can be reliably differentiated from other gall is needed, as well as a reliable monitoring system (Ramsden midge species by their specific wing veining (Fig.  4), but et al. 2017). this feature is difficult to identify with the naked eye. Con- The overall damage by D. brassicae is usually determined sequently, monitoring of D. brassicae midges by farmers did by counting infested pods per plant during the ripening stage never catch on in praxis. of OSR (see EPPO Standard PP 1/220). The proportion of The emergence and flight of the first generation can damaged pods can exceed 50%, and high infestation rates be monitored by using photoeclectors that are placed at with yield losses were reported regularly in the past hun- the OSR fields of the previous year (Waede 1960). In dred years (Buhl 1960; Döring and Ulber 2012; Fröhlich addition, there are commercial prediction models that 1956b; Kirchner 1966; Nilsson et al. 2015; Schütte 1979; indicate which days are suitable for the first generation Speyer 1925; Thiem 1970). However, the damage is often of D. brassicae to emerge and that also calculate what concentrated at field margins and the head lands (Ferguson percentage of the flight period has passed (Johnen et al. 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 651 Preventive measures In IPM, preventive measures that reduce pest insect densi- ties are preferable to direct control measures. Such indirect and preventive measures can include cultural measures, crop rotation, resistant cultivars, landscape management, and the enhancement of natural enemies (Hokkanen 2015). Dasineura brassicae can use spring sown OSR to develop Fig. 4 The veining of Dasineura brassicae, modified after Kirk 1992. a strong third generation (Axelsen 1992c). For this reason, Wings have three veins reaching the wing margin. Typically, the long the growing of winter and spring sown OSR in the same vein from the base ends just before the tip of the wing region has been considered a key factor for the development of large D. brassicae populations and heavy infestations for a long time (Doberitz 1973; Speyer 1921). To what extent a third generation is limited by the lack of suitable host plants 2010). Based on regional meteorological data, these pre- or by the induction of diapause of second-generation larvae, diction models can help farmers to determine the critical needs to be further investigated. The control of cruciferous time when immigration of D. brassicae in their region is weeds, especially on non-crop habitats, was recommended probable. Field-specific forecasts are not possible though, by Speyer (1921). However, it was shown that D. brassicae since the migration of females to the new crop is affected survives only in small numbers on such weeds, which limits by factors like wind and the distance from the previous the potential of this measure (Åhman 1988). As the dispersal year’s OSR fields. Information on which specific fields capabilities of D. brassicae are limited, the cultivation area or parts of a field are colonized is crucial for the imple- of OSR at landscape scale affects the damage potential of mentation of IPM. Yellow water traps are potentially suit- the midge as well. The risk of infestation is reduced to less able for this purpose, although they create the risk of than half, if a distance of more than 3 km of this year’s OSR misidentification, as several similar gall midge species is maintained from the previous year's cropland (Erichsen can be found in the OSR fields. For this reason, attempts 1982). To interfere with the build-up of high pest popula- were made to selectively catch D. brassicae using baited tions, the interruption of OSR cultivation at a landscape traps. The addition of an extract of OSR seeds with a scale is suggested as a possibility (Zheng et al. 2020). This high content of glucosinolates to water traps increased was successfully demonstrated for C. obstrictus and D. bras- the capture efficiency at the emergence sites (Erichsen sicae in a one-season trial in northern Germany (Schütte and Daebeler 1987). Traps baited with allyl isothiocy- 1979). anate caught more male and female D. brassicae than Soil tillage affects the vertical distribution of cocoons traps baited with 2-phenylethyl isothiocyanate or unbaited in the soil (Buhl 1960; Froese 1992). Ploughing did nei- traps (Murchie et al. 1997). However, mostly males were ther reduce the number of D. brassicae cocoons in the soil caught in both studies. Traps baited with the sex phero- (Nielsen et al. 1994) nor the total emergence of adults in mone of virgin females (Williams and Martin 1986) also spring (Axelsen 1995), though the temporal distribution of selectively caught D. brassicae but also predominately the emergence was expanded. Still, some authors assume males (Williams 1990). Since males usually remain at the that ploughing is an important mortality factor for D. brassi- emergence sites after mating, their catch is not suitable cae (Axelsen 1992c; Ferguson et al. 2004; Williams 2010b). to predict the colonization of the OSR fields by females. Dasineura brassicae can discriminate between low- and The development of a trap attracting specifically female good-quality hosts (Åhman 1988). The differences in alight- midges would be a great step forward in the monitoring ing frequency between different Brassica spp. indicate the of D. brassicae. possibility of antixenosis (Åhman 1988). The lower rates of In recent years, agriculture has experienced a trend survival and larval weights on low-quality hosts are prob- towards the use of new, innovative technologies. Artificial ably related to lower nutritional values or substances that intelligence and camera traps enable the development of are harmful for D. brassicae (Åhman 1985), which could real-time monitoring systems. For example, lidar technol- be seen as a kind of antibiosis. In summary, these are differ - ogy allows insects to be identified in situ by their wing ent starting points for breeding resistant cultivars. However, beat, colour, and the proportions of wing width to body successful resistance breeding against D. brassicae is not size. Technology offers promising possibilities for the foreseeable yet based on the limited knowledge of variability monitoring of flying insects (Brydegaard and Svanberg in resistance of OSR and related species for this pest. 2018), and first tests with pest insects in OSR have been Natural enemies contribute to the control of D. brassi- carried out (Kirkeby et al. 2021). cae populations by predation and parasitisation. At least 31 1 3 652 J. Hausmann parasitoid species parasitize eggs and larval stages of D. activity of the insecticides will often decline rapidly in the brassicae (Ulber et al. 2010b). The key parasitoid species e fi ld. Hence, it is a challenge to protect the crop with a single are Platygaster subuliformis (Hymenoptera: Platygastridae) insecticide application, which requires a precise timing of and Omphale clypealis (Hymenoptera: Eulophidae), both the application. Therefore, reliable and precise monitoring widely distributed in Central and Northern Europe (Ulber data would be a prerequisite. et al. 2010b). However, the multivoltine life history of the Until now, D. brassicae is sensitive to insecticides and host and its parasitoids complicate investigations and exten- there is no evidence of insecticide resistance. However, in sive studies on parasitism in D. brassicae are scarce. Exist- Germany, increasing pyrethroid resistance in populations ing studies indicate substantial variability in parasitism rates of C. obstrictus can be observed (Brandes and Heimbach (Murchie 1996). In general, parasitism rates post-diapause 2019). seem to be higher and can exceed 50% (Ferguson et  al. Insecticide applications below the flowering canopy of 2004; Murchie 1996). Predation of larvae might also affect the crop with dropleg technique can reduce side effects on D. brassicae populations. Larvae are especially vulnerable pollinators but tend to have reduced efficacy against D. bras- to predation by spiders or ground dwelling predators, when sicae (Hausmann et al. 2019). Regarding alternative con- they drop down from the pods to pupate into the soil. Alto- trol measures, only few studies have investigated botanicals gether, 11 carabid species fed on pod midge larvae in labora- such as extracts from neem tree (Azadirachta indica) (Pavela tory studies; however in choice tests, species differed in their et al. 2009) or the application of nitrophenoles (Kazda et al. preference for D. brassicae and in the amount of consumed 2015), which have shown some efficacy in field trials. larvae (Williams et al. 2010). Only Amara similata (Coleop- tera: Carabidae) was proven to feed on larvae in field studies (Schlein and Büchs 2006). Spiders may prey on larvae and Conclusions emerging midges of the first generation. Studies of Felsmann (2007) revealed a temporal coincidence between web densi- This literature review shows that so far IPM of D. brassicae ties of linyphiid spiders and both, the dropping of larvae, and in OSR is rather a collection of promising ideas than state the emergence of new generation midges in OSR. of the art. Most preventive control measures are limited in In conclusion, preventive measures can contribute to a terms of their efficiencies. Resistance breeding or a large- reduction of D. brassicae infestation to a limited extent. scale interruption of OSR cultivation in individual years is In particular, the potential of natural antagonists, such as difficult to establish in the short term and more knowledge predators and parasitoids, should be further explored and about the effectiveness of all these measures is needed. De promoted through adherence to good agricultural practice facto, direct control with insecticides remains the most effec- (i.e. IPM, use of economic thresholds). The distance to OSR tive control measure, and it is, therefore, essential that it is fields of the previous year, and the avoidance of winter and practiced within the framework of IPM. So far, the most spring sown oilseed rape in the crop rotation, are effective practicable option to predict D. brassicae damage appears measures to reduce pest pressure. to be monitoring of C. obstrictus, which provides access to pods and so for a mass propagation. However, a clear Control measures relation between the two species only exists at high pest insect densities. At present, insecticide sprays in flowering The brassica pod midge has been a subject of research since OSR are often retrospectively motivated and tend to have the 1850 (Winnertz 1853) and different control options have character of an insurance spray rather than being targeted been under discussion so far. Early on, the control of D. and economically justified from an integrated pest manage- brassicae was rather indirect, while direct measures aimed ment perspective. To improve this, the development of an for control of the cabbage seedpod weevil C. obstrictus (Spe- economic threshold for D. brassicae is a necessary require- yer 1921). In general, insecticide spray treatments of field ment. So far, it is poorly understood what the number of margins and headlands are considered adequate for moder- individuals constitutes the critical threshold for a potential ate pest insect pressure (Ferguson et al. 2004; Thiem 1970). mass propagation within the season. Therefore, the mortality Today, control of the cabbage seedpod weevil and the bras- rate of the first generation of D. brassicae and other factors sica pod midge pest insect complex relies mainly on the favouring the development of a large second generation need use of synthetic chemical insecticides. All direct measures to be studied in detail. To be reliable, prediction models target C. obstrictus and the first generation of D. brassicae. of potential crop damages should further include tempera- Insecticides with non-systemic properties have to be applied ture as a variable, as this affects many aspects of population before the main flight, to hit the midges before they start lay - development. However, the absence of long-term weather ing eggs. Since OSR is rapidly growing during the flower - forecast has a limiting effect. Furthermore, there is great ing period and temperatures can be quite warm, the residual need for an improved method that allows easy monitoring 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 653 Axelsen JA (1992) The developmental time of the pod gall midge Das- of D. brassicae. Currently, the identification of midges in yneura brassicae Winn. (Dipt., Cecidomyiidae). J Appl Entomol the field is not practicable and it is therefore impossible to 114:263–267. h t t p s : / / d o i . o rg / 1 0 . 1 1 1 1 / j . 1 4 3 9 - 0 4 1 8 . 1 9 9 2 . t b 0 1 1 determine which fields or specific areas within a given field 25.x are infested and are likely to suffer crop damage. Promising Axelsen JA (1992) The population dynamics and mortalities of the pod gall midge (Dasyneura brassicae Winn.) (Dipt., Cecidomyiidae) avenues of research are the development of selective attract- in winter rape and spring rape (Brassica napus L.) in Denmark. J ants and real-time monitoring of insects, using remote-sens- Appl Entomol 114:463–471. https://doi. or g/10. 1111/j. 1439- 0418. ing technology. 1992. tb011 52.x Axelsen JA (1995) The winter mortality and emergence time of Acknowledgements I would like to thank Meike Brandes, Michael Dasineura brassicae in Denmark. IOBC-WPRS Bul 18:81–87 Rostás, Jan Schinkel, and Bernd Ulber, who contributed to the work Axelsen JA, Fink R, Kjaer C (1997) Global solar radiation as the factor through many discussions and helpful suggestions. My thanks also go controlling induction of diapause in the pod midge (Dasyneura to Urs Wyss, who kindly provided a picture of Dasineura brassicae. brassicae Winn.). Oecologia 111:178–182. https:// doi. org/ 10. 1007/ s0044 20050 223 Barzman M, Bàrberi P, Birch ANE, Boonekamp P, Dachbrodt-Saaydeh Funding Open Access funding enabled and organized by Projekt S, Graf B, Hommel B, Jensen JE, Kiss J, Kudsk P, Lamichhane DEAL. 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Mitteilungen Aus its infestation of spring oilseed rape (Brassica napus L.). J Agric Der Biologischen Reichsanstalt Für Land- Und Forstwirtschaft. Sci 109:309–314 21:208–217 Williams IH, Ferguson AW, Kruus M, Veromann E, Warner DJ (2010) Speyer W (1925) Kohlschotenrüßler (Ceutorrhynchus assimilis Payk), Ground beetles as predators of oilseed rape pests: incidence, Kohlschotenmücke (Dasyneura brassicae Winn) und ihre Para- spatio-temporal distributions and feeding. In: Williams IH (ed) siten. In: Arbeiten aus der Biologischen Reichsanstalt für Land- Biocontrol-based integrated management of oilseed rape pests. und Forstwirtschaft, vol 12. Paul Parey, Berlin, pp 79–108 Springer, Dordrecht, pp 115–149 Stechmann D-H, Schütte F (1978) Zur endophytischen Eiablage von Winfield AL (1992) Management of oilseed rape pests in Europe. Agric Dasineura brassicae Winnertz, 1853 (Dipt., Cecidomyiidae). J Zool Rev 5:51–95 Appl Entomol 85:412–424. https:// doi. org/ 10. 1111/j. 1439- 0418. Winnertz J (1853) Beitrag zu einer Monographie der Gallmücken. Lin- 1978. tb040 52.x naea Entomologica 8:154–322 1 3 656 J. Hausmann Zheng X, Koopmann B, Ulber B, von Tiedemann A (2020) A global Publisher's Note Springer Nature remains neutral with regard to survey on diseases and pests in oilseed rape—Current challenges jurisdictional claims in published maps and institutional affiliations. and innovative strategies of control. Front Agron 2:590908. https:// doi. org/ 10. 3389/ fagro. 2020. 590908 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Arthropod-Plant Interactions Springer Journals

Challenges for integrated pest management of Dasineurabrassicae in oilseed rape

Arthropod-Plant Interactions , Volume 15 (5) – Oct 1, 2021

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Copyright © The Author(s) 2021
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1872-8855
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10.1007/s11829-021-09861-1
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Abstract

The use of insecticides in flowering oilseed rape (Brassica napus L.) against pest insects such as the brassica pod midge (Dasineura brassicae W.) often conflicts with the protection of pollinating and beneficial insects. Dasineura brassicae is a major pest insect in European oilseed rape production. However, a comprehensive and sustainable pest control strategy within the framework of integrated pest management (IPM) does not exist, and little research on the insect has been published dur- ing the past two decades. This paper reviews the existing knowledge about D. brassicae along its life cycle and is intended to form the basis for further research activities on pod-damaging pest insects in oilseed rape. Important knowledge gaps are identified, regarding the significance of natural enemies, diapause induction, and predictions on damage potential, based on initial pest insect population. The short lifespan of the adults is particularly challenging in praxis. The implementation of IPM for D. brassicae is discussed on the basis of the four IPM steps (set an economic threshold, establish pest monitoring, preventive measures, and direct control measures) and remaining hurdles, as well as potential solutions for a better IPM, are identified. For D. brassicae, there is no science-based economic threshold and no applicable monitoring methods for farmers, which hinders a field-specific damage forecast and the precise timing of insecticide applications. Research into improved monitoring (e.g. selective attractants, real-time monitoring using remote-sensing technologies) appears to be a promising step towards an integrated pest management of D. brassicae. Keywords Insect pests · Monitoring · Pest control · Economic threshold Introduction monitoring is established, preventive measures are taken, and only as the last option, chemical control is used. Integrated pest management (IPM) is considered to be the Oilseed rape, Brassica napus L., (Brassicaceae) (OSR) is standard in modern agriculture (Dara 2019; European Com- one of the most important break crops in cereal-dominated mission 2020). It aims to establish sustainable crop manage- crop rotations in Europe (Lundin 2021; Zheng et al. 2020). ment systems, with effective regulation of pest organisms by Its seeds are processed into versatile oil for human nutri- natural antagonisms and environmentally friendly measures. tion, industry, and biodiesel, and its by-products are used There are various approaches how to implement IPM strat- as animal feed (Friedt and Snowdon 2009). A major chal- egies in practice, all covering the following four steps as lenge in the cultivation of OSR is the control of various core elements (Barzman et al. 2015; Ehler 2006; Hokkanen pest insects that cause average annual yield losses of 15% 2015). At first, an economic threshold is set, then a pest across Europe (Zheng et al. 2020). Substantial efforts have been made to develop IPM strategies in oilseed rape pro- duction, and extensive knowledge on pest insects has been published (Alford et al. 2003; Nilsson et al. 2015; Williams Handling Editor: Severin Hatt. 2010a). Nevertheless, there is still no IPM strategy for the * Johannes Hausmann brassica pod midge, Dasineura brassicae Winnertz (Diptera: johannes.hausmann@julius-kuehn.de Cecidomyiidae) and there has been little research on this insect during the last two decades. Dasineura brassicae is Julius Kühn Institute (JKI)–Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Field a major pest insect of OSR and widely spread throughout Crops and Grassland , Messeweg 11-12, 38104 Brunswick, all important growing areas in Europe and in parts of China Germany Vol.:(0123456789) 1 3 646 J. Hausmann (Alford et al. 2003; Zheng et al. 2020). During the ripening and decision support systems. The obstacles that currently period of seeds, the larval instars of D. brassicae feed on prevent the implementation of an effective IPM programme the inner pod walls and secrete enzymes, causing the pods against D. brassicae and how to overcome those shortcom- to turn yellowish, swell and deform (Meakin and Roberts ings, are described in third part of the review. 1991). Significant yield losses occur due to a decrease in This review elucidates that the management of D. bras- seed weight by up to 80% (Williams 2010b) and a premature sicae in agricultural praxis is difficult, because monitoring splitting of the pods, resulting in the loss of seeds (Meakin systems are not yet available and knowledge gaps in the and Roberts 1991). In traditional OSR growing areas, D. biology allow only vague predictions of pest insect popula- brassicae spawns two generations in winter OSR and a third tions and damage, which also prevents the establishment of generation develops in spring OSR (Williams et al. 1987a, sustainable thresholds. It is intended to provide a compre- b). To prevent damage from D. brassicae, farmers regularly hensive overview of the state of knowledge on D. brassicae spray insecticides during the bloom of OSR, which is critical and a basis for further research activities. for several reasons. Insecticides are often added to fungi- cide treatments for Sclerotinia sclerotiorum (Lib.) de Bary and, thus, usually miss the optimal timing aligned with the Current knowledge on the biology flight of the first generation of D. brassicae. Additionally, of Dasineura brassicae insecticide applications during the bloom of OSR have a particularly high risk to harm non-target organisms, such Emergence of the first generation as pollinators (Karise et al. 2017; Mänd et al. 2010) and many important parasitoids of OSR pest insects (Ulber et al. Dasineura brassicae hibernates as larva in a cocoon in fields 2010a). In line with the IPM objectives, pesticides should be where OSR was grown in previous years (Williams 2010b). applied only after economic thresholds have been exceeded After diapause, the larvae pupates inside the cocoons (Buhl and in a targeted manner. In case of D. brassicae, the size and Schütte 1964) and the pupa moves up to the soil sur- of single generations is highly fluctuating and cumulated face (Buhl 1960). The emergence of the first generation is larval densities of individual years can range from a few mainly driven by soil temperatures (Axelsen 1992b; Hansen −2 hundred to over 30.000 larvae m (Felsmann 2007; Haus- 1994; Kirchner 1966). For the development of the cocoons mann et al. 2019). Most studies found the second genera- in the soil, 141 day degrees above 8.1 °C after the first of tion to be the largest (Buhl 1960; Erichsen 1982; Fröhlich January are needed (Axelsen 1992b). The first generation 1956a). However, applications against the second generation of midges emerges when the soil temperature in 5 cm depth are not sensible, because OSR branches out during pod set exceeds 15 °C and air temperature is around 19 °C (Kirchner and late applications result in major plant damage along the 1966), which coincidences with the early flowering stage of driving alleys, among other problems. Consequently, the OSR in most years (Fröhlich 1956a; Williams et al. 1987a). second generation develops undisturbed and can only be Pupation itself is not influenced by soil moisture (Erichsen controlled indirectly by a reduction of the previous genera- 1982; Hughes 1998; Kirchner 1966). However, soil moisture tion. Thus, a thorough understanding of the factors driving affects the warming of the soil and the mechanical resistance D. brassiae population dynamics is absolutely necessary for for the movement of pupae to the soil surface (Blume et al. the successful management of this multivoltine pest insect, 2016). Consequently, the emergence of midges within one with only one application against the first generation early in field can vary due to small-scale differences in soil moisture the season. For targeted control, it is important to precisely and soil type and depends also on the depths at which the determine the time point at which a pest insect emerges and cocoons were located in the soil. The flight period of the first immigrates into the crop. Species-specific migration behav - generation lasts about 3–6 weeks (Williams et al. 1987a). iour has a major impact, on which fields, or areas within, Shifting temperatures can delay emergence, and often there will be infested. Knowledge about the maximum reproduc- is no constant flight, but several waves of migration. tion capacity of a single female is important for estimat- The emergence of D. brassicae occurs mainly in the ing the maximum possible population increase over several morning (Buhl 1960). At the emergence site, virgin females generations at a given pest insect density. These and other show a “calling behavior” and release a sex pheromone aspects are linked to biological traits in the life cycle of D. (Williams and Martin 1986) that is produced by glandular brassicae, which are addressed in the first part of this review. tissue in the epidermis of an intersegmental membrane in the To predict the occurrence of a pest insect and the related ovipositor (Isidoro et al. 1992). After mating, the females damage, the most important factors influencing its popula- immediately search for host plants, which is illustrated by tion dynamics have to be known. This is analysed in the sec- the curve of the flight activity at the emergence sites (Mur - ond part of this review. Together, this information can pro- chie et al. 2001). It was observed that the curve is unimodal vide the basis for the development of economic thresholds with a peak for males at 9:00 (searching for virgin females) 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 647 and time shifted at 11:00 for females (mated females search cuticula (Åhman 1986). On a potential host plant, females for suitable host plants). There is no flight activity at night can be observed walking along pods. Tactile and sensory time (Murchie et al. 2001) (Fig. 1). stimuli are perceived by the tarsi and antennae (Coutin 1964). In most cases, females lay their eggs in pods that were Finding and accepting host plants previously damaged (Åhman 1987). Potential oviposition sites are externally palpated with the maxillary palps and In general, the range of dissemination of D. brassicae is finally investigated by the insertion of the ovipositor which rather low. In search of new host plants, the females mainly is equipped with different types of sensory hairs at its tip fly downwind (Sylvén 1970). Just as they deflect the wind, (Hallberg and Åhman 1987). hedges, and other landscape elements can act as barriers or sluices for the dispersal of D. brassicae. Distances of up to Reproduction of Dasineura brassicae 500 m upwind were observed only at low wind speeds of −1 max. 4.5 m  s (Schütte 1964), which indicates an olfactory- Virgin females produce up to 140 eggs in their ovaries (Syl- mediated upwind anemotaxis. This was confirmed by olfac- vén (1949) cited by Axelsen 1992a); however, the average tometer bioassays in which mated females (but no males) number of eggs laid per female is estimated to be around 60 were attracted to leaves and pods of OSR (Pettersson 1976) (Buhl and Schütte 1971). Adult midges were observed lick- and crushed OSR leaves (Williams and Martin 1986). At a ing on plant sap (Fröhlich 1960), but no feeding behaviour shorter distance, males and females of D. brassicae respond of the adults was observed so far. Whether egg maturation in positively to the yellow colour of the flowers (Williams and D. brassicae is proovigenic, or whether additional eggs also Cook 2010). mature after eclosion, is not yet known. However, fecun- Host plants of D. brassicae are OSR, close relatives such dity is correlated with the body length of a female (Sylvén as turnip rape (Brassica rapa subsp. oleifera), cabbage (1949), cited by Åhman 1985), which indicates that all eggs (Brassica oleracera), and some cruciferous weeds. In gen- mature before eclosion. Environmental stimuli affect ovipo- eral, the survival on Brassica spp. is higher than on other sition as well. According to Fröhlich (1956a) temperatures cruciferous plants, which only serve as hosts to a limited above 19 °C are preferred for oviposition. Additionally, the extend (Åhman 1988; Speyer 1925). In choice tests between quality of a host plant influences the egg loads and at a later OSR and other crucifers, females did land more frequently stage, larval weights which are higher on suitable hosts, on OSR and the number of batches per ovipositing female compared to low-quality hosts (Åhman 1988). Females was higher (Åhman 1988). The initial host plant adaption lay their eggs in several batches, and there is evidence for behaviour is probably elicited by the wax composition of the monogeny of broods of a single midge (Murchie and Hume 2003). Regarding the overall sex ratio in D. brassicae, sev- eral authors described a slight bias towards females (Buhl 1960; Fröhlich 1956a; Murchie and Hume 2003). The development of the eggs and larvae depends on tem- perature (Axelsen 1992b; Hughes 1998). Eggs hatch after 3–4  days and the egg-larval stage of the first generation needs 134°DD above a developmental threshold of 6.7 °C, which lasts about 3–4 weeks in the field (Axelsen 1992b). At maturity, larvae leave the pods and drop down to the soil where they burrow in 0–5 cm depth (Buhl 1960; Fröhlich 1956a). According to Buhl (1960) about 5% of the first-generation larvae, but almost 80% of the second-generation larvae enter winter diapause. In contrast, Axelsen et al. (1997) found that the proportion of larvae that enter diapause varies within a season and between years and is not constantly increasing in every generation. The authors suggested that the cumula- Fig. 1 Female of Dasineura brassicae. The adults of D. brassicae are tive solar radiation perceived by the growing larvae trig- delicate with body length of 0.7–1.5  mm (♂) and 0.9–2.2  mm (♀), respectively (Kirk 1992). Males have stalked antennae with annular gers diapause. Still the specific factors that control diapause sensory hairs. Distinctive features of the female are the non-stalked induction remain unknown. Additional, not all diapausing antennae and the ovipositor. The three larval instars live gregariously larvae pupate in the following year, e.g. Schütte (1979) within the pods and grow up to 2 mm. The first larval instar is almost investigated that 13% of the overwintering larvae did not translucent, and older larvae are white coloured with yellow fat bod- ies emerge in spring following diapause. Diapausing larvae of 1 3 648 J. Hausmann D. brassicae can survive in the soil for up to 5 years (Buhl top gauze net. Each six cups (replicates) were placed in 1960; Nilsson et al. 2004), but there is a negative correlation climate chambers (RUMED®, P 210) at constant tempera- between the duration of the cocoon stage in the soil and the ture levels of 10 °C, 15 °C, 20 °C, and 25 °C. The experi- average lifespan of adults (Schütte 1979). ments started at 12 a.m., and the mortality of the midges was recorded every six hours for three days. Thereafter, Life expectancy of Dasineura brassicae assessments were made every 12 h. Data analysis was performed using R (version 3.6.1) In the field, a life expectancy of 1–3 days is assumed for (R Core Team 2019). A generalized linear model (glm) adult D. brassicae (Williams 2010b), though conclusive explaining the number of dead midges per cup by tem- reports on the lifespan of D. brassicae are missing. Hughes perature treatments and time was fitted. A binomial error (1998) demonstrated that the lifespan of D. brassicae is distribution was assumed. The effects of different variables temperature dependent; however, experiments were biased were tested via an analysis of deviance using the “Chi- because midges had no access to water and did not survive test”. For model diagnostics, the residuals were plotted longer than 48 h in any of the temperature regimes. against the predicted values and the explanatory variables To shed more light on this question, I have conducted and were checked visually. The LT values were calcu- an experiment in which larvae of the second genera- lated using the function dose.p from the MASS package tion were collected in the field in 2019 and were held (Venables and Ripley 2007). The effect of different tem - for almost one year in moist sand at 5 °C in the climate peratures on the mortality of midges over time was also chamber, before they were reared to adult midges. The analysed using Kaplan–Meier survival analysis. midges used for this experiment, emerged from the same As a result, 50% of female D. brassicae were alive for sample in the morning of the 16th June 2020. Groups of 35 h (SE ± 1.2) at 25 °C (max. 66 h) (Fig. 2). At a con- five females were transferred into transparent plastic cups stant temperature of 10 °C, the LT was 224 h (SE ± 6.8) (500 ml, height 16.5 cm), which had three openings (each and single females lived up to 17  days. Adult lifespan 4  cm ), covered with gauze to allow the circulation of air. was significantly dependent on temperature treatments A water saturated cube (3.5  cm ) of floral foam in each (Kaplan–Meier survival analysis, p < 0.001). This outcome cup supplied moisture to the midges. The foam cubes were confirmed that under humid conditions, adult lifespan is resupplied with drops of tap water every 12 h through the inversely related to temperature. Fig. 2 Calculated mortality with 95% confidence limits of Dasineura brassicae females over the time (hours). Midges were kept in plastic cups with a moist cube of floral foam at constant temperatures. Dashed lines indicate the time after which 50% of the midges have died (LT ). n = 30 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 649 quickly changing weather conditions during the flight Drivers of population dynamics period of the first and second generation, especially pre- cipitation, may kill adults and prevent successful oviposi- A distinction can be made between factors that have the tion. Strong winds may disperse the first-generation adults potential to promote population dynamics of D. brassicae and partly prevent colonization of suitable crops. and others that have negative effects (Fig.  3). As mentioned earlier, D. brassicae is reliant on damaged Regarding the life cycle, Axelsen (1992c) identified two pods for oviposition because the ovipositor is not suitable for critical life stages, in which the population of D. brassicae piercing or drilling of mature pod walls, as demonstrated by suffers larger losses, namely the pre-cocoon stage and the morphological studies (Hallberg and Åhman 1987; Stech- diapause during winter. The author calculated a generation mann and Schütte 1978). For this reason, the cabbage seed- survival of about 2–4% (Axelsen 1992c). During the pre- pod weevil, Ceutorhynchus obstrictus Marsham (Coleoptera: cocoon stage, which is the time period between the drop- Curculionidae), by injuring on the pods through its feeding ping of larvae from the pods until they spin a cocoon in and oviposition activity, is considered the most important the soil, losses may occur because of predation by carabids factor for a severe infestation of an OSR crop with D. bras- (Warner et al. 2000) and spiders (Felsmann 2007). In addi- sicae (Ferguson et al. 1995; Free et al. 1983; Speyer 1921). tion, dry weather conditions that lead to desiccation are Strong increases in the seed weevil population lead to a being discussed (Axelsen 1992c). The losses during dia- time shifted growth of the D. brassicae population (Schütte pause can be attributed to parasitism (Ferguson et al. 2004; 1979). In many cage trials on OSR, no oviposition of D. Murchie 1996), pathogens (Hokkanen et al. 2003), and brassicae could be observed without artificial injury of the adverse effects of tillage, e.g. ploughing (Axelsen 1992c). pods or the addition of C. obstrictus (Ankersmit 1955; Buhl There is still a need for research on all of these points. 1957; Doberitz 1973; Fröhlich 1956b; Hughes and Evans Weather conditions can affect the population dynam- 2003). In contrast, several authors described that D. bras- ics of D. brassicae in different ways. As described, many sicae can also independently oviposit in small and young physiological processes, like the emergence of the first pods up to a length of 40 mm (Axelsen 1992c; Fröhlich generation, egg laying, larval and pupal development, and 1956b; Hoßfeld 1963; Mühle 1951; Nietzke 1976). Thus, C. lifespan, are temperature dependent. Warmer tempera- obstrictus is probably more important for the development of tures reduce the developmental time of eggs, larvae, and the second than the first generation. Also, at low pest insect pupae, resulting in a faster generation turnover. Whether densities, the abundance of C. obstrictus is not limiting the diapause is induced by environmental conditions remains population size of D. brassicae (Axelsen 1992a; Fröhlich to be investigated. On the other hand, it seems likely that 1956b). This can be explained by the larvae of D. brassicae Fig. 3 The life cycle of Dasineura brassicae, modified after Buhl 1960 1 3 650 J. Hausmann living gregariously and more than one female using a suit- et al. 2004; Thiem 1970; Warner et al. 2000). In addition, the able pod for oviposition. For this reason, the average number proportion of damaged pods cannot be equated with yield of larvae within one pod can fluctuate considerably and is losses, since OSR compensates early pod losses up to 10% dependent on the availability of damaged pods for female by increasing grain weight (Diepenbrock 2000; Erichsen midges. In addition, other phytophagous insects, such as 1982; Williams and Free 1979), and also compensates early lygid bugs [Lygus spp. (Heteroptera: Miridae)] (Hughes pod losses at the main inflorescence on lateral shoots (Pinet and Evans 2003) or abiotic damages such as hail and wind et al. 2015). The plant’s ability to compensate, however, is (Winfield 1992), can provide suitable oviposition sites. Con- less pronounced for damage caused by the second genera- cluding, C. obstrictus is important for the economic damage tion of the midge. potential of D. brassicae within one year, but not a manda- Knowing the important driving factors of an insect’s tory prerequisite. population dynamics and their relation to potential damage, an economic action threshold can be derived. Presently, threshold values for direct control of D. brassicae do not Challenges for the implementation exist in most European countries. Most commonly, the eco- of integrated pest management nomic threshold for C. obstrictus, the alleged pioneer of the midge, is lowered from one weevil per plant to one weevil Defining economic thresholds per two plants, if both pest insect species occur together (Heimbach 2017; Ramsden et al. 2017). Older thresholds Dasineura brassicae is a typical r-strategist, with short for D. brassicae ranged between 0.25–1 midges per plant generation time and high reproductive capacity. The short (Heimbach 2017; Lauenstein 1993). Other approaches try lifespan of the adults is particularly challenging for farmers, to predict the damage potential from the overall population because the midges start egg laying immediately after their size of D. brassicae estimated from the number of D. bras- emergence in OSR, leaving little time for control measures. sicae cocoons that are washed out of soil samples. Buhl As stated above, it was shown that the abundance of the wee- and Schütte (1964) recommended to treat OSR fields in a vil C. obstrictus at full flowering promotes pod damage by region if the number of cocoons with living larvae in the soil D. brassicae later in the season. However, predation, parasit- exceeds the threshold of 40 per 100  cm . A similar method is ism, and weather conditions (especially temperature) seem used in several federal states in northeast Germany. Here, the to be additional important drivers of the midge’s population threshold for insecticide applications in the following year dynamics. Main losses during the life cycle occur during the against C. obstrictus is lowered if the average number of 25 winter diapause and the overall generation survival is low. cocoons per 100  cm (assessed after the harvest of OSR) Nevertheless, small numbers of individuals seem to be able is exceeded (Hahn, M pers. communication). However, it to build up a strong population over the season, if condi- should be stated that a scientic fi ally based and peer-reviewed tions are favourable. Hence, the shift from the first to the economic threshold does not exist. second generation should be the focal point for the overall reproduction capabilities and population size within one sea- Pest monitoring son. Altogether, it is difficult to make a prediction about the population dynamics of two generations, at the time when The establishment of an economic threshold requires moni- the decision for or against an active control has to be made. toring of the pest insect and represents the second stage in This challenge should be met by an economic threshold, the implementation of an IPM strategy. In case of D. bras- the creation of which is the first step of the IPM approach. sicae, the monitoring is challenging for several reasons, not Therefore, knowledge about the potential damage of a pest least because of the insect’s small size (Fig. 1). Adults of insect and the tolerance of a host plant towards a pest insect D. brassicae can be reliably differentiated from other gall is needed, as well as a reliable monitoring system (Ramsden midge species by their specific wing veining (Fig.  4), but et al. 2017). this feature is difficult to identify with the naked eye. Con- The overall damage by D. brassicae is usually determined sequently, monitoring of D. brassicae midges by farmers did by counting infested pods per plant during the ripening stage never catch on in praxis. of OSR (see EPPO Standard PP 1/220). The proportion of The emergence and flight of the first generation can damaged pods can exceed 50%, and high infestation rates be monitored by using photoeclectors that are placed at with yield losses were reported regularly in the past hun- the OSR fields of the previous year (Waede 1960). In dred years (Buhl 1960; Döring and Ulber 2012; Fröhlich addition, there are commercial prediction models that 1956b; Kirchner 1966; Nilsson et al. 2015; Schütte 1979; indicate which days are suitable for the first generation Speyer 1925; Thiem 1970). However, the damage is often of D. brassicae to emerge and that also calculate what concentrated at field margins and the head lands (Ferguson percentage of the flight period has passed (Johnen et al. 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 651 Preventive measures In IPM, preventive measures that reduce pest insect densi- ties are preferable to direct control measures. Such indirect and preventive measures can include cultural measures, crop rotation, resistant cultivars, landscape management, and the enhancement of natural enemies (Hokkanen 2015). Dasineura brassicae can use spring sown OSR to develop Fig. 4 The veining of Dasineura brassicae, modified after Kirk 1992. a strong third generation (Axelsen 1992c). For this reason, Wings have three veins reaching the wing margin. Typically, the long the growing of winter and spring sown OSR in the same vein from the base ends just before the tip of the wing region has been considered a key factor for the development of large D. brassicae populations and heavy infestations for a long time (Doberitz 1973; Speyer 1921). To what extent a third generation is limited by the lack of suitable host plants 2010). Based on regional meteorological data, these pre- or by the induction of diapause of second-generation larvae, diction models can help farmers to determine the critical needs to be further investigated. The control of cruciferous time when immigration of D. brassicae in their region is weeds, especially on non-crop habitats, was recommended probable. Field-specific forecasts are not possible though, by Speyer (1921). However, it was shown that D. brassicae since the migration of females to the new crop is affected survives only in small numbers on such weeds, which limits by factors like wind and the distance from the previous the potential of this measure (Åhman 1988). As the dispersal year’s OSR fields. Information on which specific fields capabilities of D. brassicae are limited, the cultivation area or parts of a field are colonized is crucial for the imple- of OSR at landscape scale affects the damage potential of mentation of IPM. Yellow water traps are potentially suit- the midge as well. The risk of infestation is reduced to less able for this purpose, although they create the risk of than half, if a distance of more than 3 km of this year’s OSR misidentification, as several similar gall midge species is maintained from the previous year's cropland (Erichsen can be found in the OSR fields. For this reason, attempts 1982). To interfere with the build-up of high pest popula- were made to selectively catch D. brassicae using baited tions, the interruption of OSR cultivation at a landscape traps. The addition of an extract of OSR seeds with a scale is suggested as a possibility (Zheng et al. 2020). This high content of glucosinolates to water traps increased was successfully demonstrated for C. obstrictus and D. bras- the capture efficiency at the emergence sites (Erichsen sicae in a one-season trial in northern Germany (Schütte and Daebeler 1987). Traps baited with allyl isothiocy- 1979). anate caught more male and female D. brassicae than Soil tillage affects the vertical distribution of cocoons traps baited with 2-phenylethyl isothiocyanate or unbaited in the soil (Buhl 1960; Froese 1992). Ploughing did nei- traps (Murchie et al. 1997). However, mostly males were ther reduce the number of D. brassicae cocoons in the soil caught in both studies. Traps baited with the sex phero- (Nielsen et al. 1994) nor the total emergence of adults in mone of virgin females (Williams and Martin 1986) also spring (Axelsen 1995), though the temporal distribution of selectively caught D. brassicae but also predominately the emergence was expanded. Still, some authors assume males (Williams 1990). Since males usually remain at the that ploughing is an important mortality factor for D. brassi- emergence sites after mating, their catch is not suitable cae (Axelsen 1992c; Ferguson et al. 2004; Williams 2010b). to predict the colonization of the OSR fields by females. Dasineura brassicae can discriminate between low- and The development of a trap attracting specifically female good-quality hosts (Åhman 1988). The differences in alight- midges would be a great step forward in the monitoring ing frequency between different Brassica spp. indicate the of D. brassicae. possibility of antixenosis (Åhman 1988). The lower rates of In recent years, agriculture has experienced a trend survival and larval weights on low-quality hosts are prob- towards the use of new, innovative technologies. Artificial ably related to lower nutritional values or substances that intelligence and camera traps enable the development of are harmful for D. brassicae (Åhman 1985), which could real-time monitoring systems. For example, lidar technol- be seen as a kind of antibiosis. In summary, these are differ - ogy allows insects to be identified in situ by their wing ent starting points for breeding resistant cultivars. However, beat, colour, and the proportions of wing width to body successful resistance breeding against D. brassicae is not size. Technology offers promising possibilities for the foreseeable yet based on the limited knowledge of variability monitoring of flying insects (Brydegaard and Svanberg in resistance of OSR and related species for this pest. 2018), and first tests with pest insects in OSR have been Natural enemies contribute to the control of D. brassi- carried out (Kirkeby et al. 2021). cae populations by predation and parasitisation. At least 31 1 3 652 J. Hausmann parasitoid species parasitize eggs and larval stages of D. activity of the insecticides will often decline rapidly in the brassicae (Ulber et al. 2010b). The key parasitoid species e fi ld. Hence, it is a challenge to protect the crop with a single are Platygaster subuliformis (Hymenoptera: Platygastridae) insecticide application, which requires a precise timing of and Omphale clypealis (Hymenoptera: Eulophidae), both the application. Therefore, reliable and precise monitoring widely distributed in Central and Northern Europe (Ulber data would be a prerequisite. et al. 2010b). However, the multivoltine life history of the Until now, D. brassicae is sensitive to insecticides and host and its parasitoids complicate investigations and exten- there is no evidence of insecticide resistance. However, in sive studies on parasitism in D. brassicae are scarce. Exist- Germany, increasing pyrethroid resistance in populations ing studies indicate substantial variability in parasitism rates of C. obstrictus can be observed (Brandes and Heimbach (Murchie 1996). In general, parasitism rates post-diapause 2019). seem to be higher and can exceed 50% (Ferguson et  al. Insecticide applications below the flowering canopy of 2004; Murchie 1996). Predation of larvae might also affect the crop with dropleg technique can reduce side effects on D. brassicae populations. Larvae are especially vulnerable pollinators but tend to have reduced efficacy against D. bras- to predation by spiders or ground dwelling predators, when sicae (Hausmann et al. 2019). Regarding alternative con- they drop down from the pods to pupate into the soil. Alto- trol measures, only few studies have investigated botanicals gether, 11 carabid species fed on pod midge larvae in labora- such as extracts from neem tree (Azadirachta indica) (Pavela tory studies; however in choice tests, species differed in their et al. 2009) or the application of nitrophenoles (Kazda et al. preference for D. brassicae and in the amount of consumed 2015), which have shown some efficacy in field trials. larvae (Williams et al. 2010). Only Amara similata (Coleop- tera: Carabidae) was proven to feed on larvae in field studies (Schlein and Büchs 2006). Spiders may prey on larvae and Conclusions emerging midges of the first generation. Studies of Felsmann (2007) revealed a temporal coincidence between web densi- This literature review shows that so far IPM of D. brassicae ties of linyphiid spiders and both, the dropping of larvae, and in OSR is rather a collection of promising ideas than state the emergence of new generation midges in OSR. of the art. Most preventive control measures are limited in In conclusion, preventive measures can contribute to a terms of their efficiencies. Resistance breeding or a large- reduction of D. brassicae infestation to a limited extent. scale interruption of OSR cultivation in individual years is In particular, the potential of natural antagonists, such as difficult to establish in the short term and more knowledge predators and parasitoids, should be further explored and about the effectiveness of all these measures is needed. De promoted through adherence to good agricultural practice facto, direct control with insecticides remains the most effec- (i.e. IPM, use of economic thresholds). The distance to OSR tive control measure, and it is, therefore, essential that it is fields of the previous year, and the avoidance of winter and practiced within the framework of IPM. So far, the most spring sown oilseed rape in the crop rotation, are effective practicable option to predict D. brassicae damage appears measures to reduce pest pressure. to be monitoring of C. obstrictus, which provides access to pods and so for a mass propagation. However, a clear Control measures relation between the two species only exists at high pest insect densities. At present, insecticide sprays in flowering The brassica pod midge has been a subject of research since OSR are often retrospectively motivated and tend to have the 1850 (Winnertz 1853) and different control options have character of an insurance spray rather than being targeted been under discussion so far. Early on, the control of D. and economically justified from an integrated pest manage- brassicae was rather indirect, while direct measures aimed ment perspective. To improve this, the development of an for control of the cabbage seedpod weevil C. obstrictus (Spe- economic threshold for D. brassicae is a necessary require- yer 1921). In general, insecticide spray treatments of field ment. So far, it is poorly understood what the number of margins and headlands are considered adequate for moder- individuals constitutes the critical threshold for a potential ate pest insect pressure (Ferguson et al. 2004; Thiem 1970). mass propagation within the season. Therefore, the mortality Today, control of the cabbage seedpod weevil and the bras- rate of the first generation of D. brassicae and other factors sica pod midge pest insect complex relies mainly on the favouring the development of a large second generation need use of synthetic chemical insecticides. All direct measures to be studied in detail. To be reliable, prediction models target C. obstrictus and the first generation of D. brassicae. of potential crop damages should further include tempera- Insecticides with non-systemic properties have to be applied ture as a variable, as this affects many aspects of population before the main flight, to hit the midges before they start lay - development. However, the absence of long-term weather ing eggs. Since OSR is rapidly growing during the flower - forecast has a limiting effect. Furthermore, there is great ing period and temperatures can be quite warm, the residual need for an improved method that allows easy monitoring 1 3 Challenges for integrated pest management of Dasineura brassicae in oilseed rape 653 Axelsen JA (1992) The developmental time of the pod gall midge Das- of D. brassicae. Currently, the identification of midges in yneura brassicae Winn. (Dipt., Cecidomyiidae). J Appl Entomol the field is not practicable and it is therefore impossible to 114:263–267. h t t p s : / / d o i . o rg / 1 0 . 1 1 1 1 / j . 1 4 3 9 - 0 4 1 8 . 1 9 9 2 . t b 0 1 1 determine which fields or specific areas within a given field 25.x are infested and are likely to suffer crop damage. Promising Axelsen JA (1992) The population dynamics and mortalities of the pod gall midge (Dasyneura brassicae Winn.) (Dipt., Cecidomyiidae) avenues of research are the development of selective attract- in winter rape and spring rape (Brassica napus L.) in Denmark. J ants and real-time monitoring of insects, using remote-sens- Appl Entomol 114:463–471. https://doi. or g/10. 1111/j. 1439- 0418. ing technology. 1992. tb011 52.x Axelsen JA (1995) The winter mortality and emergence time of Acknowledgements I would like to thank Meike Brandes, Michael Dasineura brassicae in Denmark. IOBC-WPRS Bul 18:81–87 Rostás, Jan Schinkel, and Bernd Ulber, who contributed to the work Axelsen JA, Fink R, Kjaer C (1997) Global solar radiation as the factor through many discussions and helpful suggestions. My thanks also go controlling induction of diapause in the pod midge (Dasyneura to Urs Wyss, who kindly provided a picture of Dasineura brassicae. brassicae Winn.). Oecologia 111:178–182. https:// doi. org/ 10. 1007/ s0044 20050 223 Barzman M, Bàrberi P, Birch ANE, Boonekamp P, Dachbrodt-Saaydeh Funding Open Access funding enabled and organized by Projekt S, Graf B, Hommel B, Jensen JE, Kiss J, Kudsk P, Lamichhane DEAL. 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Journal

Arthropod-Plant InteractionsSpringer Journals

Published: Oct 1, 2021

Keywords: Insect pests; Monitoring; Pest control; Economic threshold

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