Alternative flowering crops as potential food sources for beneficial arthropods

Blühende Alternativkulturen als potentielle Nahrungsquelle für Nützlinge

Material and Methods

In addition, the activity of arthropods within the flowering plots was registered using water traps. These consisted of round transparent plastic bowls (diameter 18 cm) with 2 l capacity, which were installed at the level of the florets of each crop. The bowls were filled with saline solution (3% plus a few drops of liquid soap). Water traps were set into the plots at the time of full blossom for 14 days (Table 1). At the same time, similar traps were put in the grass strip around the experimental field and served as control without flowers around. Every two to three days, captured arthropods were removed from the traps and were transferred into ethanol (70%) for further examination in the laboratory. The arthropods were assigned to the same categories as in the visual observation method.

For graphical analysis, the relative abundance of beneficials (i.e. Apis, Bombus, other wild bees, Syrphidae, para­sitic Hymenoptera, Formicidae, Coccinellidae) in relation to the remaining arthropods in the data set of observed flower visitors were presented in bar charts. The relative distribution of these taxa in the late sowing buckwheat/mustard trial was presented in circular diagrams. The appearance of certain beneficial groups in relation to the different flowering crops (termed as “preference”) was compared by analysing recorded numbers in appropriate general linear models (GLM) with adequate error distribution (R version 3.2.4). For binomial data (number of flower visitors/positive evaluated inflorescence) binomial or quasibinomial models were used. For count data (number of specimen/water trap), poisson models, quasipoisson models or negative binomial models were chosen. The GLM tested the effect of “crop plant species” on the number or proportion of a particular taxon in water traps and observation data. After determination of significance, multiple comparison between means were performed using the library “multcomp” in order to identify preferences of that taxon for particular crop plants. In some cases, the standard error could not be estimated if only zero values exist for a particular plant – insect combination, which leads to an exclusion of these data from the analysis (indicated by # in Tables 2 to 5).

To estimate the diversity of the visitor profile (only the beneficial taxa) of a particular crop plant, the Berger-Parker-Index D (May 1975) was calculated according to D = N_(max)/N, which is the measure of the proportion of the most abundant taxon in the sample (Wheater et al., 2011).

Results

Considering the suggested beneficial guilds, these contribute to more than 50% of the registered arthropods on most of the crop plants (Fig. 1 and 2). Plants with flowers of the open disk type (Table 1) were visited by nearly all considered beneficial taxa (Fig. 1 and 2), but insects with less specialised mouthparts (Coccinellidae, Formicidae, parasitic Hymenoptera, Syrphinae) were more frequent on these plants than members of the Apoidea. The Apiaceae were also frequently visited by beetles belonging to the family Cantharidae. Buckwheat and mustard were visited by the honeybee and some wild bees (especially Lasioglossum, but in the case of mustard also by the rare oligolectic species Andrena agillisima) beside ants and other “short tongue” groups. Plants with more concealed nectaries attracted Apis and Bombus in 2013 (lupine, phacelia) as well as in 2014 (faba bean, milk thistle). But ants exploited also the extrafloral nectaries of faba bean located at the stipulae of the leaves. Flax was mainly visited by bee species.

Fig. 1. Relative abundance of different arthropod groups which had been observed visiting flowers of alternative crop plants in a small-scale field trial in 2013.

Fig. 2. Relative abundance of different arthropod groups which had been observed visiting flowers and/or ex­trafloral nectaries of alternative crop plants in a small-scale field trial in 2014.

The composition of the flower visitors on buckwheat and mustard at two different blooming periods (June 2013 versus August 2013) did not differ fundamentally. For mustard, the proportion of Apoidea accounted to 40 to 50% of the registered beneficial guilds (Fig. 4 and 5) during both periods. The proportion of Syrphinae was higher during the late summer period, which was probably a consequence of higher abundance of this taxon later in the year (increased 2^nd generation of bivoltine species). Buckwheat was always attractive to ants which were frequently observed on the nectar-rich flowers of this plant during early as well as late summer.

Fig. 4. Relative abundance of different arthropod groups which had been observed visiting flowers of yellow mustard (Sinapis alba) blooming in late Au­gust 2013.

Fig. 5. Relative abundance of different arthropod groups which had been observed visiting flowers of buck­wheat (Fagopyrum esculentum) blooming in late August 2013.

The honey bee was observed on all plant species in the year 2013 with a preference for mustard, phacelia and buckwheat (Table 2). In 2014, the milk thistle was most attractive for A. mellifera (Table 3). Representatives of Bombus sp. preferred phacelia in 2013 and also milk thistle in 2014. Both Apis and Bombus were rarely caught in the water traps (Table 4 and 5).

Various wild bees occurred in all plots. Members of the genus Halictus were regularly observed as dominant group in flax in both years, collecting pollen there (Table 2 and 3, Fig. 6). Higher numbers of wild bees were caught in the water traps installed in buckwheat (Table 4 and 5); these belong to various genera (Lasioglossum, Andrena, Hylaeus and others).

Fig. 6. Wild bee Halictus sp. collecting pollen on flo­wers of flax (Linum usitatissimum).

No clear preference for certain flowering plants could be determined for the hoverflies. In the year 2013, many of them were observed in phacelia, but they occurred also in other plots, indicating that they are attracted to many different plants. In general, they were rarely caught in the water traps.

Parasitic Hymenoptera and ants (Lasius niger, Formica species and others) were highly attracted by inflores­cences of parsnip. This plant developed plenty of postfloral nectar droplets on the developing fruits (Fig. 3). Ants were observed on the inflorescences in large numbers (Table 2 and 3) and their prevailing activity was also confirmed by the capture rates in the water traps installed at the height of the inflorescences. Parasitic Hymenoptera were mainly recorded by the water traps and here they were found more frequently in parsnip than in the other crop plots (Table 4 and 5). Parsnip was also the plant most attractive for the Coccinellidae (Table 3).

Fig. 3. Inflorescence of Pa­stinaca sativa showing developing fruits with droplets of nectar (ar­rows).

Flower morphology and especially nectar accessibility determines the suitability of a plant to “feed” beneficial insects (Campbell et al., 2012; Wäckers and van Rijn, 2012; Garibaldi et al., 2015; van Rijn et al., 2016). It is a well-known fact that specialized nectar foragers like honey bees, bumble bees, other bee species and some dipteran groups are able to exploit particular flower types (Kugler, 1970) due to their specialized mouthparts. In contrast, insects with less specialized, more primitive short, broad mouthparts (“chewing type”) have only access to flower types with exposed nectaries and pollen. Most species acting as predators or parasitoids belong to this group. These biological determinants (flower trait, mouthpart morphology) need to be considered for the design of improved plant composition in flowering strips adjacent to agricultural fields or orchards (Wäckers and van Rijn, 2012). Recent research demonstrated the usefulness of this concept with the aim to promote particular beneficials and their ecosystem services like pest control or pollination (Campbell, 2014; Garibaldi et al., 2015; Tschumi et al., 2015; van Rijn et al., 2016).

In addition to semi-natural habitats (flower strips, field margins, hedgerows etc.), also flowering crop plants may contribute to the availability of floral resources in the agricultural landscape. Oilseed rape is an early mass-flowering crop attractive for many beneficial groups (Jauker and Wolters, 2008; Holzschuh et al., 2013; Diekotter et al., 2014). But other cultivars may provide additional or even better opportunities, e.g. because they flower later in the year or their cultivation does not need the application of insecticides, which may harm flower visitors.

Buckwheat showed the highest diversity of the considered flower visitors in our study (Berger-Parker Index, lowest value D = 0.27), thus supporting a wider range of beneficial taxa (pollinators and pest control agents). Nectaries in buckwheat flowers produce nectar of high viscosity with sugar concentration around 60% sucrose (w/w) (Cawoy et al., 2008; Herz, unpublished data). Its positive effect on the fitness of beneficial insects, especially to parasitic Hymenoptera was demonstrated in numer­ous studies. Increase in survival and consequently realized fecundity of parasitoid females, having access to buckwheat flowers, was frequently reported (Lee et al., 2004; Lee and Heimpel, 2008a, b; Winkler et al., 2009; Laubertie et al., 2012; Pumarino et al., 2012; Sigsgaard et al., 2013; van Rijn et al., 2013). Nectar is secreted from nectaries located at the basis of the stamina which can easily be exploited by short-tongue flower visitors, but are also attractive to honey bees and other bee species. It was reported that buckwheat mainly produced nectar in the morning (Hedtke and Pritsch, 1993) and we observed a frequent “nectar harvesting” by ants in our experiment in the morning too. How this nectar depletion may affect other taxa with a different temporal foraging pattern needs to be explored under field conditions. Buckwheat has many interesting agricultural uses: it is useful as green manure, fodder and biofuel plant as well as pseudocereal in human food. Furthermore, honey production and use for medicinal purposes is possible (Cawoy et al., 2008). Buckwheat can be easily integrated into crop rotation schemes and the cultivation usually does not require the application of any pesticides or herbicides (Heyland et al., 2006). Due to its multifunctional use, several seeding dates are possible (early for seed production, late as green manure or cover crop) and as consequence buckwheat flowering can occur from early June to mid of September in the landscape. Buckwheat is often included as component in annual flower strip plant mixtures (Fig. 7).

Fig. 7. “Greening” mixture composed of yellow mustard, buckwheat and phacelia established along a corn field in 2016.

Also flax was visited by various beneficial groups (D = 0.33). It was highly attractive to wild bees (genus Halictus) as pollen source. Syrphinae were observed too, but it was not clear if they exploited pollen or nectar. Flax opened the flowers mainly during morning and sunshine. The total flowering period was about 3 to 4 weeks. This plant is autophilious, nevertheless nectar and pollen are apparently produced in higher amounts which makes it attractive for many insects. Due to its particular value for beneficial taxa the cultivation of this crop on a broader scale would be desirable. We used a cultivar for oilseed production in our trial. The demand for oilseed is rising (e.g. production of lineseed oil also for human nutrition), especially for the organic sector (Hiltbrunner et al., 2009). Flax is also recommended as a component of so called “greening” cover crops (Anonymous, 2016), which may increase the cultivation of this plant on a larger scale.

Mustard was found to attract many beneficial groups, whereby honey bees were dominant in both years of the study. Later in the year (second sawing in 2013), also Syrphidae (both Eristalinae and Syrphinae) visited the flowers frequently. The nectar is secreted plentiful at the base of the stamina where insects with prolonged mouthparts can reach it easily. Pollen was collected by many bee species, e.g. the oligolectic Andrena agilissima, indicating its value also for rare endangered species. Also higher numbers of small parasitic Hymenoptera were caught in the water traps in mustard plots, being probably attracted by this flowering plant. They might be able to enter the flower and to crawl to the nectaries for feeding, but this still needs to be confirmed. The different varieties of mustard (Sinapis alba and relatives) can be widely used in agriculture (Heyland et al., 2006). They are often used as cover crops and green manure. But they can also deliver oilseed, spices or seeds for technical and medicinal products. Together with buckwheat and phacelia, mustard is included in annual “greening” seed mixtures (Anonymous, 2016, Fig. 7) offering food for a broad range of beneficial taxa.

Due to their more specialized flower type, phacelia, milk thistle, lupine and faba bean provided reward especially for Apoidea, mainly bumble bees and honey bees, which were able to exploit the hidden nectar in the prolonged corolla of these plants. Beneficial taxa with less specialized mouthparts were not observed on the flowers, but ants and parasitic Hymenoptera visited the extrafloral nectaries of faba bean. These EFN already developed on the first leaves of the plants long before flowering. The potential role of these nectar providers for parasitic Hymenoptera requires further research in the field, because laboratory studies showed that parasitoids feed on them and their longevity and fecundity is increased (Jamont et al., 2013; Walach and Herz, 2015). Faba bean and other Leguminosae are suitable cover crops for green manure and within greening regimes and may be even become more important as human food.

Many vegetables belong to the Apiaceae. They are mainly cultivated for their vegetative parts (carrot, fennel, parsnip, celery, dill), although some cultivars are grown for seeds (caraway, coriander, fennel, dill) too. For organic seed production, these plants need to be cultivated till flowering and often require successful pollination by insects (Howlett, 2012). Apiaceae are known to support many natural enemies due to their exposed nectaries and stamina (Kugler, 1970; van Rijn et al., 2016) and wild forms are often recommended to be part of flower strips along arable crops (e.g. Isaacs et al., 2009; Sivinski et al., 2011). We included vegetable cultivars which grew more vigorously than the wild types. Parsnip developed rich nectar droplets of a high sucrose content (around 70% (w/w); Herz unpublished data), especially on the developing seeds (postfloral nectaries, Fig. 3). These droplets were systematically harvested by ants, but also by other insects with unspecialized mouthparts (beetles, wasps, many different Dipteran groups including Syrphidae). In addition, some wild bee species visited carrot and parsnip indicating the values of these plants for them. Seed cultures of Apiaceae certainly need a particular management, but their cultivation may be suitable for some regions and of particular value for organic growers. They flower mainly in the second half of the summer, thus providing an interesting nectar supply during this time which may be important for migrating and overwintering wasps and flies (e.g. Syrphidae, parasitic Hymenoptera).

To conclude, most of the tested plants in this small-scale study supported many beneficial taxa, although their value for particular groups differed in dependence on biological determinants. But due to this fixed relationship, it can be assumed that the findings here can be also found on a larger scale in the agricultural landscape. Certainly the surroundings of agricultural fields and their provision with available nectar and pollen resources affect the attractiveness of the flowering crop plants as it was demonstrated for the role of flowering strips and other semi-natural habitats (Haenke et al., 2009; Haenke et al., 2014; Jonsson et al., 2015). A more diverse array of different crop systems can also have other benefits (less attraction to particular pests), even with economic consequences (Letourneau et al., 2011; Iverson et al., 2014). Thus, strategies which favour crop diversification by including also alternative crops with new purposes may have the effect of benefitting providers of ecosystem services too. To reach this goal, the elaboration of guidelines is needed how these alternative crops can be integrated into the farm management and into the matrix of the surrounding agricultural landscape.