Sown wildflower fields are an efficient measure to reduce visitation rates of honeybees and other pollinating insects on Jacobaea vulgaris

Highlights

• Mass occurrences of Jacobaea vulgaris may be hazardous to livestock and humans.

• Common countermeasures undermine conservation targets of extensive grasslands.

• Wildflower patches reduce pollinator visitation rates on J. vulgaris.

• Our findings add to the evidence for the multifunctional role of wildflower fields.

• Wildflower fields may also assist in reducing the spread of invasive plants.

Abstract

Local mass occurrences of Tansy ragwort (Jacobaea vulgaris, Asteraceae), a native plant usually sparsely interspersed within extensive grassland, have been suggested to cause health hazards for livestock and humans. While current management options, particularly herbicide application and mechanical eradication, undermine conservation targets of extensive grasslands, sown wildflowers are a popular agri-environment scheme that may reduce pollinator visitation on J. vulgaris and thus, mitigate the plant’s dominance. Hence, with this study we aimed to explore whether the availability of sown wildflower patches reduces pollinator visitation rates on J. vulgaris in species-rich and species-poor grassland, respectively, and whether patterns depend on wildflower cover. To do so, we monitored pollinator visitation rates on J. vulgaris when wildflower fields were available to flower visitors or temporarily covered by mesh nets in a field experiment. The availability of wildflower patches significantly reduced visitation rates of honeybees, bumblebees, solitary bees and hoverflies on J. vulgaris, while increasing wildflower cover promoted this effect for J. vulgaris in species-poor grassland. Moreover, species-specific flower preferences and seasonal shifts in the quantitative availability of wildflower species determined the efficacy of wildflower patches. To conclude, our findings suggest sown wildflower fields as an alternative management option to mitigate the dominance of J. vulgaris in plant-pollinator networks given that wildflower mixtures are tailored to species-specific requirements of flower visitors. Future research, however, should explore whether wildflower fields ultimately mitigate the negative consequences associated with the local mass occurrences of J. vulgaris without undermining conservation targets on extensive grassland.

Introduction

Tansy ragwort (Jacobaea vulgaris, Asteraceae, formerly Senecio jacobaea), a grassland species native throughout central Europe, has been reported to show a sudden and disproportionate spread coupled with local mass occurrences. Common measures to mitigate these local mass occurrences and thus, prevent potential health hazards for livestock and humans include herbicide application and mechanical eradication, which however, undermine conservation targets on extensively managed grassland. Hence, we aimed to explore sown wildflower patches as an alternative measure to mitigate the negative consequences associated with J. vulgaris.

Jacobaea vulgaris is a native plant species on extensively managed grassland throughout central Europe, usually characterized by a sparse distribution with single stands of individual plants (Neumann and Huckauf, 2016). During the last 20 years, however, J. vulgaris has repeatedly been reported to show local mass occurrences, i.e. in Germany (Augustin et al., 2018; Gottschalk et al., 2018; Neumann and Huckauf, 2016) and Switzerland (Suter et al., 2007). Concerns associated with the mass occurrences of J. vulgaris largely originate from pyrrolizidine alkaloids, the most widespread phytochemicals that serve as anti-herbivore defence in more than 6000 plant species and about 3% of all flowering plants worldwide, respectively (Moreira et al., 2018; Wiedenfeld et al., 2008). Despite limited empirical evidence, the consumption of J. vulgaris by livestock, i.e. contained in dry fodder, has been suggested to cause mild toxicity and occasionally lethal incidents, i.e. in cattle and horses (Augustin et al., 2018; Cortinovis and Caloni, 2015). Moreover, current scientific evidence does not reliable exclude health hazards to humans due to the consumption of honey when beehives are in close proximity to mass occurrences of J. vulgaris (Moreira et al., 2018, and sources therein). Hence, even though J. vulgaris is native to central Europe it is vital to develop efficient management measures, which do not aim at complete eradication but mitigate the consequences associated with its local mass occurrences.

The disproportionate spread of native plant species is – similar to alien species – a result of a complex interplay of multiple factors, including characteristics of the respective species and determinants of the local environment including natural or anthropogenic disturbances (Bjerknes et al., 2007; Keane, 2002; Levine et al., 2003; Richardson et al., 2007). With respect to mass occurrences of J. vulgaris, land-use changes during the last centuries seem to be a major driver, particularly the extensification of grassland in order to promote biodiversity in landscapes dominated by agriculture. Therefore, management suggestions to mitigate the local spread of J. vulgaris mainly entail increased fertilization, intensified grazing or chemical control (Roberts and Pullin, 2007). While the efficiency of those measures is still under debate, side effects on valuable and protected non-target organisms as well as the protected status of extensively managed grassland largely preclude their unrestrained application (Augustin et al., 2018) and call for the development of alternative management options.

An alternative management option may build on previous studies suggesting that the flowering period of J. vulgaris coincides with a scarcity of alternative flower resources in modern agro-ecosystems (Augustin et al., 2018; Cameron, 1935; Neumann and Huckauf, 2016). Modern agro-ecosystems are dominated by large-scale agricultural monocultures that do not provide a broad range of resources for pollinators across seasons (Baude et al., 2016). Thus, subsequent to highly rewarding mass-flowering crops such as oilseed rape early in the season, pollinators in agricultural landscapes may be attracted by and confined to densely growing patches of J. vulgaris. In turn, being the sole provider of flower resources may increase pollinator visitation rates on J. vulgaris and, with respect to honeybees, pollen shares of J. vulgaris and thus, pyrrolizidine alkaloid content in honey (Neumann and Huckauf, 2016). Consequently, increased pollinator visitation rates may promote pollen deposition and seed set and ultimately, plant reproductive success (Kehrberger and Holzschuh, 2019).

In fact, plant-animal mutualisms such as animal-mediated pollination have been identified as one of the key mechanisms that promote the reproductive success and thereby, facilitate the invasive spread of alien plant species (Aizen et al., 2008; Richardson et al., 2007). Pollination particularly plays a decisive role for the successful establishment of generalist alien plant species, often characterized by an exuberant flower display, extended flowering phenology and highly rewarding flowers, such as Impatiens glandulifera (Chittka and Schürkens, 2001; Richardson et al., 2007; Vervoort et al., 2011). Similarly, the native J. vulgaris exhibits a generalist pollination syndrome and is visited by a broad range of different pollinator species, i.e. hoverflies, solitary bees, bumblebees and butterflies (Vanparys et al., 2011, 2008). Based on previous studies, increased visitation rates seem to translate into higher seed set and thus, reproductive success in J. vulgaris (Vanparys et al., 2011, 2008). Consequently, interference with the plant-pollinator mutualism of J. vulgaris through reduced visitation rates of honeybees and other pollinating insects may pose an alternative management option not explicitly discussed so far (Carvalheiro et al., 2014).

This alternative management option may entail a targeted provisioning of alternative flower resources in agro-ecosystems, i.e. by sowing wildflower fields in close proximity to mass occurrences of J. vulgaris. Due to the general preference of pollinators for high floral densities, patches of sown wildflower fields adjacent to J. vulgaris may attract pollinators and thereby, exert a concentration and cause an overall increase in pollinator abundances at the local patch scale (Ebeling et al., 2008; Ghazoul, 2006; Hambäck and Englund, 2005; Hegland and Boeke, 2006). Simultaneously, sown wildflower fields offer a wide spectrum of plant species that potentially are more attractive to pollinators than J. vulgaris and may thus, increase competition for shared pollinators (Mitchell et al., 2009; Morales and Traveset, 2009). Hence, even given an overall increase in absolute numbers, pollinators may still focus on potentially more rewarding or preferred wildflower species and thus, visit proportionally fewer flowers of J. vulgaris (Brown and Mitchell, 2001; Dauber et al., 2010; Goulson, 2000; Lázaro et al., 2009). Yet, the potential of co-flowering plants provided by sown wildflower fields to pull pollinators from J. vulgaris may depend on their floral traits and pollinator preferences (Campbell et al., 2012; Hegland and Boeke, 2006). Previous studies suggest that honeybees (Neumann and Huckauf, 2016; Vanparys et al., 2008) as well as other flower-visiting insects such as hoverflies (van Rijn and Wäckers, 2016) do not prefer J. vulgaris. Low pollinator preferences for J. vulgaris may in turn, indicate increased chances of co-flowering plants to reduce pollinator visitation rates on J. vulgaris (Bjerknes et al., 2007; Chittka and Schürkens, 2001; Morales and Aizen, 2006; Morales and Traveset, 2009).

In this study, we aimed to explore an alternative management option that ultimately, may mitigate the negative consequences of local mass occurrences of J. vulgaris for animals and humans without undermining conservation targets on extensive grasslands. Hence, with a field experiment we studied if sown wildflower patches have the potential to reduce visitation rates of honeybees and other pollinating insects on J. vulgaris and whether the efficacy of this measure differs for J. vulgaris grown in species-rich or species-poor grassland and depends on wildflower cover.