Disruption of trophic interactions involving the heather beetle by atmospheric nitrogen deposition

Elevated nitrogen (N) deposition impacts the structure and functioning of heathland ecosystems across Europe. Calluna plants under high N-inputs are very sensitive to secondary stress factors, including defoliation attacks by the heather beetle. These attacks result in serious damage or death of Calluna, its rapid replacement by grasses, and the subsequent loss of heathland. We know very little about the mechanisms that control the populations and trigger outbreaks of the heather beetle, impeding proper management measures to mitigate the damage. We investigated the effects of N deposition on the relationships between the heather beetle, its host plant, and two arthropod predators at building (rejuvenated through fire) and mature heathlands. The study combines field manipulation experiments simulating a range of N deposition rates (0, 1, 2, 5 g N m⁻² year⁻¹ for 2 years, and 5.6 g N m⁻² year⁻¹ for 10 years), and food-choice laboratory experiments testing the preferences of adults and larvae of the heather beetle for N-treated Calluna plants, and the preferences of predators for larvae grown on plants with different N-content. The larvae of the heather beetle achieved the highest abundances after the long-term (10-year) addition of N at mature Calluna plots in the field. Contrary to the adults, the larvae foraged preferentially on the most N-rich Calluna shoots under laboratory conditions. Predators showed no aggregative numerical responses to the accumulation of heather beetle larvae at high N-input experimental plots. During the feeding trials, predators consumed a small number of larvae, both in total and per individual, and systematically avoided eating the larvae reared on high-N Calluna shoots. Our study showed that the most severe defoliation damage by the heather beetle is inflicted at the larval stage under prolonged availability of high-N inputs, and that arthropod predators might not act as effective regulators of the beetle's populations. - Highlights: • Heather beetle adults consumed high rates of low-N content Calluna shoots. • Heather beetle larvae foraged preferentially on high-N content Calluna shoots. • Heather beetle larvae reached high abundances after the long-term addition of N. • Polyphagous predators did not respond to larval accumulation at high-N Calluna plots. • Polyphagous predators avoided eating larvae reared on high-N content Calluna shoots. - Effects of N deposition on the heather beetle, its host plant and two predators were investigated by a long-term field manipulation study, laboratory rearing and food-choice experiments.