Through a three-year investigation, we found that a moderate decrease of nitrogen from 280 to 140–210 kg N ha−1 did not markedly influence the populations of cereal aphids or the parasitism rate. However, a moderate decrease of nitrogen input from 280 to 140–210 kg N ha−1 maximized the fitness of two predominant Aphidiinae parasitoid species, suggesting parasitoid control of cereal aphid would get benefit from the moderate decrease of nitrogen fertilizer. Those results showed that moderately decreasing nitrogen fertilizer could boost the parasitoid control of cereal aphids. Our research suggests that moderately decreasing nitrogen input is qualitatively beneficial to parasitoids but would not control cereal aphids quantitatively.
Effect of decreasing nitrogen fertilizer on the cereal aphid population
This study demonstrated that nitrogen fertilizer has the potential to positively influence densities of S. avenae and R. padi among all manipulated nitrogen fertilizer levels (70–280 kg N ha−1) (Fig. 1). Similar conclusions have been documented in research linked with aphids, including cereal aphids5,17,24. First, the plant usually responds monotonously and positively to nitrogen fertilizer. The percentage of nitrogen in the dry weight of tobacco leaves was positively associated with fertilizer levels25. Nitrogen fertilizer in the range of 0–225 kg N ha−1 improved nitrogen concentration of canola throughout the growing season26. It has been reported that fertilization has a positive influence on plants, indicating a cascading effect on herbivorous pests24,26,27. Nitrogen input could enhance the nutritional quality of the host, as nitrogen input increases sugars and amino acids availability for aphids, thereby accelerating the population growth of the herbivores28,29. Second, fertilization negatively affects plant defensive responses to herbivores and lessens the amounts of toxins in host plants27. For example, nitrogen fertilizer employed for walnut seedlings decreased the allocation to defensive toxins such as juglone, thereby lowering resistance to walnut aphids30. Third, fertilization alters the microclimate of crops and thereby contributes to the population growth of aphids17,31.
However, only the lowest nitrogen level manipulated in our experiment (70 kg N ha−1) significantly reduced the population of cereal aphids compared with the conventional nitrogen level (280 kg N ha−1) in 2016 and 2017 (Fig. 1). Those results showed that the magnitude of decreasing fertilizer input from the conventional level (280 kg N ha−1) to a moderate level (140–210 kg N ha−1) was insufficient to contain the population of cereal aphids. The performance of cereal aphids could remain unaffected when fertilizer input was decreased to a low level, as aphids could adapt to the pressure of deficient nutrition by sucking more strongly10. Therefore, to reduce the population of cereal aphids, the nitrogen level should be decreased to 70 kg·N·ha−1 or lower. Similarly, as fertilizer was applied to tobacco in the range of 0–200 ppm N, the nymph weights of whiteflies on tobacco plants did not diminish markedly until the nitrogen concentration level was reduced from 200 to 0 ppm N25.
Nevertheless, cereal yield responds to nitrogen levels as a negatively accelerating curve based on previous studies7,9. Far lower nitrogen input sharply reduces grain yield, and moderate nitrogen fertilizer is always imperative in agricultural production2,7. Therefore, the tradeoff between maintaining the essential grain yield and reduction of the pest population would not have been optimized solely by decreasing nitrogen input.
The wheat variety adopted in our experiment was susceptible to cereal aphids. The landscape around our field employed in this experiment was predominated by winter wheat, and thus the landscape was extremely simplified. By comparison, use of a resistant variety and intercropping wheat with another crop mediated the impact of nitrogen input on densities of cereal aphids10,12. If these factors are taken into consideration, it then seems more unlikely that the pest population can be controlled solely by decreasing nitrogen input in complex realistic agricultural environments.
Effect of decreasing nitrogen fertilizer on the densities of parasitoids and parasitism rate
The results showed that the parasitism rate remained unchanged with nitrogen input (Fig. 2), similar to the results of Garratt, who pointed out that fertilizer levels did not affect the parasitism rate in a cereal-aphid-parasitoid system, as the densities of aphids and their parasitoids increased synchronously with the amount of fertilizer18. Similar findings were observed in a walnut aphid-Aphidiinae parasitoid system24. Mixed results were reported in previous studies5,11. The densities of cereal aphids and parasitoids increased when input of nitrogen fertilizer increased from 115 to 170 kg N ha−1, while the parasitism rate increased steadily5.
Parasitoids are subject to pressures derived from higher trophic level. Coincidental intraguild predation is ubiquitous in the form of parasitized aphids suffering from predation. The effect of coincidental intraguild predation on biocontrol and the abundance of parasitoids remains controversial32,33. Importantly, the Aphidiinae parasitoids have the potential to identify the odors of ladybird beetles and reduce searching efficiency by themselves and their offspring, a trait-mediated indirect effect unrelated with the densities of ladybird beetles34. It is possible that the behavior of Aphidiinae parasitoids and the parasitism rate could have been mediated indirectly by ladybird beetles and other predators. Furthermore, the hyperparasitoids also could have relieved biocontrol by Aphidiinae parasitoids35. Hence, the higher trophic level could relieve the effects of nitrogen levels on densities of parasitoids and the parasitism rate.
Effect of decreasing nitrogen fertilizer on the body size of Aphidiinae parasitoids
This research has shown that nitrogen fertilizer application impacted the body sizes of the two Aphidiinae parasitoids (Figs. 3, 4). It has been reported that the body sizes of parasitoids increased monotonically with nitrogen fertilizer under low densities of aphids in the laboratory18,22, meanwhile the dispersion capacity of parasitoid adults, the fecundity of adult females, the emergence rate, the adult longevity of parasitoids, and the parasitism rate increased with the body sizes of parasitoids19,20,22. In contrast to previous reports, this field study found that a moderate decrease in nitrogen application from 280 to 140–210 kg N ha−1 maximized the body sizes of parasitoids. The body sizes of parasitoids depend negatively on the abundance of parasitoids and positively on the hosts diversity19,36,37. Hence, combining the positive effect of the abundance of aphids and of the nitrogen input with the negative effect of parasitoid abundance, it is assumed that an equilibrium should emerge balancing the positive effect of abundance of aphids and the negative effect of abundance of parasitoids. Analogously, It has been reported that an optimized nitrogen level maximized the ratio of predators to prey in a canola-mustard aphid-predatory gall midge system26.
Manipulating nitrogen fertilizer to maximize the fitness of parasitoids plays a crucial role in natural pest control. Increasing the body sizes of parasitoids means greater fertility and dispersal ability of adults20,21, higher fitness of offspring38, and the resulting greater capacity to control the aphid. Thus, decreasing nitrogen fertilizer from the conventional level to more environmentally-friendly magnitudes (140–210 kg N ha−1) could increase the fitness of Aphidiinae parasitoids and boost the biocontrol by parasitoids. Regrettably, this research study did not validate such a viewpoint since the parasitism rate was not maximized under the moderate nitrogen levels. First, there may be hysteresis effects. The parasitoids that were measured for body sizes came from mummies that were sampled in the flowering phases. These parasitoids came into play and mummified cereal aphids after more than ten days. The mummies remained scarce before the flowering phase. Thus, a notable lag occurred and the effect of parasitoid fitness on the parasitism rate could have been unobservable in this study. Second, apart from affecting parasitoid fitness, nitrogen application affected pest fitness. A moderate amount nitrogen maximized the performance of the green peach aphid and the Bertha armyworm23,39. A positive relationship between aphid weight and hind tibia length of parasitoids has been reported18. Combined with the finding in this study that the body sizes of parasitoids were maximized by moderate nitrogen levels, these results imply that the fitness of cereal aphids also benefited from moderate nitrogen levels. However, the densities of cereal aphids in moderate nitrogen levels were similar to those under higher nitrogen levels, suggesting that there could be a compensation between the effect of nitrogen input on fitness of cereal aphids and the effect of nitrogen input on fitness of parasitoids. Currently, long-term agricultural intensification limited biocontrol of parasitoids5. Previous study has reported that the parasitoids were more strongly influenced by agricultural intensification compared to cereal aphids5,13,14. If serious agricultural intensification had mediated, for example decreasing nitrogen fertilizer to an optimized extent, the equilibrium between the impact of moderate decreasing nitrogen fertilizer on parasitoids and the counterpart on cereal aphids would be reshaped. Thus, the positive influence of decreasing nitrogen fertilizer on parasitoids would prevail. Coincidentally, such a magnitude of decreasing nitrogen application would maintain the current wheat yield and lessen the potential environmental risks9.
Relationship between the parasitism rate and the population growth of cereal aphids
From flowering to milking phase, the population of the cereal aphid R. padi that escaped from Aphidiinae parasitoids increased substantially in both 2017 and 2018, while the population of the cereal aphid S. avenae decreased markedly in both 2016 and 2017 (Table 1). Combining the differences between dynamics of the two cereal aphid species with the fact that the Aphidiinae parasitoids rarely parasitize R. padi in China40, it is apparent that the Aphidiinae parasitoids play a pivotal role in suppressing the cereal aphid S. avenae. Furthermore, a higher parasitism rate had a greater suppression effect on the population of the cereal aphid S. avenae, in line with previous research6,14,41.
Year-to-year fluctuation of the cereal aphids-Aphidiinae parasitoids interaction
Obvious fluctuations in the cereal aphids-Aphidiinae parasitoids interaction across years have been documented in this study. Such population fluctuations of aphids and their natural enemies are ubiquitous14,17,42. It has been assumed that a disadvantageous climate accounted for the fluctuations17. The climate changes could not have been manipulated in our study, but they play essential roles in population fluctuations43. Climate warming induced an outbreak of the cereal aphids, but the parasitism rate remained unchanged43,44. Lack of Aphidiinae parasitoids caused higher populations of the cereal aphid S. avenae in a simulated warmed wheat field. However, abundant Aphidiinae parasitoids retained effective suppression of the cereal aphids even when the wheat field was warmed45. The synchronization of parasitoids with pests is vitally important for maintaining biocontrol46, while climate change has the potential to mismatch the pests with parasitoids and cause strong population fluctuations of pests and natural enemies47.
In this study, the parasitism rate was evaluated according to the densities of discernible mummies, a conventional method widely adopted5,6,24. We keep in mind that this method neglects the fact that the symptomless aphids that have been parasitized. Consequently, the parasitism rare was underestimated and the annual fluctuations of abundance of the parasitoids and the parasitism rate were magnified, especially early in the season. Molecular detection, which has the capacity to evaluate whether symptomless aphids have been parasitized and if so by which parasitoid species, presents an exceedingly promising alternative for exploring the aphid-parasitoid interaction11,33. This burgeoning method should be employed to more accurately evaluate the aphids-parasitoids interaction.
Source: Ecology - nature.com
