Ant-mealybug mutualism modulates the performance of co-occurring herbivores

Abstract

Mutualism between ants and honeydew producing hemipterans has been extensively studied. However, little is known on how ant-hemipteran mutualism impacts the co-occurring herbivores, which in turn affect the mutual relationship in ecosystems. Herein, we investigated the effect of ant-mealybug mutualism on the oviposition preference and spatial distribution of cotton leaf roller Sylepta derogata, a polyphagous herbivore, and in Apantetes derogatae performance, a larvae parasitoid of S. derogata. Leaf rollers constructed shelters for mealybugs to prevent them from enemy attack and preferred to lay eggs on plants with ant-mealybug mutualism. Egg abundance on mutualism-present plants was higher than on mutualism-absent plants. Leaf roller parasitoid A. derogatae showed higher parasitism on mutualism-absent plants. No obvious change in leaf roller egg abundance was observed when A. derogatae was excluded, suggesting that the parasitic pressure can also regulate the oviposition behavior of S. derogate. Apantetes derogatae showed higher aggressiveness in parasitizing leaf roller larvae at the absence of the mutualism. There was a definite correlation between leaf roller egg abundance and the number of patrolling ants on plants. Without ant-mealybug mutualism, S. derogata eggs showed a significantly aggregated distribution pattern, but a uniform distribution pattern was observed when the mutualism was present. Ant workers showed a consistently uniform distribution on plants. The results reveal a novel mediation effect of ant-mealybug association on the composition and structure of food webs in cotton field, which may contribute to a better understanding of the cascading effects of ant-hemipteran mutualism on other niche-related species in ecosystem.

Figure 1

Effects of ant-mealybug mutualism on cotton leaf roller prevalence in field investigation. (A) Leaf roller infection percentage per plant; (B) leaf roller egg abundance per plant. Boxes extends from the 25^th to 75^th percentiles, with the band indicating median; whiskers represent the 5^th and 95^th percentiles; dots outside the whiskers are outliers. Boxes sharing the same letters indicate no significant differences among treatments (P > 0.05). The number of leaf roller eggs was log₁₀ transformed.

Figure 2

Effects of ant-mealybug mutualism on cotton leaf roller prevalence in greenhouse investigation. The data are presented as the mean ± SD. (A) leaf roller egg abundance per plant; (B) leaf roller larvae parasitism per plant; (C) leaf roller egg abundance without interference by Apantetes derogatae. Asterisk (*) and (**) on bars indicate significant differences between treatments (P < 0.05 and P < 0.01, respectively).

Figure 3

Effects of ant-mealybug mutualism on Apantetes derogatae aggressiveness. The data are presented as the mean ± SD. (A) Aggressiveness index; (B) percentage aggressiveness level. Boxes extends from the 25^th to 75^th percentiles, with the band indicating median; whiskers represent the 5th and 95th percentiles; Asterisk (*) and (**) on bars indicates significant differences between treatments (P < 0.05 and P < 0.01, respectively).

Figure 4

Effects of ant-mealybug mutualism on abundance of patrolling ants and leaf roller eggs on plants. (A) number of patrolling ants; (B) number of leaf roller eggs. Boxes extends from the 25^th to 75^th percentiles, with the band indicating median; whiskers represent the 5th and 95th percentiles; dots outside the whiskers are outliers. Asterisk (**) on boxes indicates significant differences between ant-mealybug mutualism presence and absence (P < 0.01).

Figure 5

Effects of ant-mealybug mutualism on correlation between abundance of leaf roller eggs and patrolling ants. Red circle: mutualism presence; orange circle: mutualism absence.

Figure 6

Effects of ant-mealybug mutualism on spatial distribution pattern of leaf roller egg. (A) Sep.7; (B) Sep.22; (C) Oct.9; (D) superimposed data set from Sep.7 to Oct.9. Red circle: mutualism presence; orange circle: mutualism absence.

Figure 7

Spatial distribution pattern of ant workers on plants. Red circle: Sep.7; orange circle: Sep.22; blue circle: Oct.9.

Figure 8

Correlation between abundance of leaf roller eggs and patrolling ants on plants. (A) Sep.7; (B) Sep.22; (C) Oct.9.