Ecological effects of multi-species, ant-hempiteran mutualisms in citrus

Background/Question/Methods

Protection mutualisms between ants and honeydew-producing insects can influence the structure of arthropod food webs by altering the behavior, activity and local abundance of ants on plants. To examine the broader ecological consequences of such mutualisms, we conducted a two-year removal experiment in organic lemons in San Diego County, CA. Interactions between ants and multiple species of honeydew-producing hemipterans are ubiquitous in citrus, and the arthropod food web of this agro-ecosystem is well characterized. Experimental groups (n = 10 trees for each category) consisted of ant-removal trees, honeydew-producing hemipteran-removal trees, and un-manipulated control trees. In addition to monitoring the abundance of the Argentine ant and five species of honeydew-producing hemipterans, we estimated the abundance and parasitism of California red scale, which is an important insect pest in citrus that produces no honeydew but that nonetheless benefits from the presence of ants because they interfere with red scale’s primary biological control agent (parasitoid Aphytis wasps). Here we test the hypotheses that mutualisms between ants and honeydew-producing insects are sufficient to disrupt biological control of red scale and that the degree to which such interference takes place increases when more than one species of honeydew-producing hemipteran is present.

Results/Conclusions

Canopy abundance of honeydew-producing hemipterans differed in the two years of the study (2009 and 2010), but of the hemipteran species observed citrus mealybug and brown soft scale were consistently the most abundant. As expected, whole-tree removals of targeted insect groups revealed strong and reciprocally positive interactions between ants and honeydew-producing hemipterans. Removal of honeydew-producing hemipterans, for example, reduced per tree ant recruitment by 64%, and regression analyses revealed strong positive relationships between per tree ant recruitment and the abundance of citrus mealybug in particular. Mutualism between ants and honeydew-producing hemipterans indirectly and positively affected red scale: red scale parasitism decreased and red scale density increased with increasing abundance of honeydew-producing hemipterans. Positive effects of honeydew-producing hemipterans on red scale were strongest when all species of honeydew-producing hemipterans were considered together. Although we do not yet know the mechanism underlying this latter result, it seems plausible that guilds of honeydew-producing hemipterans might provide ants with honeydew more consistently or over a longer period during the season compared to that produced by any single species of hemipteran. These results argue for a greater appreciation of how mutualist diversity affects the ecological consequences of mutualisms.