The Pest Partnerships that Threaten Citrus

Biocontrol of Asian citrus psyllids can be improved by controlling ants.

By Kelsey Schall and Mark Hoddle

More than a decade of battle with the Asian citrus psyllid (ACP)-huanglongbing (HLB) complex has drained the vigor from Florida’s citrus industry, costing billions in disease management and production losses. With HLB established in parts of urban Southern California, the second largest citrus producer of the United States anxiously faces the same threat.

Figure 1. Protective Argentine ants capture Tamarixia parasitoids while tending their Asian citrus psyllid colony for honeydew (left). A close-up of a Tamarixia parasitoid (right).

Though coordinated insecticide sprays have been a successful tactic for ACP-HLB management in commercial groves, the cost of a sustained chemical program in urban Southern California is prohibitive. The result is millions of untreated backyard citrus trees susceptible to buildup of large populations of HLB-infected ACP. Spillover from these hotspots may accelerate disease spread throughout urban areas and into commercial groves, despite the best efforts of growers maintaining rigorous ACP-HLB programs.

In response to this troubling dilemma, California is developing a sustainable, long-term control program for ACP. Central to the program is a natural enemy complex that includes the ACP parasitoid, Tamarixia radiata, and generalist predators. Combined, these biological control (biocontrol) agents can significantly reduce ACP populations, which can help slow HLB spread.

Though more than 3.5 million Tamarixia have been released in the state, monitoring indicates ACP parasitism is negatively impacted by several factors. Particularly problematic are the interactions among ACP, natural enemies and well-known biocontrol disruptors — ants. Ants tend sap-feeding pests, “milking” them for a sugary honeydew reward, and protecting them from natural enemies in the process (see Figure 1). This stifling of biocontrol facilitates pest outbreaks that lead to greater plant damage, disease transmission and yield loss.

ANTS AND ACP: A DEADLY DUO

Though ant-sap-feeding pest partnerships are well documented for many systems, little is known about the consequences of ant-ACP interactions. Studies completed in Florida indicate that ACP tending by the big-headed ant, rover ant and red imported fire ant drastically reduces ACP biocontrol. A similar trend is likely for ACP in Southern California, where more than half of ACP colonies are tended by the invasive Argentine ant (AA).

FIELD TRIALS
To determine if AAs disrupt ACP biocontrol, ant control treatments were applied to ACP- and AA-infested navel orange trees at five residential and research groves. Trials were run in August 2013, August 2014 and September 2014. On experimental trees, flush infested with ACP were identified and colony sizes recorded. AA activity was assessed by two-minute counts of workers ascending the trunk.

Following these baseline measurements, ant control treatments were applied. In all trials, half of ACP-infested flush received an ant-excluding sticky barrier. Additionally, in trial 3, half of the trees were treated with thiamethoxam-based liquid poison bait containing an attractive AA trail pheromone. AA workers consume and store this sweet, slow-acting bait in a communal stomach, sharing it with queens and developing ants before it takes effect. Thus, sustained insecticide transfer kills the entire colony.

Figure 2. Tamarixia parasitoids are released onto flush infested with Asian citrus psyllids.

Three days after treatments were applied, 200 (trials 1 and 2) or 400 (trial 3) Tamarixia were released per tree (see Figure 2). Some of the Tamarixia released were monitored and their interactions with AA and ACP recorded. Two weeks after parasitoid release, all ACP-infested flush were collected, transported to the lab and examined for parasitism and predators.

RESULTS
Across all three trials, more than 800 ACP-infested flush were collected from 86 trees. Our results confirmed our suspicions: AA control drastically improved ACP biocontrol by Tamarixia. Overall, ACP parasitism was 70 to 800 percent higher when ant control was applied (see Figure 3). In the absence of ants, average parasitism of ACP on sampled trees peaked at 64 percent, but was only 31 percent when tending ants were present.

ACP predators were also spotted more frequently (1.5 to 3 times more) on flush that received an ant control treatment (see Figure 3). The most common predators found were green lacewing larvae. Other notable players included hover fly larvae, and to a lesser extent, lady beetles, the dominant ACP predator guild in Florida.

Antagonistic interactions between Tamarixia and AA during ACP tending may explain the disparity in parasitism between treatments. Tamarixia deposited eggs on ACP half as often in colonies tended by ants than those where ants were excluded. Furthermore, 95 percent of Tamarxia released on these ant-tended colonies were attacked, killed or chased off during the two-minute observational period. Our observations indicate that AAs disrupt natural enemies, thereby suppressing biocontrol.

CONCLUSIONS
We have demonstrated that AAs interfere with natural enemies of ACP in California similarly as other ant species do in Florida. Drastically improved parasitism and predator activity can be achieved by minimizing detrimental ant-ACP interactions. In addition to improving ACP biocontrol, AA control may improve biocontrol of other common ant-tended pests of citrus such as aphids, mealybugs and soft scales. Ongoing projects aim to quantify the long-term impact of AA control on biocontrol by predators and parasitoids of several major sap-feeding pests.

Kelsey Schall is a Ph.D. candidate in the Hoddle lab in the Department of Entomology, University of California, Riverside. Mark Hoddle is an Extension specialist in biological control and the director of the Center for Invasive Species Research in the Department of Entomology, University of California, Riverside.

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