Figure 1. Typical symptoms of ground pearl infestation on centipedegrass include irregular, thinned, chlorotic patches. Turf may die in the winter or never green up in spring. Photo by JC Chong
We turf entomologists pride ourselves on our ability to develop successful management programs for various insect pests. But in the past 10 years, I have been frustrated and humbled by two pests of warm-season grasses: One is bermudagrass mite, and the other — the focus of this article — is ground pearl. The name “ground pearl” is deceptive and disappointing — ground pearls are not beautiful, and they won’t bring riches or happiness to your life as a golf course superintendent.
Ground pearls: An underground menace
For an entomologist, ground pearls are unique and fascinating insects. As a specialized group of scale insects, ground pearls share two important features with their scale insect cousins: They suck plant sap through a modified, strawlike mouthpart, and they produce a waxy covering on their bodies (described below in the section “Ground pearl life stages”). These two features present significant challenges when it comes to developing a good monitoring and management program for ground pearls.
Ground pearls have a subterranean habit, which makes them difficult to detect. They feed on the roots of grasses and other plants by inserting their strawlike mouthpart into the roots and sucking out cell contents, sap and nutrients. The removal of nutrients from roots gradually weakens the host plants. Unlike fall armyworm, which produces telltale thinning of the turf, ground pearls cause subtle damage that often takes years to show itself.
In the early phase of infestation, when ground pearl density is low, there are no obvious symptoms, and infested turf can often tolerate the infestation. However, as ground pearl density increases, root systems become more severely damaged. Symptoms first appear as irregular, thinned, chlorotic patches (Figure 1, above) that turn brown in summer and die in winter or never green up in spring. The greatest numbers of ground pearls can be found near the boundary between apparently healthy and chlorotic turf (3), and this is where superintendents suspicious of ground pearl infestation should sample.
The symptoms of ground pearl infestation are very similar to those of drought stress and grub or nematode infestation. Many turf managers often do not detect the infestation until it is too late, or they incorrectly identify the problem as drought or nematode damage (and therefore employ the wrong management tools).
A bane of warm-season turf
Ground pearls can attack all warm-season turfgrass species, with centipedegrass being the most severely damaged and slowest to recover. I have seen centipedegrass lawns in Myrtle Beach, S.C., devastated while the neighboring bermudagrass, St. Augustinegrass or mixed-species lawns maintained their apparent health and vigor for a short time despite infestations.
Ground pearl is not restricted to lawns. If golf course superintendents think they do not have to worry about ground pearls because they don’t have centipedegrass roughs, they should think again. Ground pearls can be equally at home feeding on bermudagrass or zoysiagrass. If the infestation is not detected, diagnosed and managed in its early stage, bermudagrass roughs and fairways can be just as devastated as centipedegrass lawns over time.
Although ground pearls can be found worldwide, there are only nine species in the U.S. Two ground pearl species are pests of warm-season turfgrasses, mainly along the sandy plains from North Carolina to Southern California (2). Dimargarodes meridionalis is known to infest the roots of grapevines and grasses in the southeastern U.S., Arizona and California, and Eumargarodes laingi is a pest of grasses in the southern U.S. and of sugarcane in Australia (likely introduced from the U.S.). I have found only E. laingi during sampling of turfgrass in South Carolina. Both D. meridionalis and E. laingi are native to North America and likely have similar biology.
Ground pearl life stages
Figure 2. Cysts are the waxy balls produced by immature ground pearls for protection against the environment and natural enemies. Cysts also inhibit the contact of insecticide solutions with the ground pearls. Photo by Meg Williamson, Clemson University Plant and Pest Diagnostic Clinic
Ground pearls get their name from the layer of wax that the nymphs (that is, immature insects) produce on the outside of their bodies. The layer of wax is deposited as yellowish, shiny, hardened balls (Figure 2, above). These wax balls, sometimes called cysts, are usually 0.06 to 0.13 inch (0.16-0.32 cm) in diameter and are found 2 to 6 inches (5-15 cm) deep in the soil. The cysts protect ground pearls from adverse environmental conditions (too hot, too cold, too wet, too dry, etc.), natural enemies and insecticides. Insecticides are often mixed in water, which cannot penetrate the waxy cysts to kill the nymphs inside. Even granular insecticides require water to dissolve and activate. As a result, ground pearls are invulnerable to insecticide treatment when they are protected inside the cysts.
Ground pearls produce one generation per year and overwinter as nymphs in cysts attached to roots (2). They become adults in late spring to mid-summer. Males are not known to occur in ground pearls that attack turfgrass. Adult females typically emerge from the cysts in late April through August (2). I have found adult females active from April through July in South Carolina, and their emergence time changes from year to year depending on soil moisture and temperature. It is unclear at this point what temperature and what level of soil moisture would trigger consistent emergence of adult females from the cysts.
Adult females have legs and are pink (E. laingi) or orange (D. meridionalis), fat, and glob-like. One of the most striking differences between the cysts and the adults is the absence of waxy covering in adult females. This presents an opportunity for the management of ground pearls.
Figure 3. Adult females produce waxy ovisacs (where they deposit about 100 eggs) from April through August. Ovisacs (red circle on the right) and cysts (blue circle on the left) can be detected in the soil profile. Photo by JC Chong
The front legs of adult females are modified into claws. Adults use these claws to crawl around in the soil and near the soil surface for about a week, after which they secrete a mass of loose, waxy filaments (called an ovisac) in the soil at a depth of 1 to 4 inches (2.5-10 cm) (Figure 3, above). Each female deposits about 100 eggs in the ovisacs over a two-week period (2). Eggs hatch in nine to 15 days, but because adult females emerge and eggs are deposited over a long period of time, egg hatch may continue until the end of August.
Hatchlings and nymphs
The hatchlings (called “crawlers”) disperse from the ovisacs and find, settle and feed on the grass roots. The crawlers secrete their own cysts, and develop through the nymphal stage in the cysts from spring through fall. The nymphs overwinter and then emerge as adults in spring. Under unfavorable environmental and host conditions, nymphs may take more than a year to complete development.
Searching for chemical management solutions for ground pearls
Although it’s true that insecticide solutions cannot penetrate cysts, that does not mean ground pearls are completely invulnerable. Adult females and crawlers are not covered with cysts or wax, which means their bodies can come into direct contact with insecticides, and these stages of the insect can be controlled. Adult females and crawlers should therefore be the main targets for insecticide treatment.
No insecticide is currently registered for ground pearl management on golf turf. Insecticides registered for ground pearl control on home lawns usually contain bifenthrin (for example, Amdro Quick Kill Lawn Insect Killer Granules, Central Gardens and Pets; Bonide Eight Insect Control Flower & Vegetable Above & Below Soil Insect Granules), carbaryl (for example, GardenTech Sevin Insect Killer Lawn Granules), or a combination of chlorantraniliprole and bifenthrin (for example, Roundup for Lawns Bug Destroyer, Scotts Co.). It is necessary to always follow pesticide label instructions and restrictions.
The fact that some products are registered for the management of certain pests does not mean that the active ingredients of those products are indeed effective against those pests. Research is ongoing in the southern U.S. to identify insecticides that may be effective against ground pearls.
My early research
I conducted (but did not publish) a study in 2008 to evaluate the efficacy of several turf insecticides: Arena 50WDG (clothianidin, Nufarm), Meridian 25 WG (thiamethoxam, Syngenta), Merit 2F (imidacloprid, Bayer), Dylox 80 T&O (trichlorfon, Bayer), Malathion 50 EC (malathion, Southern Ag), Orthene TT&O 97 (acephate, AMVAC), Sevin SL (carbaryl, Bayer), and Talstar One (bifenthrin, FMC Corp.). The insecticides were sprayed at the highest label rates, at an application volume of 85 gallons per acre (795 liters/hectare), and mixed with or without Revolution (modified alkylated polyol, Aquatrols) — a wetting agent to reduce water repellency of dry, sandy soil in order to improve penetration of insecticide solution. Untreated plots were also prepared for comparison. The plots (5 feet × 5 feet; 1.5 meters × 1.5 meters) were laid out in a split-plot design with four replicates per treatment.
We applied the insecticides in July 2008 to target adult females and crawlers. We counted the numbers of live adult females and cysts in soil collected with a cup-cutter to a depth of about 4 inches (about 50 cubic inches or 820 cubic cm) at three months and nine months after the application. If our hypotheses — insecticides could reduce ground pearl abundance, and wetting agents could improve control efficacy — were correct, we would see fewer ground pearls in insecticide-treated plots, especially those mixed with Revolution.
Alas! Our hypotheses were refuted. No insecticide (with or without Revolution) was effective in reducing the numbers of live ground pearl cysts when compared with the untreated check at three months after treatment (October 2008) (Figure 4). At nine months after treatment (April 2009), however, plots treated with Arena without Revolution and Meridian with Revolution had fewer live ground pearl cysts than the untreated plots (Figure 5). Ten years after the experiment, I still cannot explain why Arena was more effective without Revolution and Meridian was more effective with Revolution.
The data from the 2008 study were too inconsistent for me to generate a conclusion and recommend Arena or Meridian as a management tool for ground pearls. Based on the average of live cysts at nine months after treatment in plots treated with Sevin SL (the highest average in this study), the plots were infested with as many as 912 individuals per 50 cubic inches, or more than 31,500 individuals per cubic foot!
The study did, however, produce one consistent observation. Plots treated with Sevin SL, and to a lesser extent, Malathion, Orthene and Talstar (both with or without Revolution), had more live ground pearls than the untreated check. I think these broad-spectrum insecticides had killed off natural enemies or interrupted their activities. The natural enemies of ground pearls are unknown, but it is likely that ants and other soil-dwelling arthropods might have helped in reducing the numbers of adult females and crawlers (1). If the natural enemies of ground pearl are removed from the environment, ground pearls have no check on their population growth.
Among the insecticides evaluated in this study, neonicotinoids (Arena, Meridian and Merit) hold the most promise. Neonicotinoids (except for Arena with Revolution), along with Dylox, slightly reduced the numbers of live ground pearl cysts at nine months after treatment. Studies and observations by Rick Brandenburg, Ph.D., North Carolina State University, and Kai Umeda, University of Arizona Cooperative Extension, also support the potential of neonicotinoids (1; Brandenburg and Umeda, personal communication).
Overall, however, neonicotinoids did not result in significantly lower numbers of live ground pearl cysts in this study (Figures 4, 5). I think one application is insufficient to cover the entire activity period of adult females and crawlers. Although an individual adult female lives for less than a month, adult females in a population emerge at different times, so reproduction of the entire population occurs over a very long period. Even if the application applied in July had killed 85% of the adult females and crawlers present at the time of application, that one application would not have killed adult females that had laid eggs and nymphs that had formed cysts before July, or the adult females and crawlers that emerged after July. Therefore, the most effective approach may be to initiate treatment with neonicotinoids as soon as adult females have emerged from cysts, and to repeat the application until all crawlers have hatched.
Problems with neonicotinoid use
Repeated use of neonicotinoids has several drawbacks. The first and most obvious shortcoming is that repeated applications can be extremely time-consuming and costly. The second problem is that no experimental data support the efficacy of this approach, and resources are not available to support a study that could gather such data. It is likely that the same management approach would have to be repeated over several years to result in an improvement in turf health and appearance.
A more technical issue with the approach is our general lack of knowledge about ground pearl biology and ecology. Adult emergence time changes from year to year, and there is no method of predicting when emergence will occur each year. Without that predictive ability, turf managers may have to initiate application from April through August. Again, this would be very time-consuming and expensive.
Another consideration is safety to natural enemies and pollinators. Several studies have demonstrated that neonicotinoids, although generally not as detrimental to natural enemies as organophosphates and pyrethroids, are still harmful to natural enemies and pollinators. There is no conclusive information on whether insecticides with better safety profiles for natural enemies and pollinators, such as the diamides Acelepryn (chlorantraniliprole, Syngenta) and Ference (cyantraniliprole, Syngenta), have any potential in managing ground pearls.
Other systemic insecticides?
Turf managers often ask about using systemic insecticides for ground pearl control. The idea is that systemic insecticides will be absorbed into plant tissues and will then be translocated to the roots. The ground pearls will feed on the roots, suck in the insecticide, and die.
Neonicotinoids and diamides are systemic insecticides. It is important to understand that these systemic insecticides are not fully systemic, meaning that most of the active ingredients are concentrated in the leaf tissues — very few, if any, are translocated to the roots where the ground pearls are feeding. Our results on the efficacy of neonicotinoids in this study confirmed that neonicotinoids are not the stealth bombers we have been looking for. Currently, no fully systemic insecticide is available to the turf industry.
So, no insecticide is labeled for ground pearl control in golf turf, and no insecticide is known to be effective against ground pearls. What else can you do?
Improving water penetration
As I observed in my study, improving water penetration helped improve the health of an infested lawn. Increased fertilization and irrigation can result in temporary improvement in turf appearance, but this is only masking the damage. Without an effective method of reducing the ground pearl population, it is only a matter of time before the damage reappears or is magnified.
Replacing susceptible grasses
An obvious option is to replace a susceptible grass like centipedegrass with another species. No warm-season turfgrass species is immune to ground pearls. Bahiagrass seems to tolerate infestation better than other species, but I am doubtful that anyone would willingly replace a centipedegrass lawn or rough with bahiagrass. Bermudagrass and zoysiagrass are the obvious alternatives. Cultivars that grow vigorously with supplemental fertilization and irrigation, such as Celebration, may develop symptoms later than other cultivars. Decline of the bermudagrass lawn or rough is inevitable, however, especially if grown on sandy soil.
Damaged turf area can also be replaced with ornamental landscapes. This is the only viable option for severely damaged lawns. With some careful and clever redesign, golf course roughs can also be converted to plantings of ornamental plants or pollinator habitat.
Persistence of infestation
One of the most frustrating aspects of ground pearl management is the persistence of the infestation. Damaged turfgrass can be killed with herbicides, but that does not remove the ground pearls. Ground pearls can survive in the cyst stage for a long time (1). Ground pearls have been known to survive for 15 years in the absence of a suitable host.
I have seen multiple incidences in which infested grass was removed and sod was placed on the bare dirt that remained. The new sod was either immediately infested with adult females, or it became infested with cysts within a year (1). Another turf manager removed the top 2 inches (5 cm) of soil, replaced it with clean topsoil and resodded, only to have the new sod infested with cysts within a year of renovation. We dug into the soil and found live cysts from the root zone to a hardpan 12 inches (30.5 cm) below the soil surface. Ground pearls living deep in the soil had become the source of infestation in the new sod.
Research continues on understanding ground pearl biology and developing an effective management program for the pest. A successful management approach will likely integrate tolerant grass cultivars, cultural practices (such as irrigation and fertilization), insecticides, surfactant, knowledge and persistence.
You know what else is a good way to deal with ground pearls? Grow rocks. No one has followed this recommendation yet.
The research says ...
- Ground pearl, a type of scale insect, is an especially persistent pest in warm-season turfgrasses on lawns and golf courses.
- Ground pearls can live deep in the soil and use a strawlike mouthpart to suck sap and nutrients from the roots of grasses, gradually damaging the root system and producing thin, chlorotic patches in the turf.
- Nymphs take a year to mature and produce a waxy coating that protects them from pesticides. There is potential for control of adult females and crawlers, but after an area has become infested, it is extremely difficult to manage the problem.
- Replacing severely infested turf with ornamental plantings or pollinator habitat is sometimes the only option.
- Brandenburg, R. 2003. Don’t give up on ground pearls. Grounds Maintenance. (http://www.grounds-mag.com/mag/grounds_maintenance_dont_give_ground_2).
- Hertl, P.T. 2012. Ground pearls. Pages 46-48. In: R.L. Brandenburg and C.P. Freeman, eds. Handbook of Turfgrass Insects, Second Edition. The Entomological Society of America, Lanham, Md.
- Potter, D.A. 1998. Destructive Turfgrass Insects: Biology, Diagnosis, and Control. Ann Arbor Press, Ann Arbor, Mich.
Juang Horng “JC” Chong is an associate professor of turf and ornamentals entomology, Clemson University, Clemson, S.C.