Oracella acuta
(loblolly pine mealybug)

This species has had limited distribution from its native habitats in the southern region of the USA since its discovery and description (Lobdell, 1930). O. acuta appears to be restricted to feeding on species of pines and loblolly pine, Pinus taeda, is its preferred food source. In its native habitat, populations seldom reach pest status due to the presence of natural enemies. In 1988, it was transported to a pine seed orchard in China on slash pine, Pinuselliottii, scions purchased in the USA. Sun et al. (1996) noted that O. acuta-infested slash pine scions leaving the USA and entering China in 1988 were not subjected to the quarantine restrictions of either country. The loblolly pine mealybug quickly became established and rapidly spread throughout pine plantations in the Guangdong Province, China where it threatens both native and introduced species of pines in the region.

The mealybug, O. acuta, was originally discovered infesting pine needles collected in Mississippi, USA (Lobdell, 1930). This mealybug is found on various pine species throughout the southern USA (Johnson and Lyon, 1976). It is speculated that this species is native to the Mississippi basin and over time has spread eastward and westward feeding on various species of pines. Since its discovery, O. acuta has been recorded in fourteen southern states (Miller, 2005; Ben-Dov, 2010a). The project to introduce genetic material into China to enhance their pine forests resulted in the introduction of the loblolly pine mealybug from the purchase and importation of O. acuta-infested scions of slash pine (Pinus elliottii) from a company in Baldwin, Georgia, USA, in 1988 (DeBarr, 1992; Sun et al., 1996; FAO, 2001). The infested plant material was not detected during its route from Georgia to the Hongling Seed Orchard in Taishan City, Guangdong Province, China (Pan et al., 1995; Sun et al., 1996). The presence of O. acuta is not easily detected as the first instar nymphs tend to settle beneath the fascicles or at the base of the needles. As such, the 70 infested scions were grafted onto P. elliottii in the pine orchard (Sun et al., 1996). In 1989, Sun et al. (1996) reported that some 2,460 scions were obtained from the newly-infested trees and grafted onto trees in uninfested areas of the seed orchard. The mealybug was initially thought to be that of the native species, Pseudococcus pini. However, specimens of the mealybug were eventually sent to D. R. Miller in 1991 who identified the specimens as O. acuta. The most severe damage currently occurs on slash pine in China, but there is concern that this invasive pest could spread north and cause significant damage in plantations of its preferred host, loblolly pine [Pinus taeda] (Sun et al., 1996).

The risk of introduction of O. acuta from country to country is low as long as inspections are made of pine material that is to be shipped internationally. However, the risk of spread of established populations of O. acuta locally into uninfested pine forest is moderate to high as the specimens are easily transferred to new hosts by the wind, as well as carried on the bodies of animals.

This species is recorded only from species of Pinus and appears to be restricted to regions in the eastern and southern USA, and the southern region of China.The tips of the new-growth needles appear to be the preferred feeding site for this species.However, mealybugs will also settle and feed on other areas including at the old growth internode or between the needles near the top of the fascicle (Clarke et al., 1990a). Specimens of O. acuta tend to settle throughout the tree canopy with no significant differences in the population density for a preferred location in the four cardinal directions on the trees (Li et al., 1994). However, a higher population density more often occurs in the lower strata of the host trees. This mealybug is capable of surviving temperatures from -1 to 32ºC; thus, potentially posing a threat to pines in more northern regions (Sun et al., 1996). Currently, populations of the loblolly pine mealybug are located at latitudes south of the range of the mealybug in the USA (Sun et al., 1996). Population decreases that have been observed during the summers have been attributed to the impact of high temperatures (Tang et al., 2000; 2001). Stages of this species are found either under the bark or in a ‘resinous cell’ produced by the female. This protective waxy covering allows the mealybug to maintain a favourable humidity level, prevents rapid temperature changes, functions as a protective barrier against topically applied chemicals, and provides some protection against natural enemies.

The loblolly pine mealybug is reported to be capable of infesting eight species of pines (Pinuscaribaea,Pinusechinata, Pinuselliottii, Pinusmassoniana, Pinuspalustris, Pinustaeda, Pinusthunbergiana, and Pinusvirginiana), and potentially can survive on these pine species throughout their range (Sun et al., 1996; Xie et al., 2001).

Seasonal development of the loblolly pine mealybug and potentially the impact of beneficial control agents differ slightly throughout its range with the mealybug having three or four complete generations annually in warmer climates and two or three in more northern climates. Also, their preferred feeding site at the new growth needles results in growth damage, needle damage and needle drop, and stem die-back. The survival of crawlers is dependent upon their behavioural pattern of searching for an acceptable place to settle and feed, as well as upon the environmental conditions at the time of their emergence. In the USA, the spring generation of O.acuta feeds on the new growth and cones, whereas in China they infest both the new and old needles (Ciesla, 1995).

Reproductive Biology

O. acuta is a bisexual mealybug capable of four or five generations annually, especially in more southern climates (Clarke et al., 1990a; Sun et al., 2004a). Kosztarab (1996) reported that the mealybug had two or three generations annually in Virginia, USA. Development of the O. acuta female consists of egg, first (crawler), second, third and adult stages. However, the males undergo egg, first, second, prepupa, pupa and adult stages. Females are always wingless. Apterous males are present during the winter and spring months, whereas alate males occur throughout the remainder of the year in the southern USA. In late-March, first generation females begin secreting their white resinous covering between the needles, including those with swollen bases from feeding by other insects, in which to lay their eggs in mid-April (Clarke et al., 1990a). In Georgia, USA first generation adult females were reported to be capable of producing approximately 182 pink eggs in a chain-like arrangement within the resin cells, whereas the second generation females produced approximately 113 eggs (Clarke et al., 1990a; Sun et al., 1996). The fecundity and number of eggs laid per female, as well as the mortality of the adults, have been determined to be effected by temperature (Tang et al., 1996; 2000; 2001). The eggs hatch within 8-10 days with an egg-hatch rate of about 90% (Sun et al., 1996). In Virginia, Kosztarab (1996) reported that females laid their eggs either under the bark or on twigs in the resinous cells. Crawlers from eggs that hatch in the autumn tend to settle in the needle sheaths where they remain through the second or occasionally the third stage before moving under the bark where they mature. The period of development from crawler to adult stage was reported to be effected by the weather and temperature (Tang et al., 2000; 2001). Crawlers leave the cell and tend to settle most often at the shoot tip of the new growth, whereas females settle on both the new growth and at the old growth internodes (Clarke et al., 1990a). This species is reported to overwinter as crawlers between the needles in the fascicles or under the old resin cells of the females by the previous generation (Clarke et al., 1990a; Sun et al., 1996).

Nutrition

Environmental Requirements

These mealybugs are located under the bark, in resin cells, in the needle sheaths or on the tips of needles. O. acuta overwinters as crawlers in the fascicles between the needles and under previously-used resin cells (Clarke et al., 1990a). The number of generations annually may be affected by temperature (Tang et al., 1996; 2000; 2001).

The loblolly mealybug, O. acuta, is a native species of pines in the southern USA that seldom obtains pest status due to the effectiveness of parasitoids and predators that maintain populations at low levels (Clarke et al., 1990a,b; 1992; Negron and Clarke, 1995; Sun et al., 1996; Sun et al., 2004a,b). This mealybug was accidentally introduced into pine plantations in Guangdong Province, China in 1988 (Sun et al., 1996) on pine scions purchased in the USA. Upon the establishment and severe damage to pine forests by the invasive loblolly pine mealybug in 1990, surveys were initiated to find potential biological control agents from which 21 natural enemies were recorded by Pan et al. (2002) and Xu et al. (2007). However, these proved to be ineffective (Yang, 1991; Pan et al, 1994; Pang and Tang, 1994a; Zhou et al., 1994) in suppressing the pest populations. Initial efforts to control the loblolly pine mealybug were implemented by Chinese forest entomologists, and later (1992) the programme was funded by the Forestry Department of Guangdong Province and the Ministry of Forestry (Sun et al., 1996). Cooperative assistance between China and the USA agencies and personnel provided the basis for identification of O. acuta and information on its development and natural enemies. As a result of the continual increase in the pest populations (Tang, 1994), a 10-year Sino-USA cooperative project was initiated in 1995 (DeBarr et al., 1998; Clarke, 2007) to survey native habitats in the USA for potential biological control agents (Sun et al., 1996). This cooperative international programme to biologically control O. acuta in China was conducted from 1995-2004 (Clarke, 2007). The objective of the programme was to collect parasitized females from its native range in the southeastern USA and ship them to China. The parasitoids would be mass-reared and released into O. acuta-infested forests in China.

A variety of natural enemies have been observed to be associated with the loblolly mealybug in its natural habitats in the southern USA (Clarke et al., 1990a). An encyrtid (Acerophagus coccois), a platygastrid (Allotropa spp.), and a signiphorid (Chartocerus sp.), were the most abundant parasitoids observed attacking the mealybug in Georgia, USA (Clarke et al., 1990a,b). The polyphagous parasitoid, A. coccois is known to parasitize species in several genera of Pseudococcidae (Clarke et al., 1990a; Bertschy et al., 1997), including O. acuta (Dorn et al., 2001). Parasitism was reported to increase from May to September at one site in 1982, and exceeded 50% at one site and 90% at another site in 1984 (Clarke et al., 1990a,b). A new primary parasitoid species, Zarhopalus debarri,of the loblolly pine mealybug was discovered and described (Sun et al., 1998). All known members of this genus are parasitoids of mealybugs.

The loblolly pine mealybug is the only known pseudococcid on pine that produces a white, resinous cell. Monitoring potential host trees for the presence of dead or dying needles or for the presence of sooty mould may provide the opportunity to control the invasive pest prior to a massive population build-up.

Species identification requires observing the morphology of the slide-mounted adult females.

Conduct observations on the stems and needles of the new and last year’s growth for the resinous cells. These cells are usually located on the stems at the base of the needles and may contain a distinctive pink female with a protruding abdomen. Survey the needles and branches for the presence of sooty mould resulting from feeding loblolly pine mealybugs.

The loblolly pine mealybug can be detected by monitoring the needles, especially in the sheaths, for the presence of a whitish, resinous covered mealybug. The adult female is usually found enclosed within a whitish resinous cell (2-3 mm long) that is open at one end, from which the pygidium protrudes (Lobdell, 1930). The elimination of honeydew results in the development of sooty mould growth on the lower needles and stems, reducing photosynthesis and causing significant die-back of the infested foliage. Inspection of mealybug-infested plant material, as well as the use of yellow sticky traps, were found effective in attracting the two parasitoids, Allotropa sp. and Zarhopalus debarri (Sun and Zhang, 2003), and O. acuta males (Sun et al., 2002).

Upon examination of this unique species, Ferris (1950) erected a new genus, Oracella, for this mealybug. Lobdell (1930) noted the presence of a series of large multilocular pores on the dorsal and ventral margins of the posterior abdominal segments, distinguishing this species from other known pseudococcids. The presence of four to seven pairs of inconspicuous cerarii and the lack of an anal ring bar also aid in separating this species from other mealybugs. The production of ‘resin cells’ by O. acuta distinguishes this species from all known pine-infesting pseudococcids.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Implementation of programmes to survey potential hosts for the invasive loblolly pine mealybug, administering control tactics in mealybug-infested areas, and maintaining quarantines to prohibit transporting the species into uninfested regions can be effective in suppressing the pest populations.

Prevention

The implementation of surveys in pine forests in an effort to discover infestations early enough to control the population before it has the opportunity to increase in size is required. Maintaining quarantines can limit the spread of the invasive pest from region to region. This mealybug has been placed on China’s National Quarantine List since 1996.

Public Awareness

Education of the public through literature, presentations, and workshops can enhance the awareness of managers, property owners and government officials. The use of field surveys to teach individuals the damage symptoms on the host and the morphology of the loblolly pine mealybug may be used to more quickly implement control tactics.

Eradication

Upon the discovery of this invasive species in 1990, an immediate attempt was made to identify the species and implement control procedures to eradicate the loblolly pine mealybug (Sun et al., 1996). Insecticides that had been effectively used against two other similar exotic pests were selected for use against the infestation at Hongling Seed Orchard, in Guangdong Province, China. After the various application methods (foliar sprays, trunk injections, aerosols, etc.) proved ineffective, the infested branches and limbs were cut off and burned. Eventually, whole trees that were infested were cut down and burned (Sun et al., 1996). By 1992, other insecticides were evaluated (Pan et al., 1994) as well as two bioinsecticides as a possible control agent for O. acuta (Sun et al., 1996). Monitoring hosts and early detection provide the opportunity to suppress pest populations of O. acuta (Zhang et al., 2009).

Control

Physical/mechanical control

New infestations, small in size or limited to a few branches, can be eliminated by pruning the infested limbs and burning.

Movement control

Periodic surveys of uninfested pine plantations need to be conducted to discover new infestations due to wind and animal dispersal of O. acuta. Local observations of individual trees may prevent pest population build-up resulting in massive outbreaks in a given area. Quarantine restrictions for the movement of infested material into non-infested regions may slow the spread of the invasive species. Due to the increase in world trade, there is a need to develop a more effective inspection methodology to prevent the introduction of exotic plant pests in or on logs, processed and unprocessed lumber, manufactured and unmanufactured wood articles, and genetic material for enhancing native plant species.Ciesla (1995) proposed inspections of incoming logs, wood products and plant material including crates and pallets to reduce the chance of new invasions by the invasive species. However, because this mealybug settles on and feeds on the twigs and needles on the tree, observations focused on these materials would be most effective.

Biological control

The transfer of O. acuta from the USA to hosts in China; thus, leaving behind those natural enemies that maintained the population at low levels allowed for its establishment and rapid population growth in the new region. Upon the discovery of the invasive O. acuta and its damage to slash pine [Pinus elliottii] stands in the Guangdong Province, a two-year search to find potential native natural enemies in the infested pine stands was employed. From field evaluations, it was concluded that in the absence of natural enemies, populations of O. acuta increased 1.26 times per generation (Tang et al., 1996). In studies to assess potential natural enemies of the loblolly pine mealybug in China, the predaceous Cryptolaemus montrouzieri was determined to have some potential in regulating the pest populations (Tang, 1994; Tang et al., 1995a; Pan et al., 2002). One discovered parasitoid, Allotropa sp., was found to be ineffective against the loblolly pine mealybug. Cooperative efforts between the USA and China were initiated to evaluate the natural enemies of O. acuta as potential biological control agents to import into China to suppress infestations of the pest. Nine parasitoid species have been found to be associated with O. acuta (Clarke et al., 1990a; Sun et al., 1998, 2004a,b; Masner et al., 2004). Of these, two species,Allotropa oracellae and Zarhopalus debarri, are consider primary parasitoids for use against the loblolly pine mealybug.

Chemical control

Several studies have demonstrated that effective insecticides are available to suppress population levels of O. acuta on pine hosts (Clarke et al., 1992; Sun and Zhang, 2003). However, Clarke et al. (1992) concluded from evaluations of four pyrethroids that insecticide use often resulted in endemic populations reaching outbreak levels in Georgia and Oklahoma pine seed orchards. They concluded the use of these insecticides resulted in a lower parasitoid population on treated branches although they were not significantly lower than numbers on untreated branches (Clarke et al., 1988; 1992). Chemical applications that do not completely cover the tree often result in a resurgence of the mealybug as the insecticides have been documented to be detrimental to populations of biological control agents resulting in an explosion in the pest population. The general concept that insecticide use has a detrimental impact on natural enemies of the loblolly pine mealybug is widely supported (Clarke et al., 1988; 1990a,b; 1992; Sun et al., 1996; Sun and Zhang, 2003). They proposed that consideration be given to appropriate timing of insecticide applications to lessen the impact on parasitoids. As a result, newly discovered, local populations of O. acuta may be controlled with repeated spot applications of insecticides. To suppress population numbers of the invasive pest, insecticides or insecticidal soaps may be used on infested trees accessible to equipment required for application.

IPM

Due to the discovery of natural enemies for O. acuta in its native habitats, classical biological control tactics may well be successfully implemented to suppress populations of this exotic pest in China. The rearing and mass releases of parasitoids are currently used as part of an integrated pest management programme against the loblolly pine mealybug in pine forests. Several IPM programmes at the state and provincial levels have been initiated against the loblolly pine mealybug (Diansheng, 2003). The combined use of biological control agents, selective insecticides appropriately timed to have a minimal impact on natural enemies, mechanical pruning and destruction of infested material, and quarantine of infested material, holds the potential of maintaining this invasive pest below economic threshold levels.

Monitoring and Surveillance

The use of yellow-sticky traps may be used to determine not only the population density of the invasive pest, but assess the effectiveness of the parasitoids of O. acuta (Sun et al., 2002).

Additional studies need to be conducted on the immature and adult male stages of this species. Thus, more precise morphological and developmental studies are needed on O. acuta. Also, behaviour studies on the species may play a significant role in the eventual control of this invasive mealybug. Further investigations on the natural enemy complex that will lead to the suppression of the pest populations are needed to protect the affected ecosystems.

31/12/09 Original text by:

Paris Lambdin, Department of Entomology, Agricultural Experimental Station, University of Tennessee, PO Box 1071, Knoxville, TN 37901, USA