Concern arose about the Asian form of gypsy moth (Lymantria dispar) following increased trade from Russian far east ports, particularly the increased connection between these ports and the Pacific coast of North America (Gninenko and Gninenko, 2002). Asian forms of gypsy moth were found in North America (Oregon and Washington, USA and British Colombia, Canada) in 1991. This incursion is considered to have been associated with ships arriving from far eastern Russia (USDA 1995). In 1990 and 1991, gypsy moth numbers were very high around the ports of Vladivostok, Nakhodka and Vostochny and ships from these ports were found to be heavily contaminated with egg masses (Walsh, 1993). While incursions of Asian gypsy moth in North America have been eradicated, concern about reintroduction remains.
Largely in response to this situation, New Zealand has had a surveillance trapping programme for gypsy moth since 1993 (Ross, 2005). In March 2003, a moth was caught in a trap in Hamilton. Based on DNA profiling, the gypsy moth detected in New Zealand is considered to have been the Asian form and most likely from Japan (Ross, 2005). The timing of the
detection suggested that the moth was most likely from an imported egg mass and had developed in New Zealand (Ross, 2005) rather than from an imported pupa. An eradication programme including aerial spraying was conducted. No further moths were trapped and Asian gypsy moth was declared eradicated from New Zealand in May 2005 (Ross, 2005). Asian gypsy moth life stages (most commonly egg masses) have been detected at the New Zealand border on hundreds of occasions (BMG, unpublished data). They are most frequently associated with used vehicles from Japan although they have been intercepted from containers and vessels.
5.1.2. Previous risk assessments on Asian gypsy moth
There have been two previous risk assessments for Asian gypsy moth, one, in 1993, focused primarily on the introduction via shipping (Cowley et al., 1993) and the other, in 2000, for used cars (MAF, 2000). The current risk analysis covers all the pathways that are now known or suspected for Asian gypsy moth and incorporates new information on the life cycle, host range, pathways and the incursion in Hamilton.
5.2. PEST INFORMATION
5.2.1. Pest taxonomy
Scientific name: Lymantria dispar L.
Synonyms: Porthetria dispar L., Ocneria dispar1
Class: Insecta
Order: Lepidoptera Superfamily: Noctuoidea
Family: Lymantriidae
Common names: gypsy moth, Asian gypsy moth, European gypsy moth
Lymantriidae is a worldwide family with representatives on all continents except Antarctica, but it is absent from certain oceanic islands (Schaefer, 1989). The genus Lymantria contains more than 158 species including the nun moth (L. monacha), another well-known pest (Schaefer, 1989). New Zealand has no native members of the Lymantriidae, and no exotic lymantriids are currently established in New Zealand (Dugdale, 1988).
As expected for a widespread and variable species, the taxonomy is complicated. A number of subspecies have been described for Lymantria dispar but a recent revision of the genus only accepted two subspecies: the mainland L. dispar dispar and, in parts of Japan, L. dispar
japonica2 (Schintlmeister, A. (2004). Little is reported about how these subspecies differ (or
otherwise) in biology. In the literature, the main differences in biology reported are between gypsy moth from Asia (generalised under the name Asian gypsy moth) and gypsy moth from Europe and North America. From a biosecurity perspective the two most important
differences between and Asian and European forms are the greater flight ability of females and the wider host range shown by Asian populations (for example far eastern Asia and Siberia) (Roy et al., 1995). Another difference is the type of sites chosen for pupation and egg-laying (Humble and Stewart, 1994), which may also have some significance for risk analysis of this species. The terms Asian gypsy moth and European gypsy moth are widely used without denoting a strict taxonomic distinction, nor is there a strict geographical boundary between the ranges of the two forms. In this risk analysis the term Asian gypsy moth refers to moths from eastern Asia with predominantly flying females – Japan, China, North and South Korea and Russia to the east of the Ural Mountains, while European gypsy moth refers to predominantly non-flying forms in Europe (west of the Ural Mountains) and North America. Gypsy moth from western and central Asia would usually be referred to as Asian gypsy moth but is not included in this analysis.
Information based on non-typical forms such as females capable of flying in Europe is identified in the text. Some sources refer to populations with females capable of flying that occur in Europe as Asian gypsy moth, that is, introduced from Asia (e.g. see Charlton et al. 1999; USACHPPM 1994). Others consider the presence of flying females to be part of the natural variation of gypsy moth in Europe (Roy et al. 1995; Zolubas et al. 1999). Others do not specify, or consider that there is insufficient evidence to determine the population origin (Reineke and Zebitz 1998). This analysis is concentrated on the Far East, and risks associated with these populations in Europe are not considered in the analysis. There is further
discussion of the flight ability of female gypsy moth in the section on dispersal (5.2.5).
1 This is not a complete synonomy. These are the synonyms most widely used in publications on gypsy moth.
2 While L. dispar japonica is only considered to occur in Japan, it is unclear whether the author accepts L. dispar dispar as present in Japan or not. The text of the revision implies that L. dispar dispar is present on Hokkaido at least and possibly elsewhere in Japan.
The Asian/ European distinction is not the only significant variation in gypsy moth. Gninenko and Orlinskii (2003) summarise differences between four geographical forms in Russia (including flight capability of females and larval dispersal distances). Japanese populations also vary, with a number of subspecies described (Higashiura, 1989; Paul Schaefer pers. comm. September 2005).
This risk analysis concentrates on the form of gypsy moth found in far eastern Asia, because gypsy moth from far eastern Asia is commonly detected at the New Zealand border; the post- border detection of a male in a trap in 2003 was determined to be of Japanese origin by DNA profiling (Ross, 2005). The term “Asian gypsy moth” is used, in this analysis, to refer to this form of the species. Gypsy moth from other regions, with or without flying females, is also regarded as a threat to New Zealand. Information from this risk analysis will be useful in understanding the threat posed by gypsy moth from other regions as well as other lymantriids not included in this analysis.
While this risk analysis is focused on Asian gypsy moth, the majority of the research has been conducted on the gypsy moth in the USA, which originated in western Europe. In a number of cases the assumption is made that biological information based on European forms of gypsy moth is also relevant to Asian gypsy moth. Where this assumption has been made, the origin of the moths used is stated where possible, and if there is any suggestion that Asian gypsy moth is different this has been recorded. It is also assumed that information on gypsy moth in one Asian country or region is relevant to gypsy moth from other Asian countries. This
assumption may be problematic given the variation within the species. Again, the origin of the gypsy moth used for the research is stated wherever possible.
These assumptions are important because it means that new information on variations in the biology of gypsy moth may alter the recommendations and conclusions of this risk analysis. 5.2.2. Geographical range
Gypsy moth is native to Eurasia, its range extending into North Africa and Japan (CAB International 1999). It has been introduced into North America and has established over large areas there (CAB International 1999). A full list of countries with gypsy moth present is given in Appendix A. This risk analysis includes only east Asian countries with gypsy moth – Japan, mainland China, North and South Korea, Taiwan and the Russian Federation.
5.2.3. Morphology 1
5.2.3.1. Eggs
In far eastern Russia, egg masses usually contain 228 to 431 eggs, depending on whether there is an outbreak, and if so, the population stage during the outbreak (Anonymous, 1992), although they can contain as many as 1500 eggs (Savotikov et al., 1995). Egg masses usually range from 15-40 mm in length (Humble and Stewart, 1994), although an egg mass 7.5 cm long was reported on a tyre on a car imported from Japan (MAF Quarantine Service, unpublished data, September 2005, see figure 2). Egg masses are roughly oval in shape and slightly raised, and have a covering of hairs from the female’s body which gives them a buff to beige colour (Humble and Stewart, 1994). Eggs are laid on a wide range of objects, for example, tree trunks, rocks, buildings, sea containers (see figure 3) and vehicles.
Figure 2. Asian gypsy moth egg mass from car imported from Japan (source MAF Quarantine Service)
Figure 3. Asian gypsy moth egg masses on container from Russian Federation (source MAF Quarantine Service)
5.2.3.2. Larvae
Larvae range from 2-3 mm long when newly hatched to 60mm long when mature (Humble and Stewart, 1994). They are hairy and have rows of blue (forward) and red (hind) spots along the back which are very distinctive (figure 4).
Figure 4. Asian gypys moth larvae (photo: Melody Keena, USDA Forest Service).
5.2.3.3. Pupae
Pupae are dark reddish brown in colour, usually with hairs attached (Humble and Stewart, 1994). Female pupae are 15-35 mm long, with male pupae generally smaller (15-20 mm). They are found in protected areas such as bark crevices, under moss and leaf litter (see figure 5).
Figure 5. Gypsy moth pupae on rock, from Kyrgyz Republic (from Andrew Liebhold http://www.fs.fed.us/ne/morgantown/4557/liebhold/kyrgyz1/)
5.2.3.4. Adults
Males are strong fliers, tan to brown with irregular markings and a wingspan of 37-50 mm (Humble and Stewart, 1994). Females are whitish with dark, wavy bands on the forewing and a wingspan of 37-62 mm (or up to 97 mm, Melody Keena pers. comm. July 2006, figure 6). A wide range of factors other than sex influences adult size, including diet, population density and geographical origin (Keena et al., 2007). Adults have non-functional mouthparts and therefore do not feed, a feature common to all lymantriids (Schaefer, 1989).
Figure 6. Asian gypsy moth adult female (left) and male (photo: Melody Keena, USDA Forest Service).
Adults, pupae and mature larvae of Asian gypsy moth are reported to be larger on average in size than European gypsy moth (Humble and Stewart, 1994). However the overall picture is more complex than this generalisation, for example Keena et al. (2007) reported that females from a population from Mineralni (far eastern Russia) had a greater wing size but lower body weight than females from a North Carolina population (reared under laboratory conditions). 5.2.4. Life cycle
The life cycle of Asian gypsy moth is illustrated in figure 7. Gypsy moth is univoltine, and survives for most of the year in the egg stage (Humble and Stewart, 1994; Savotikov et al., 1995). It has previously been suggested that under New Zealand conditions Asian gypsy moth may have more than one generation per year (Walsh, 1993), although this hasn’t been
reported in gypsy moth populations elsewhere. Reported chilling requirements for egg masses and the preference of larvae for spring foliage (both discussed later in this analysis) now suggest that multivoltine populations of gypsy moth are unlikely and therefore the possibility of wild, multivoltine forms of gypsy moth is not considered further in this analysis.
Figure 7. Life cycle of Asian gypsy moth
Egg hatching typically occurs in spring, for example April-May in Russia (Savotikov et al., 1995) and early May in Inner Mongolia, northern China (Tong et al., 2000).
Gypsy moth eggs in North America undergo a prediapause phase, a diapause phase typically lasting several months, then a postdiapause phase prior to hatching (Gray et al., 2001). The transition from one phase to another is dependent on temperature; this transition has been modelled in detail by Gray et al. (2001). European and Asian populations of gypsy moth differ in the number of degree-days necessary for larval development in the egg. Under daily average temperature of 10o C, development takes 27.5 and 26.0 days for European1 and Asian2 populations, respectively (Anonymous, 1992).
Temperature strongly influences hatching patterns in gypsy moth, as is shown in the work of Keena (1996). Asian gypsy moth3 eggs required a shorter exposure to low temperature (5oC)
1 from the European part of Russia 2 from the Asian part of Russia 3 from Nadhodka in far eastern Russia
than the European gypsy moth1 eggs. For both forms of gypsy moth, eggs that had undergone longer chilling periods tended to hatch more rapidly and in a more synchronised manner (i.e. more eggs hatched within a shorter time period), with a greater proportion of eggs having hatched at the end of the experimental period (225 days). For Asian gypsy moth, chilling at both 5oC and 10oC for a 60 day period resulted in subsequent hatch rates in excess of 60 percent, while chilling at 15 oC for a 60 day period resulted in hatching rates around 20 percent (after 10 weeks at 25 oC). Exposure to constant temperatures of 25 oC resulted in less then 1 percent of eggs hatching, but constant temperatures of 15 oC and 20 oC (i.e. with no “chilling” period) resulted in hatching rates in excess of 80 percent and 60 percent
respectively (after 39 weeks).
Keena (1996) also noted that there is a lot of variability within and between strains and evidence for adaptation to shorter chilling times (or no chilling) observed in the laboratory, suggesting that gypsy moth should be able to adapt to climates with warmer and shorter winters than those in the current range.
Some sources record that approximately 25 percent of Asian gypsy moth eggs do not undergo diapause, but hatch in the year in which they were laid (CFIA 2002; Walsh, 1993). A further 25 percent hatch in the second year, then hatching becomes continuous (Walsh, 1993). Egg hatching before winter is also recorded for European gypsy moth, (although a much smaller proportion of the eggs) but it is noted in this case that these larvae do not complete
development in nature (Leonard, 1974) presumably because they are hatching in the wrong season. The temperatures at which these hatching observations were made are not stated, but given the influence of temperature on hatching in the laboratory (Keena, 1996) it is reasonable to assume that the levels and timing of hatching observed in the field will depend very much on specific temperature conditions.
Gypsy moth spends a greater proportion of its life cycle in the egg state than all other life stages put together (approximately 9 months). The maximum time that egg masses can remain viable is uncertain but some authors consider it greater than 2 years (Glare et al., 2003). European gypsy moth2 egg masses are tolerant of extreme conditions including sub-zero temperatures (Leonard, 1981; Sullivan and Wallace, 1972) and heat (41oC) for short periods (Yocum et al., 1991). Viable Asian gypsy moth egg masses have been reported from ships that have spent more than a year in the tropics (Walsh, 1993). The temperature sensitivity of eggs varies depending on the developmental stage of the eggs, so all eggs will not necessarily show this tolerance (Melody Keena pers. comm. July 2006). These extremes represent their environmental tolerance, but not the temperatures at which development occurs. For
modelling purposes the range at which development can occur is considered to be 1-32 oC (Matsuki et al., 2001).
Following hatching larvae disperse by ballooning, then feed for 6-8 weeks, typically with 5 male and 6 female instars (Humble and Stewart, 1994)3 although the length of the larval stage and number of instars is variable. When densities are lower, late instar larvae feed at night and shelter during the day, while early instar larvae remain on the leaves night and day, but during the day are found in more sheltered areas such as leaf undersides (Anonymous, 1992). When population densities are high, Asian gypsy moth4 larvae feed night and day (Anonymous, 1992). This behaviour is similar to that reported for gypsy moth in North America. There, early instar larvae are usually day-feeding, with later instars night-feeding,
1 from Massachusetts
2 from various locations in North America
3 Asian gypsy moth but the origin is not specifically stated. 4 from Russia
but at high densities later instar larvae are commonly observed wandering during the day (Leonard, 1981).
Once feeding is completed, larvae move to protected locations to pupate. Asian gypsy moth pupates on a variety of substrates, similar to those reported for European gypsy moth (under bark flaps, in holes and crevices, on or under stones, among litter) (Melody Keena, pers. comm. September 2005) as well as sometimes pupating on foliage (Humble and Stewart, 1994; Wallner, 1996). It is reported the European gypsy moth1 often pupates on non-host or poor host trees, indicating that pupation site is not necessarily linked to a suitable host species (Mauffette and Lechowicz, 1984).
Keena (M. Keena, pers. comm. September 2005) gives Asian gypsy moth2 laboratory
pupation times as 9-15 days for females and 10-17 days for males at 25oC. Kay et al. (2002a) reported mean pupation times of 27 days at 20 oC for females and 28.5 days for males, indicating that temperature has a strong influence on pupation times. Literature records for European gypsy moth pupation times are variable but often quoted as around or just over 2 weeks (Leonard, 1981). Pupation times for Asian gypsy moth are similar to reported times for European gypsy moth (M. Keena, pers. comm. September 2005).
In the Russian Far East the flight period for adult moths commences in mid-late July or early August and goes through to mid-September (Savotikov et al., 1995), with the peak in early to mid August (P. Schaefer, pers. comm. September 2005). In Japan it is reported to be mid-June to mid-September, varying with latitude, in Korea the peak is late July, in China, mid-June for Beijing (P. Schaefer, pers. comm. September 2005) and July to early August from Inner Mongolia and Shenyang (Tong et al., 2000). As gypsy moth development is dependent on temperature, variation in the flight period between different years (such as that recorded in Savotikov et al., 1995) may be due to climatic variation. However, there are differences in development rates between North American populations that don’t necessarily correspond to climate (Leonard, 1974).
Figure 8. Approximate flight periods for Asian gypsy moth (for references see text).
June July August September Notes early late early late early late early late China (Beijing)
Peak reported to be mid-June
China (Inner Mongolia
and Shenyang) Japan
Varies with latitude Korea
Russia (far east)
overall flight season
peak of flight season
European gypsy moth3 females generally mate only once and move to shaded areas to lay their eggs in a single mass, unless they are disturbed during laying (Leonard, 1974). Asian
1 from North America
2 from far eastern Russia and Japan 3 from North America
gypsy moth1 females mate once or twice and lay one or two egg masses (Tong et al., 2000). Eggs of European gypsy moth are usually laid on trees but may be in any sheltered location relatively near food plants (McManus et al., 2006). For Asian gypsy moth in Russia,
temperature conditions and not proximity to food plants determines the site selection for oviposition, with eggs often laid on areas such as rock outcrops and not in direct proximity to the host plant (Baranchikov and Sukachev, 1989). Oviposition is reported on a range of substrates including foliage, tree boles, rocks and objects associated with lights (Wallner, 1996) and is sometimes described as indiscriminate (Humble and Stewart, 1994). However there are known sites where egg masses are commonly found (e.g. underneath rather than on sides of sea containers, wheel arches of vehicles) (MAF Quarantine Service, unpublished data) suggesting some discrimination in site preference. Egg masses intercepted at the border