Chinese tallow tree (Triadica sebifera (L.) Roxb., Euphorbiaceae) is native to south-southeastern China, Taiwan, and northern Vietnam (Pattison & Mack 2008), is cultivated in Japan and may have naturalized there (Huang et al. 2010), and is either naturalized or invasive in northern India, northern Pakistan, Bangladesh, Java, Indonesia, and southeastern Australia (Figure 1). Tallow tree is reported from Thailand (Sangsawang et al. 2009), and from Panama and Peru (Pattison & Mack, 2008), though the status of the tree populations in these countries is unknown. The species is presently cultivated in South Korea, where there is interest in its capacity to support honey production (Ryu et al. 2008).

In the United States, Triadica sebifera is a noxious and highly invasive species that reportedly was introduced into Georgia in 1772, by Benjamin Franklin (Bell 1966). Recent studies on the genetic variation of T. sebifera (DeWalt, et al 2011; Boyd 2011) have revealed that the genetic strain that Franklin imported (and now confined to coastal areas of southern South Carolina and northern Georgia) is genetically distinct from the more invasive, widespread strain which was introduced by federal biologists around 1905 and has since spread primarily from Florida to East Texas. DeWalt et al, (2011) also concluded that the different phenotypic traits and relative invasiveness evident between the different strains of T. sebifera probably resulted from their different origins within the native range in Asia as well as geographic differences in selective pressures within their introduced ranges. The tree generally is chemically well-defended (although this varies between the different genetic strains), and few native herbivores consume Chinese tallow, though the species has been in the United States for more than 240 years (Siemann & Rogers, 2001). T. sebifera has been documented in 12 states in the southeastern United States, as well as three counties in California and one county in Wisconsin (Figure 2). Tallow tree grows well in riparian or swampy areas where soil is consistently damp or frequently inundated. It is also highly successful in disturbed habitats and open fields where sunlight is plentiful, and thrives in urban areas including Baton Rouge and New Orleans, LA, and Houston, TX.

The earliest known records of the proposed new species, Caloptilia triadicae, are from Baton Rouge, Louisiana and Sumter County, Alabama, both based on diagnostic leaf mine damage from July (photograph) and October (herbarium specimen) of 2004, respectively (Fox et al. 2012). One year later, June 7, 2005, a single male was collected by G. T. Austin in Gainesville, Florida. Larvae of C. triadicae were first discovered on September 16, 2008 and reared by Jason Sharp from Triadica sebifera at Branchton Park in Tampa, Hillsborough County, Florida and from Gainesville, Florida on September 20, 2008 by Susan Wright and James Lollis (Heppner 2008). These adults were sent eventually to DRD who identified them as a probably undescribed species of Caloptilia, not closely allied to any known North American Caloptilia.

Figs. 1–2.

Distributions of Chinese Tallow tree (Triadica sebifera) and Caloptilia triadicae. 1. World distribution of Triadica sebifera. 2. Distributions of Caloptilia triadicae and its host, Triadica sebifera, in the United States.

Because of the morphological characteristics observed, as well as the origin of its host, DRD suspected that C. triadicae may have originated from Asia. A search for all Caloptilia known to feed on Triadica (= Sapium) revealed three Old World species: Caloptilia octopunctata Turner (= C. cirrhocrotala (Meyrick), C. tetratype (Meyrick)), reported from Australia and India; C. sapina Vári, from South Africa; and C. sapiivora Kumata, from Japan (De Prins & De Prins 2012). Caloptilia sapina resembles C. octopunctata in morphology and the two may be conspecific (Kumata 1981). The male genitalia of all three species are distinct from that of C. triadicae, and none possess the relatively large spine from the ventral angle of the cucullus which partally characterizes triadicae. Images of C. triadicae also were sent to colleagues T. Kumata (Japan) and D. Yuan (China), as well as to the late G. Robinson at the Natural History Museum, London, for comparison with other possibly similar Old World species. Nothing identical was reported.

The biology, morphology, and synonymy of Caloptilia (Sphyrophora) octopunctata (Turner) were treated in detail by Kumata (1981). Kumata followed Vári (1961) in recognizing Sphyrophora as a valid subgenus, characterized primarily by the strongly constricted valvae and presence of only a single, short pair of coremata on the male abdomen. Although these characters clearly distinguish C. triadicae (without constricted valvae and with two pairs of long coremata) from this subgenus, it is interesting to note that the late instar larval biology of C. triadicae resembles that of octopunctata with the larva cutting a strip from the leaf margin of its host and rolling this to form a cone on the abaxial (underside) of the leaf, within which it eventually pupates. Caloptilia triadicae closely agrees in wing venation with C. octopunctata, particularly with regard to their extremely narrow hindwings and separation of M₂ and M₃ in the forewing (Fig. 9). The forewing pattern of C. octopunctata also is similar to that of C. triadicae in possessing four evenly spaced, whitish strigulae along the wing margins, compared to three pairs in the latter. All subgenera previously recognized in Caloptilia were treated as synonyms of Caloptilia by W. and J. De Prins (2005). Adults of the four species of Caloptilia currently known to feed on Triadica sebifera can be distinguished using the following key.

Materials and Methods

Specimens examined in this study are deposited in the following institutions:

Specimen preparation. Genitalic dissections were cleared by heating in hot 10% KOH for ∼30 minutes, and subsequently cleaned and stained with either 2% chlorazol black E or mercurochrome solutions. All genitalic illustrations were drawn from dissections temporarily stored in glycerine, which were later permanently embedded in Canada balsam. Genitalic terminology follows Klots (1970) and Kristensen (1984b).

The COI mitochondrial gene region was sequenced for C. triadicae recovered from Florida (n = 18) and Louisiana (n = 20) (Table 1). Specimens were field collected in 2008, curated in 95% EtOH, and were destructively sampled using whole larvae. DNA extraction was performed on each specimen using a Chelex extraction protocol. Each mtDNA PCR was carried out with Stratagene © Paq polymerase (0.1 μl), with primers LCOI-2198 and HCOI-1490 (Folmer et al. 1994) (1.5 μl) and additional MgCl2 (0.5 μl). Samples were thermocycled on MBS Satellite 0.2 G © units at an annealing temperature of 49° C for 35 cycles. PCR products were cleaned using Exo-SAP IT (Affymetrix) and then prepared in separate forward and reverse PCR reactions with Dyenamic dye-terminator chemistry (GE Health Care) for sequencing. Resulting products were cleaned with Sephadex columns. Sequences were then electrophoresed on an ABI 3730xl Genetic Analyzer ©.

Table 1.

Sample information for specimens submitted for COI barcoding.

Results

FIgs. 3–4.

Caloptilia triadicae, adults. 3. Holotype m, Gainesville, Florida. 4. Adult in resting posture, Bartlesville, Oklahoma.

Discussion

Biology. Eggs are laid on either the lower or upper leaf surface of young, tender leaves (Hazen and Fox 2011), often adjacent to a major vein or at the junction of two veins (Fig. 12). The eggs are flat and ∼ 0.3 mm in diameter with a white, reflective surface; they are pressed to the leaf surface, resembling a small blemish on the leaf epidermis. First instar larvae emerge from the egg and immediately chew into the cuticle of the leaf. The initial subepidermal, serpentine mine is ∼ the same width as the diameter of the egg (∼ 0.3 mm). The sapfeeding larva tends to form a rather meandering mine, except upon encountering a vein or the margin of the leaf it typically follows that boundary (Figs. 10, 13). The mine is often enlarged two- or threefold into a chamber at two or three locations along its course. If such a chamber occurs at the leaf margin, the entire leaf may be slightly folded over giving the superficial appearance of an external shelter, but the epidermis of the leaf is not broken and the larva continues to feed internally. Sapfeeding larvae do not consume all the tissue between the upper and lower leaf surfaces and on heavily infested trees there may be distinct mines on both upper and lower leaf surfaces which overlap without interfering with each other. The later externally feeding larval stages (tissue-feeding instars) construct a coiled, rosette-shaped leaf shelter (Figs. 10, 11, 14, 15). An incision is chewed across the leaf, perpendicular to the leaf margin, and the larva uses silk to coil the resulting flap of leaf (usually the flap closer to the apex of the leaf) into the shape of a cone. The dimensions of the coiled leaf shelter vary with the size of the larva and the size of the leaf, but it is always approximately coneshaped, with the smaller base of the cone (diameter 4– 9 mm) toward the midline of the leaf, and the apex of the cone (diameter 7–16 mm, or typically ∼1.75 × diameter of base) at the leaf margin. Pupation takes place within the same shelter, and following the emergence of the adult moth the empty pupal exuvium remains protruding from the center of the leaf coil.

Figs. 5–9.

Caloptilia triadicae, adult morphology. 5. Female genitalia, lateral view, USNM 34067. 6. Female genitalia, ventral view. 7. Male genitalia, ventral view, USNM 34065. 8. Male aedeagus. 9. Wing venation, USNM 34065, male.

FIgs. 10–15.

Triadica sebifera, biology and larval feeding by Caloptilia triadicae. 10. Foliage with initial evidence of larval feeding (New Orleans, Orleans Parish, Louisiana. 22 June 2012). 11. Infested tree with detail insets showing various stages of larval feeding (along Hwy 90, Lake St. Catherine, Orleans Parish, Louisiana. 14 May 2012.) 12. Oviposition sites of Caloptilia triadicae (indicated by arrows) (same collection site as 11). 13. Serpentine mines of early stage sapfeeding larvae (New Orleans, Orleans Parish, Louisiana. 10 October 2012). 14. Characteristic leaf cones rolled by later stage tissue feeding larva (same collection site as 13). 15. Larval predation within cones by ant, Pseudomyrmex gracilis (Bell Chasse, Plaquemines Parish, Louisiana. 19 August 2011).

Fig. 16.

C. triadicae haplotype tree generated for four haplotypes exhibited by study populations in North America. Bars on connecting lines indicate single basepair changes that differentiate lineages. The size of the numbered shapes, representing different haplotypes, corresponds with the abundance of each haplotype relative to the overall sample size for North America. The colors of the numbered shapes correspond to the pie charts in Figure 17, illustrating haplotype distribution by geography).

Fig. 17.

Distribution of North American C.triadicae haplotype diversity from initial collections in the southeastern U.S. in Louisiana and Florida.

In New Orleans, LA, both pupae and external feeding larvae of C. triadicae were collected in February, 2012 by RH and MF; adults were photographed by R. L. Zimlich in Mobile, AL, in January, November, and December of 2012. These observations suggest that there is no extended overwintering stage for C. triadicae, at least for the populations in the southeastern United States. In the vicinity of New Orleans, in a typical year, the authors commonly begin observing damaged leaves of T. sebifera in April or May, with adult C. triadicae emerging shortly thereafter. A complete generation takes only a few weeks, and abundance increases through the growing season, typically reaching a nearly total infestation of host trees by July or August. However, it seems that abundance of the moth early in the growing season and its subsequent rate of population growth are associated with the severity of the preceding winter: following several sustained hard freezes in winter of 2009–10, MF did not observe any evidence of C. triadicae in New Orleans until August, 2010. The population of C. triadicae plummets in winter when the temperature first approaches freezing and the host trees shed their leaves. Winter temperatures may determine the eventual northern boundary of the Chinese tallow tree's distribution, and therefore should present a similar boundary for C. triadicae.

Three species of Triadica, all native to Eastern and southeastern Asia, are currently recognized (Esser 2002). All are trees growing to maximum heights between 10–25 meters. Triadica cochinchinensis Lour. ranges widely from India to China and the Philippines. Triadica rotundifolia (Hemsl.) Esser is the least widespread of the species and occurs from southern China into Vietnam. The native range of Triadica sebifera (L.) Small includes the more southern provinces of Japan and China and is widespread in Taiwan. Because this species can grow within a wide range of dry or wet conditions and is frost hardy, its potential as an invasive species is the greatest. It is likely that larvae of Caloptilia triadicae are capable of feeding on all three species of Triadica.

Adults of Caloptilia triadicae have also been reared in Florida from a secondary host, Gymnanthes lucida Sw. (Euphorbiaceae). The genital morphology of males from this host was found to be identical with those reared from T. sebifera. Gymnanthes lucida is native to Florida, the Bahamas, the Caribbean, and Central America, and is not known to occur in the Old World (Miroslav 2005). Although possessing dissimilar native distributions and are not considered sister taxa, Gymnanthes and Triadica are closely related and belong to the same subclade within the tribe Hippomaneae of the Euphoriaceae (Wurdack et al 2005). Both genera have latex and appear relatively pest free except for specialist herbivores. Consequently, host switching between these two genera by certain herbivores may be possible. Because Caloptilia triadicae is most similar mophologically to other Asian species of Caloptilia, particularly Caloptilia hamulifera Liu and Yuan, and not to any North American Caloptilia, its utililization of New World Gymnanthes as a host is believed to be a later, secondary adaptation.

Natural enemies. The authors (RH & MF) have commonly seen polistine wasps investigating leaf rolls on tallow trees heavily infested with C. triadicae, though actual predation by these wasps has not been observed. Ants, most commonly Pseudomyrmex gracilis (Fabricius 1804), have been observed marauding leaf rolls and removing larvae of C. triadicae (Figure 15). Arachnids are often found residing in leaf rolls formerly inhabited by C. triadicae, but it is unclear whether the spiders consumed the resident larva or pupa or were opportunistically using empty shelters. Several species of parasitoid wasp have also been reared from C. triadicae in the U.S., but have not yet been identified (Hazen and Fox, unpublished data, Greg Wheeler, personal communication).

COI Sequence data. To date, sequence data for the mtDNA COI gene region of C. triadicae from two North American locations (Florida and Louisiana), suggest that populations exhibit multiple mtDNA haplotypes (Fig. 16) and appear to comprise a single species. Analysis of mtDNA sequences yielded four total haplotypes, all of which were found in Louisiana while only two were found in Florida (Fig. 17). This degree of genetic diversity is consistent with field observations (by MF and RH) of outbreak-level infestations of C. triadicae larvae on T. sebifera trees.