Research Article |
Corresponding author: David R. Smith ( sawfly2@aol.com ) Academic editor: Stefan Schmidt
© 2014 David R. Smith, Paul D. Pratt, Jeff Makinson.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Smith D, Pratt P, Makinson J (2014) Studies on the Asian sawflies of Formosempria Takeuchi (Hymenoptera, Tenthredinidae), with notes on the suitability of F. varipes Takeuchi as a biological control agent for skunk vine, Paederia foetida L. (Rubiaceae) in Florida. Journal of Hymenoptera Research 38: 1-15. https://doi.org/10.3897/JHR.39.8096
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Formosempria Takeuchi, 1929, is distributed in southeastern Asia from Taiwan and China to Vietnam, Myanmar, and possibly northern India. Three species are included: F. crassicornis Wei & Nie, 2002, F. shanensis Malaise, 1961, and F. varipes Takeuchi, 1929 (= F. annamensis Malaise, 1961, syn. n.; = F. metallica Wei, 2003, syn. n.). Formosempria varipes was reared from larvae feeding on Paederia foetida L. (Rubiaceae) in Hong Kong and was a potential biological agent for the invasive P. foetida in Florida. Larval feeding tests indicate more than one species of Paederia are suitable hosts for F. varipes and further study for use as a biological control agent in Florida is unwarranted. Descriptions and illustration of the species are given, and life history notes on F. varipes are presented.
Symphyta , biological control, skunk vine
Interest in the small and little-known genus Formosempria Takeuchi was prompted by discovery of larvae of a species in Hong Kong feeding on skunk vine, Paederia foetida L. (Rubiaceae), a target for a biological control program in Florida (
Formosempria was based on a single species, F. varipes, described from a single specimen (
Discovery of F. varipes feeding on Paederia in Hong Kong initiated studies on the species as a possible biological control agent for P. foetida in Florida. However, host preference studies showed that several species of Paederia may serve as host plants, thus making it unsuitable for release as a biological control agent of P. foetida in Florida.
Figures
Acronyms used are: CSCS (Collection of Central South University of Forestry and Technology, Changsha, Hunan, China); FSCA (Florida State Collection of Arthropods, Gainesville, FL, USA); IPRL (Invasive Plant Research Laboratory, Agricultural Research Service, U. S. Department of Agriculture. Ft. Lauderdale, FL, USA); NHR (Naturhistoriska Riksmuseet, Stockholm, Sweden); UOP (University of Osaka Prefecture, Sakai, Japan); SDEI (Senckenberg Deutsches Entomologisches Institut, Müncheberg, Germany); USNM (National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA).
Recent surveys by JM resulted in the discovery of numerous F. varipes larvae feeding on the foliage of P. foetida in the Sham Tseng area (N 22.373, E114.064), Hong Kong. Taxonomic and biological assessments were based on F. varipes individuals that were shipped from Hong Kong in March 2013 and April 2014 to the quarantine facility at IPRL, under permit #P526P-12-04814. In an effort to establish a laboratory colony of F. varipes, 25 males and 25 females from the 2013 shipment were added to each of three screen cages (33 × 33 × 61 cm) within the quarantine glasshouse (28 °C (±5), 85% (±10) relative humidity). Each cage contained a potted P. foetida plant as well as several cotton balls hydrated with dionized water, which were positioned on the top surface of each cage. Observations of these adults, the resulting eggs, and larvae were recorded.
A subset of adults arising from the 2014 shipment were incorporated into no-choice host range tests, which were designed to quantify the propensity of F. varipes to oviposit and feed on select Paederia species. Among the Paederia, only Paederia ciliata (Bartl. ex DC) Standley is native to North America and has a geographic range limited to Mexico (
Additionally, no-choice larval tests were conducted to determine if P. ciliata is a developmental host. Other Paederia species were also included to provide insights into the generic specificity of the herbivore: Paederia bojeriana (Rich.) Drake, P. cruddasiana Prain, P. pilifera Hook., and the target weed P. foetida. Tests were conducted in a single controlled environmental chamber set at 25 °C, 75% relative humidity and 14:10 light:dark. Neonate larvae (< 24 hrs old) were collected from the laboratory colony and five individuals were transferred onto a slightly moistened filter paper within individual 90 × 15 mm petri dishes. Five replicate petri dishes with the accompanying larvae were randomly assigned one of five replicated plants for each of the five host plant treatments. Leaves were excised from assigned test plant replicates and placed within the petri dish, which was sealed with parafilm and maintained at internal conditions of 25 °C and 90% relative humidity. A mixture of soft, newly developing and mature, fully expanded leaves in excess of the herbibore’s daily consumption were added to each petri dish every 24 hours. Survivorship was monitored daily and larval development time to the prepupal stage was noted. The influence of host plant species on oviposition, larval survival, and development rates were compared with ANOVA followed by Tukeys HSD post hoc analysis (PROC GLM;
Formosempria
Antenna (Figs
Species of Formosempria are superficially similar to species of Empria, being similar in size and color and similar wing venation; thus, the reason for the name.
Based on this study, two species of Formosempria are recognized, F. varipes from Taiwan, southeastern China, and Vietnam, and F. shanensis from Myanmar. Formosempria crassicornis Wei and Nie is listed, but the type was not examined and its status cannot be determined. The record of Formosempria from India by
Formosempria crassicornis
This species was described from Hainan, China. The holotype, deposited in the Institute of Zoology, Chinese Academy of Sciences, Beijing, was not examined.
The figures by
Formosempria shanensis
Malaise described this species from five females from “Burmese Southern Shan States (Taunggyi at 1500 m)”. The syntypes are in NHR and were examined. The lectotype, here designated, is a female labeled “S. Shan States, Burma, 1500 m, Taunggyi, 1-VIII-22.IX.34 [“22.IX” crossed out], Malaise”, “TYPUS” [red], “Formosempria shanensis n. sp., R. Malaise det 1958”, “NHRS-HEVA 000000834” with a lectotype label added. The other four females are paralectotypes with the same data but with the label “PARATYPUS” [in red]; three do not have dates crossed out and one has “1-VIII” crossed out.
The color and structure are very similar to F. varipes, but F. shanensis differs by its slightly larger size, the more truncate clypeus with more acute lateral corners (Fig.
Formosempria varipes Takeuchi, 1929: 85–86. Figure of wings;
Formosempria annamensis Malaise, 1961: 249. syn. n.
Formosempria metallica Wei, in
Female: Length, 6.5–7 mm. Black, with slight metallic lustre, and following white: apices of coxae, trochanters, basal third of mid and hind femora, basal third to half of mid and hind tibiae, base of hind basitarsus, most of mid and fore basitarsi. Wings lightly, uniformly infuscated; veins and stigma black. Head and body with slight metallic luster, smooth, shiny, with short silvery hairs.
Antenna (Figs
Male: Length, 6.5 mm. Similar in color and structure to female. Genitalia in Figs
Neonates (Fig.
Last feeding stage (Fig.
Prepupa: Differs from feeding stages by head, thorax, and abdomen entirely pale, whitish. Setae on head and body absent. Each mandible with 3 linear teeth; left mandible with outer tooth largest, basal 2 teeth smaller and subequal in size; right mandible with central tooth largest, outer and inner teeth smaller and subequal in size.
Takeuchi described this species from a single female “Sozan near Taihoku, Formosa” “collected by M. Kato, on May 2, 1926”. The holotype should be in UOP with the Takeuchi collection. On a visit to Japan in 1979, I examined the holotype and took some brief notes. When recently requesting the type, it could not be found in the Takeuchi collection at UOP. A thorough search for the type was made by Noria Hirai (UOP) and Akihko Shinohara (National Museum of Nature and Science), but to no avail.
Formosempria annamensis was described from a single female. The holotype is at NHR, was examined and is labeled “Phuc Son, Annam, XI-XII, H Rosse, Berlin, s.w. 11”, “TYPUS” [red], Formosempria annamensis n. sp., R. Malaise det 1958, “NHRS-HEVA 000000839”.
Formosempria metallica was described from nine female and male specimens from Hubei, Fujian, Zhejiang, Hangzhou provinces, China. The female holotype is at CSCS, from “Maheba, Xiangeng, Hubei, 1999-VII-25” and was examined. The holotype label is in Chinese, with the same date and “450 m.” and additional labels “F. metallica”, “Holotype: Formosempria metallica Wei female, M. Wei 1992”.
CHINA: Hong Kong, Sham Tseng San Tsuen Temple, larvae, March 24, 2013, on Paederia foetida, adults April 2013, reared in quarantine, ARS, Ft. Lauderdale, FL by Paul Pratt (5 ♀, 5 ♂, USNM); same data, larvae March 2014, pupated and adults emerged IV–V 2014 (about 7 ♀, 100 ♂, 20 larvae, USNM, IPRL); Hubei, holotype and paratype of F. metallica (1 ♀, 1 ♂, CSCS); Zhejiang, paratype; Henan (1 ♀, SDEI). TAIWAN: Keelung Co., Keelung City, V.2004, Malaise trap, L. Stange and H. Wang (1 ♀, 4 ♂, FSCA). VIETNAM: Holotype of F. annamensis (1 ♀, NHR).
China (Hong Kong, Hubei, Fujian, Zhejiang, Hangzhou); Taiwan; Vietnam.
Paederia foetida, also P. ciliata, P. cruddasiana, P. bojeriana, and P. pilifera based on host testing (Rubiaceae).
The interpretations of F. varipes by
Malaise’s holotype of F. annamensis from Vietnam is identical to specimens from Taiwan and Hong Kong; therefore, we synonymize this species.
Wei (in
The objective of importing F. varipes into the IPRL quarantine facility was to determine the sawfly’s host range, from which inferences can be drawn concerning the herbivore’s suitability as a biological control agent of P. foetida in Florida. Females from the 2013 survey were observed dragging their ovipositors across the leaf surface shortly after release into the cages, creating 1-2 cm longitudinal incisions through the leaf and typically located midway between the midvein and the leaf margin. Eggs (Fig.
Neonates (Fig.
A second collection of F. varipes larvae in Hong Kong was made in April 2014 and efforts to colonize the species were repeated. Adults arising from this 2014 shipment were also used in no-choice host range tests, which were designed to quantify the propensity of F. varipes to oviposit and feed on select Paederia species. Oviposition was observed among all replicates of P. ciliata and P. foetida tested. There was no difference in the number of larvae recovered from the Paederia species used in the ovipositional test (F1,9 = 3.0; P ≤ 0.1214). From these data it is clear that F. varipes females readily oviposit on the Mexican endemic P. ciliata so no-choice larval feeding tests were conducted to determine if P. ciliata is also a developmental host. Survivorship varied among hosts (F4,24 = 10.38; P < 0.001), with no individuals completing development when held with P. pilifera. Larval survivorship did not vary when feeding on the remaining species including P. foetida (90.0% (±0.05)), P. cruddasiana (88.0% (±0.08)), P. ciliata (76.0% (±0.10)), or P. bojeriana (52% (±0.22)). Host plant species also influenced development times (F3,17 = 6.69; P < 0.005). Development from neonate to prepupa was shortest when feeding on P. foetida (9.5 days (±0.3)) and P. bojeriana (9.8 (±0.5)) but slowest when held with P. ciliata (13.1 (±0.9)), with P. cruddasiana (11.6 (±0.6)) intermediate. Like those of 2013, all efforts to establish a laboratory colony were unsuccessful with the 2014 material.
Although P. ciliata may not be an optimal host based on development rates, these data demonstrate that F. varipes will readily oviposit and complete development on the Mexican native under no-choice conditions. The risk F. varipes would pose to P. ciliata populations is a function of 1) host use, as reported herein, but also 2) the permeability of geographic barriers that inhibit landscape level dispersal of the herbivore from its intended range (Florida) to the native range of P. ciliata (central Mexico). While the dispersal pathway(s) remain unknown, there are several examples of biological control agents spreading far beyond their intended geographic ranges through natural or anthropogenic means (
We thank the following for loan of specimens: Hege Vårdal (NHR); Meicai Wei (CSCS); Stephan Blank (SDEI); and Jim Wiley (FSCA). We appreciate the help of Noria Hirai (UOP) and Akihiko Shinohara (National Museum of Nature and Science, Ibaraki, Japan), for attempting to locate the type of F. varipes. We thank Elizabeth Mattison, Angelica Moncada, Sophie Philizaire, and Tatum Norrell (IPRL, USDA) for rearing, testing, and curation. We also thank Bradley Brown (ABCL) for assistance with field searches and collections in Hong Kong. USDA is an equal opportunity provider and employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.