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Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (: ) in North America J. A. Goolsby a; P. J. Moran a; J. J. Adamczyk a; A. A. Kirk b; W. A. Jones b; M. A. Marcos c; E. Cortés c a United States Department of Agriculture, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX, USA b USDA-ARS, European Biological Control Laboratory, Montpelier, France c Biodiversity Research Institute (CIBIO) University of Alicante, Spain

First published on: 26 August 2009

To cite this Article Goolsby, J. A., Moran, P. J., Adamczyk, J. J., Kirk, A. A., Jones, W. A., Marcos, M. A. and Cortés, E.(2009) 'Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (Poales: Poaceae) in North America', Biocontrol Science and Technology, 19: 9, 899 — 918, First published on: 26 August 2009 (iFirst) To link to this Article: DOI: 10.1080/09583150903189099 URL: http://dx.doi.org/10.1080/09583150903189099

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RESEARCH ARTICLE Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (Poales: Poaceae) in North America J.A. Goolsbya*, P.J. Morana, J.J. Adamczyka, A.A. Kirkb, W.A. Jonesb, M.A. Marcosc, and E. Corte´sc

aUnited States Department of Agriculture, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX, USA; bUSDA-ARS, European Biological Control Laboratory, Montpelier, France; cBiodiversity Research Institute (CIBIO) University of Alicante, Spain (Received 21 June 2009; returned 6 July 2009; accepted 14 July 2009)

The armored scale Rhizaspidiotus donacis (Leornardi) was evaluated as a potential biological control agent of the invasive reed grass Arundo donax in North America. No-choice tests, native range field surveys and non-target host exposures were used to determine the fundamental host range of the scale collected from Caloma, Spain and Perpignan, France. Thirty-five species, including two genotypes of A. donax and seven ecotypes of Phragmites australis, along with closely related grasses, economic grasses and habitat associates were tested. In quarantine no-choice testing using releases of 200 crawlers per , normal development of R. donacis was observed on A. donax and A. formosana, with very limited survival to the adult stage on alterniflora and Leptochloa spp. In follow-up studies using 1000 crawlers per plant, 10 live adult females were found on Leptochloa virgata, and one adult female on Spartina alterniflora, but average adult female abundance per plant was (2580%) 26-times lower on L. virgata and over (39,090%) 100-times lower on S. alterniflora than on A. donax. Field surveys were conducted at five locations in Spain and France at which A. donax infested with R. donacis, co-occurred with two non-target species of concern and R. donacis was only found on A. donax. Six-month field host exposures in Spain using potted Leptochloa entwined with heavily infested A. donax confirmed that R. donacis is specific to Arundo under field conditions. Based on our results, the scale R. donacis appears to be specific to the Arundo and is unlikely to harm native or cultivated plants in the Americas. Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 Keywords: biological control of weeds; host specificity testing; invasive grasses

Introduction Arundo donax is native to the Old World from the Iberian Peninsula and Mediterranean coast of Europe to south Asia, including North Africa and the Arabian Peninsula. It has been cultivated in the Old World for thousands of years as a fiber crop and source of reeds for wood wind instruments. It was later widely introduced around the world for roof thatching, craft making, and erosion control. Subsequently, it has become naturalized and invasive in many tropical, subtropical,

*Corresponding author. Email: [email protected]

First Published Online 26 August 2009. ISSN 0958-3157 print/ISSN 1360-0478 online # 2009 Taylor & Francis DOI: 10.1080/09583150903189099 http://www.informaworld.com lo

900 J.A. Goolsby et al.

and warm-temperate regions of the world. Arundo donax is an invasive weed of riparian habitats and irrigation canals of the Rio Grande River Basin and the southwestern US (Everitt et al. 2004; Spencer, Ksander, and Whitehand 2005; Quinn and Holt 2008). Giant reed, also known as carrizo cane, dominates these habitats, which leads to loss of biodiversity, alters channel morphology, damages bridges, increases costs for chemical and mechanical control along transportation corridors, and impedes law enforcement activities on the international border (Goolsby and Moran 2009; Moran and Goolsby 2009; Yang, Goolsby, and Everitt 2009). Additionally, this invasive weed consumes large amounts of water (Watts and Moore, unpublished data) and competes for water resources in an arid region where these resources are critical to the environment, agriculture and municipal users (Seawright et al. 2009). Biological control of A. donax with may be the best long-term option for managing this highly invasive weed. Tracy and Deloach (1999) reviewed the feasibility of biological control for A. donax and noted that several insects are known to feed on it in Africa and Europe. One of these insects, Rhizaspidiotus donacis (Leonardi), the Arundo scale, was selected for further evaluation because it appeared to be one the most widespread and damaging associated with A. donax in the subtropical regions of its native range in Mediterranean Europe (Figure 1). Rhizaspidiotus donacis occurs with the Arundo wasp, Tetramesa romana Walker, most notably in the western Mediterranean (Portugal, Spain, and south- western France). Populations of T. romana from Mediterranean Europe were permitted for release in Texas, USA in April 2009. Both the original description of Rhizaspidiotus donacis (as Targionia donacis, later transferred to Rhizaspidiotus by Ferris 1943) and other collections from the native range (reviewed by Balachowsky 1932, 1951) in France (Balachowsky 1930, 1933, 1951), Spain (Balachowsky 1935; Gomez-Menor Ortega 1958; Martin-Mateo 1983), Italy (Lupo 1957), and North Africa (coastal Algeria) (Balachowsky 1928) indicate that R. donacis has been collected only from Arundo donax, with the exception of one report from Turkey (Uygun, Sengonca, Erkilic, and Schade 1998) that indicated a collection from common reed (Phragmites australis) a finding inconsistent with our own field collections. Possibly, the plant was misidentified and was actually A. donax, which is known to occur in this part of Turkey. Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010

Figure 1. Rhizaspidiotus donacis scale on Arundo donax. Biocontrol Science and Technology 901

The genus Rhizaspidiotus MacGillivray contains 13 mostly Palaearctic members (Kosztarab and Kozar 1988; Ben-Dov and German 2003), including both mono- phagous/oligophagous and polyphagous species. Besides the Arundo scale, one other species, Rhizaspidiotus secretus (Borchsenius), uses Arundo donax and other Arundo spp. as hosts as well, including Phragmites australis. This species is found in Tajikistan, Pakistan and Afghanistan (Danzig 1993). A Russian species, Rhizaspi- diotus graminis Borchsenius, feeds on Arundiella spp. (Danzig 1993). Two European/ Mediterranean species in addition to the Arundo scale feed on grasses: Rhizaspi- diotus balachowskyi Kozar & Matile-Ferrero, found on gryllus (Koza´r and Matile-Ferrero 1983), and Rhizaspidiotus bivalvatus Goux, found on Festuca arundinaceae and F. ovina (Balachowsky 1951). There is also a Chinese species, Rhizaspidiotus amoiensis Tang that feeds on Imperata spp. (Tang 1984). Literature records suggest that the grass-feeding Rhizaspidiotus species are host-specific at the genus or sub-generic level, although past information on host range is limited for most species. The monophagy/oligophagy of the grass-feeding Rhizaspidiotus scales could be related to their adaptations to exploit grasses, which often employ physical, physiological, and biochemical defenses that are different from those in the types of dicot hosts used by other congeners of R. donacis. Four other species in the genus Rhizaspidiotus appear to be oligophagous, (Hall and Williams 1962; Tang, Hao, Shi, and Tang 1991; Danzig 1993). In contrast, the remaining species within the genus are polyphagous, but none of these species use grasses extensively (Lupo 1957; Gomez- Menor Ortega 1968; Martin-Mateo 1983; Kosztarab and Kozar 1988; Longo, Marotta, Pellizzari, Russo, and Tranfaglia 1995; Kaydan, Kilincer, and Koza´r 2005). The type member of the genus, Rhizaspidiotus dearnessi Cockerell, is native to North America (Ferris 1943) and can be a minor pest (Miller and Davidson 2005). Its host range includes members of the the Asteraceae family and eight other families (McDaniel 1970; Dekle 1976; Kosztarab 1996; Polavararpu, Davidson, and Miller 2000). Ferris (1943) considered the genera Targionia Signoret (the genus to which the Arundo scale once belonged) and Quadrispidiotus MacGillivray as close allies to Rhizaspidiotus. Both genera contain polyphagous armored scale species, such as Targionia vitis (Signoret) and Targionia nigra Signoret that are found throughout the northwestern and north-central Mediterranean basin (Balachowsky 1935; Ferris 1943; Lupo 1957; Gomez-Menor Ortega 1958; Martin-Mateo 1983), and in North Africa (Balachowsky 1932). Quadraspidiotus jaapi (formerly Targionia jaapi)isa

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 polyphagous species in Spain (Gomez-Menor Ortega 1958), and France (Bala- chowsky 1930). The San Jose scale (Quadraspidiotus perniciosus) is a polyphagous pest of citrus and ornamentals in Turkey (Sengonca, Uygun, Karaca, and Schade 1998; Uygun et al. 1998), Europe (Martin-Mateo 1983; Longo et al. 1995), and North America (Dekle 1976). Pest armored scale species in the Tribe Aspidiotini, such as the California red scale (Aonidiella aurantii Maskell), found in Turkey (Uygun et al. 1998) Spain (Martin-Mateo 1983), Italy (Longo et al. 1995), North Africa (Balachowsky 1932) and North America (Dekle 1976), the oleander scale (Aspidiotus nerii Bouche´), the laurel scale (Aonidia lauri Bouche´), the Florida red scale (Chrysomphalus aonidum (L.)) (Viggiani 1994) and Q. perniciosus, are usually characterized by polyphagy and the ability to complete their life cycles on factitious hosts, such as cucurbit fruit (Cucurbita, Citrullus) or potato tubers (Solanum tuberosum L.) (Rose 1990), in 902 J.A. Goolsby et al.

contrast to our native range field collections and initial laboratory observations of the Arundo scale, which both indicated a requirement for A. donax for complete development and reproduction. Monophagy is not unusual in the aspidiotine armored scales. Of the 40 species of Aspidiotini listed for Texas by McDaniel (1970), 40% were considered monophagous, and in Spain 45%, of 38 species were collected from only one host (Martin-Mateo 1983). However, the apparent percentage of monophagous species may be an overestimate since many species found in the literature are known only from their original description and some publications report the results of incomplete field surveys. No armored scale species have previously been released for classical weed biological control. However, Chionaspis etrusca Leonardi, native to North Africa and Spain (Balachowsky 1932; Martin-Mateo 1983), is an adventive scale feeding on highly invasive saltcedars ( spp.) in North America (Tracy and DeLoach 1999). A pseudococcid ( (Hemprich & Ehrenberg)) native to the eastern Mediterranean is under consideration for future release to control saltcedars. The widespread success of several Dactylopius species (Pseudococcidae) against invasive prickly pear cacti (Opuntia spp.) in Africa and Australia has been documented (Julien and Griffiths 1999). Several factors led to the selection of R. donacis as a candidate agent for biological control of A. donax in North America. First, this species has a geographically and climatically broad native range of R. donacis. Second, the information gained from the literature and our field collections indicated it has narrow host plant specificity. Lastly, R. donacis develops large, persistent, damaging populations on A. donax, which is similar to the significant impacts noted for other armored scale species. The life cycle of the Arundo scale, Rhizaspidiotus donacis follows the general outline of Koteja (1990) for sexually-reproducing, viviparous species. Females produce live crawlers which emerge from the edge of the female’s waxy scale covering. Females collected from southern France or Spain during peak reproductive periods (NovemberÁJanuary and AprilÁJune) produce about 100 crawlers each (up to 300) within one month of collection. Crawlers disperse up and down on A. donax shoots and settle on leaf collars, axillary leaf sheaths at the bases of lateral shoots, and rhizomes within 48 h of release under laboratory conditions. Another common herbivore of A. donax in the native and now invasive range is the eurytomid wasp, Tetramesa romana, which causes stem and side shoot galls. Formation of stem galls causes proliferation of side shoots which are ideal for colonization by R. donacis

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 (Goolsby and Moran 2009; Moran and Goolsby 2009). Therefore, T. romana and R. donacis appear to be complementary herbivores (Goolsby et al. 2009). Settled first-instar crawlers become immobile and began feeding within 3 days of release, as indicated by the appearance of a waxy ‘whitecap’ covering. First instars then secrete a brown waxy covering around the edge of the ‘whitecap’ and molt to the immobile second instar within 25 days of release, as indicated by the appearance of a first- instar exuvia on top of the scale covering. At this stage, males and females can be distinguished by their oyster-shaped and round scale coverings, respectively. Males complete one prepupal and one pupal stage and emerge as winged adults. The life cycle is approximately 40 days long. As in other armored scales (Koteja 1990), adult male R. donacis live only 2Á3days.Rhizaspiditous donacis males crawl on and probe females (J. Goolsby, personal observation). Females molt to the immobile thrid instar or adult stage 45Á70 days after the start of the crawler stage. Variation in Biocontrol Science and Technology 903

female development likely reflects variable quality of settling locations (Koteja 1990). Adult females require three months of continued feeding and expansion and embryonic development of crawlers before reaching reproductive maturity. The objectives of this study were to determine the host range of the Arundo scale Rhizaspidiotus donacis by testing A. donax, 37 other grass species and nine species from other plant families with large populations of crawlers in no-choice tests under laboratory conditions. Follow-up field surveys and host plant exposure tests in the native range examined the ability of R. donacis to colonize two non-target grasses of concern growing immediately adjacent to scale-infested A. donax. Separate studies are underway to determine the impact of R. donacis on A. donax under field and laboratory conditions. Information on both the efficacy and host range of R. donacis will be used to determine its suitability as a biological control agent of A. donax in North America.

Materials and methods Test plant selection The level of suitability of plants to a host-specific herbivore is hypothesized to be highly correlated to phylogenetic distance from the preferred host (Wapshere 1974). Plant species most closely related to the preferred host plant are expected to be most susceptible to attack. Therefore, knowledge of the phylogenetic relationships of plants relative to a target of biological control can help guide the choice of which plants to test, placing highest priority on those with the highest likelihood of risk. The host test list for evaluating the fundamental host range of the Arundo scale, R. donacis, is shown in Table 1. The phylogeny of order Poales puts the family Poaceae (grasses) in a clade with Flagellariacea, Joinvilleacea, and Echdeicoleace (Missouri Botanic Garden Phylogeny Website 2008). Within the family Poaceae, the subfamily Arundinoideae is in an unresolved clade with Chloridoideae, Centothe- coideae, , and Micrairoideae (Hsiao, Jacobs, Barker, and Chatterton 1998). Representatives of all these subfamilies were included in the host range testing except for Micrairoideae which is not represented in North America. Representatives from the more distant subfamilies, Aristidoideae, Danthonioideae, , and Bambusoideae were also tested. When selecting representative species for the host range tests, plants that were morphologically similar to A. donax or native to the

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 southern US were prioritized for testing. Within the Arundinoideae are the following core genera: Arundo, Dregeochloa, Hakonechloa, Molinia, and Phragmites (L. Clark, personal communication). Representatives from all of these genera were tested except Dregeochloa which is endemic to southern Africa. Representatives of the genera Hakenchloa and Molinia were obtained, but are uncommon exotic, ornamental species in North America. Of these core genera, Phragmites is the most critical because it occurs sympatrically with A. donax throughout a large part of its introduced range. There are no native Arundo species in North or South America. The only other Arundo species present in North America is Arundo formosana. This plant is native to Taiwan and is an uncommon, exotic ornamental in the San Francisco Bay Area. Considerable emphasis was placed on selection of Phragmites test plants. There is only one Phragmites species present in North America (P. australis), but there is a 904 Table 1. Results of no-choice host range tests for Rhizaspidiotus donacis, values are mean numbers of scale insects per plant.1

Livedead Indig. Grain/ Habitat Live whitecaps/ Live late 2nd Live adult adult Total live Taxa3 Scientific name to NA Forage associate Reps early 2nd instar instar Adult male2 female female all stages

Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE

Cy-Po-Arun Arundo donax L. No No Á 13 2.3191.99 0.8590.48 9.6292.83 24.1597.10 27.2397.66 37.15910.71 Laredo, TX Arundo donax L. San No No Á 16 0.3890.38 0 11.9492.34 17.8194.56 19.6994.60 30.1395.60 Juan, TX Arundo No No Á 29 1.2490.92a 0.3890.22a 10.9091.79a 20.6694.02a 23.0794.24a 33.2895.63a donax pooled Laredo and San Juan, TX A. formosana Hack. No No No 3 0 0 7.3393.67a 3.0091.53b 5.0092.89b 11.0095.57b Goolsby J.A. Phragmites australis No No No 5 0.4090.4a 0 0.2090.20b 0 0 0.6090.60b Charlestown RI (Exotic European ecotype) Phragmites australis Yes No Yes 4 0 0 0 0 0 0 Mercedes TX Phragmites australis San Yes No Yes 3 0 0 0 0 0 0

Benito TX al. et Phragmites australis Yes No Yes 6 0 0 0 0 0 0 Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 January 6 15:14 At: Library] Agricultural National [USDA By: Downloaded Colorado River CA Molinia caerulea (L.) No No No 3 0 0 0 0 0 0 Moench Hakonechloa macra No No No 3 0 0 0 0 0 0 (Munro) Makino Cy-Po-Aris Aristida purpurea Nutt. Yes No No 3 0 0 0 0 0 0 var. longiseta (Steud.) Vaseyffl Cy-Po-Cent Chasmanthium Yes No Yes 2 0.5090.50a 0 0 0 0 0.5090.50b latifolium (Michx.) Yates Cy-Po-Chlor Bouteloua hirsuta Lag. ffl Yes Yes No 3 0 0 0 0 0 0 Cynodon dactylon (L.) No Yes Yes 3 0 0.3390.33a 0 0 0 0.3390.33b Pers. Dichanthelium Yes Yes No 3 0 0 0 0 0 0 acuminatum (Sw.) Gould and Clark ffl Eragrostis intermedia Yes Yes No 3 0 0 0 0 0 0 Hitchc. ffl Table 1. (Continued). Livedead Indig. Grain/ Habitat Live whitecaps/ Live late 2nd Live adult adult Total live Taxa3 Scientific name to NA Forage associate Reps early 2nd instar instar Adult male2 female female all stages

Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE

Eragrostis spectablilis Yes Yes No 3 0 0 0 0 0 0 (Pursh) Steud. ffl Leptochloa fusca (L.) Yes No No 3 0.3390.33a 0 1.0091.00b 0 1.0091.00b 1.3391.33b Kunth ssp. uninervia (J. Presl) N. Snow Technology and Science Biocontrol Leptochloa panicea (A. Yes No No 3 1.0091.00a 0 0.3390.33b 0 0 1.3391.33b Retzius) J. Ohwi ssp. Brachiata Leptochloa virgata (L.) P. Yes No No 2 0 0 0.5090.50b 1.5091.50b 3.5093.50b 2.0092.00b Beauv. Muhlenbergia Yes Yes No 3 0 0 0 0 0 0 capillaris (Lam.) Trim. ffl Spartina alterniflora Yes No Yes 3 0 0 4.3393.84b 0 6.6796.17b 4.3393.84b Loisel. Spartina spartinae (Trin.) Yes No Yes 3 0 0 0 0 0 0 Merr. ex Hitchc. Sporobolus wrightii Yes Yes Yes 3 0 0 0 0 0 0 Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 January 6 15:14 At: Library] Agricultural National [USDA By: Downloaded Munro ex Scribn ffl Tridens albescens Yes Yes Yes 3 0 0 0 0 0 0 (Vasey) Wooton & Standl. Uniola paniculata L. Yes No Yes 3 0 0 0 0 0 0 Cy-Po-Dant Cortaderia selloana No No No 5 0 0 0 0 0 0 (Schult. & Schult. f.) Asch. & Graebn. Danthonia spicata (L.) P. Yes Yes No 1 0 0 0 0 0 0 Beauv. ex Roem. & Schult.ffl Cy-Po-Pani Andropogon Yes Yes Yes 3 0 0 0 0 0 0 glomeratus (Walter) Britton et al. ffl cognata (Schult.) Yes Yes No 3 0 0 0 0 0 0 Pilg. ffl Panicum amarum Yes Yes No 3 0 0 0 0 0 0 ffl

Elliot. 905 Panicum hirsutum Sw. ffl Yes No Yes 3 0 0 0 0 0 0 Panicum virgatum L. ffl Yes Yes No 3 0 0 0 0 0 0 906 Table 1. (Continued). Livedead Indig. Grain/ Habitat Live whitecaps/ Live late 2nd Live adult adult Total live Taxa3 Scientific name to NA Forage associate Reps early 2nd instar instar Adult male2 female female all stages

Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE

Pennisetum ciliare (L.) No Yes Yes 3 0 0 0 0 0 0 Link Saccharum officinarum L. No Yes No 3 0 0 0 0 0 0 Schizachyrium scoparium Yes Yes Yes 3 0 0 0 0 0 0 (Michx.) Nash ffl Sorghum bicolor (L.) No Yes No 3 0 0 0 0 0 0 Moench Tripsacum dactyloides (L.) Yes Yes Yes 3 0 0 0 0 0 0 L. ffl Goolsby J.A. Zea mays L. No Yes No 3 0 0 0 0 0 0 Cy-Po-Pooi virginicus L. ffl Yes Yes Yes 1 0 0 0 0 0 0 Triticum aestivum L. No Yes No 3 0 0 0 0 0 0 Cy-Po-Bamb Arundinaria gigantea Yes No Yes 3 0 0 0 0 0 0 (Walter) Muhl. Cy-Po-Ehrh Oryza sativa L. No Yes No 3 0 0 0 0 0 0

Cy-Cy Cyperus articulatus L. Yes No Yes 3 0 0 0 0 0 0 al. et Schoenoplectus maritimus Yes No Yes 3 0 0 0 0 0 0 Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 January 6 15:14 At: Library] Agricultural National [USDA By: Downloaded (L.) Lye Erio-Erio Eriocaulon decangulare L. Yes No Yes 3 0 0 0 0 0 0  Ty-Typh Typha domingensis Pers. Yes No Yes 4 0 0 0 0 0 0 Ar-Arec Sabal mexicana Mart. Yes No Yes 3 0 0 0 0 0 0 Ju-Jugl Carya illinoinensis Yes Yes Yes 3 0 0 0 0 0 0 (Wangenh.) K. Koch Sa-Sali Salix exigua Nutt. Yes No Yes 3 0 0 0 0 0 0 As-Aster Baccharis neglecta Yes No Yes 3 0 0 0 0 0 0 Britton As-Olea Fraxinus berlandieriana Yes No Yes 3 0 0 0 0 0 0 DC.

1200 crawlers placed on each plant. Means within the same column with the same letter are not significantly different in least-square comparisons of means to pooled A. donax from Laredo and San Juan, TX (in bold above) (P0.05). 2Completion of male development to the winged adult stage is inferred from empty second instar scale covers. 3Subfamilies in Cyperales, Poaceae: Cy-Po-Ar, Arundinoideae; Cy-Po-Aris, Aristidoideae; Cy-Po-Cent, Centothecoideae; Cy-Po-Chlor, Chloridoideae; Cy-Po-Dant, Danthonioideae; Cy-Po- Ehrh, Ehrhartoideae; Cy-Po-Pani, Panicoideae; Cy-Po-Pooi, Pooideae ; Cy-Po-Bamb , Bambusoideae. Other families or orders: Cy-Cy, Cyperales-Cyperaceae; Cy-Erio, Cyperales- Eriocaulaceae; Ty-Typh Á Typhales-Typhaceae; Ar-Arec, Arecales-Arecaceae; Ju-Jugl, Juglandales-Juglandaceae; Sa-Sali, Salicales-Salicaceae; As-Aster, Asterales-Asteraceae; As-Olea, Asterales-Oleaceae.  indicates Endangered in TN; ffl indicates congener of state or federal threatened or endangered species. Biocontrol Science and Technology 907

considerable body of knowledge associated with P. australis because of its worldwide distribution and invasiveness in northeastern North America (Saltonstall 2002). We obtained all of the North American ecotypes for the testing including populations from Rhode Island, California and Texas. Within the Poaceae, the main agricultural grasses, including corn, wheat, sorghum, and rice, were tested. We obtained genetic material of these grasses from the USDA-ARS Germplasm Repositories in Idaho, Georgia, and Colorado. Whole rice plants were obtained from the USDA-ARS laboratory in Beaumont, TX. Several species within the same genus as threatened or endangered grass species within the invasive range of A. donax in North America were also selected as surrogates for testing. Outside of Poaceae, several habitat associates of A. donax were selected that represented species with which the biological control agents may come in contact in the Western or Gulf Coast areas of North America. All of the habitat associates are native non-economic species, except pecans, which are a native economic species, widely planted in the riparian habitats of North America.

Plant culture Arundo donax plants with vigorously growing stems 1 m tall with side shoots were used for the testing. This plant stage was determined to be the optimum plant size and growth stage for settling by R. donacis crawlers. For all other test plant species, we grew or obtained plant material with side shoots if possible. The Arundo donax was collected from two locations along the Rio Grande, San Juan and Laredo, TX. Rhizomes from both locations were dug and transported to research facilities at the USDA-APHIS Mission Biological Control Center for potting. Plants were then held in a heated greenhouse for care and maintenance.

Quarantine host range tests No choice tests Potted A. donax, and non-target grasses, sedges, monocots and broadleaf plants were used for the tests. Plants were grown outside of quarantine in a temperature regulated greenhouse, and then transferred to the quarantine greenhouses for host

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 range testing. Plants were fertilized as needed with Osmocote 20-10-5 and Micromax micronutrients†. Plants were maintained at optimum moisture levels with water applied through a drip system. Quarantine greenhouses were maintained at 28938C with a photoperiod of 14 h L:10 h D). Field collected populations of R. donacis from France and Spain were used for the host range testing due to the length of the life cycle and the need to have large numbers of crawlers available for testing. Jean-Francois Germain, Laboratoire National de la Protection des Vegetaux, Unite´ d’Entomologie, UFR D’Ecologie animale et de Zoologie agricole, Montpellier, France identified the scale. Most of the testing was done with a population of R. donacis scale from Vingrau, France (42 47.039N; 002 54.01E) near the Spanish border. Additional populations from Spain were tested on a subset of the test plants to assure that the host range of R. donacis was consistent between populations. The pooled results are presented. 908 J.A. Goolsby et al.

To determine the genetic diversity of populations used in the testing, we collected 20 individuals from each location and evaluated them using nuclear genetic markers. PCR amplification and sequencing of the D2 and D3 expansion segments of the nuclear large ribosomal RNA gene were performed as described in Morse and Normark (2006) for 9 scale accessions obtained from A. donax plants growing in Spain and France. The locations were Vingrau (Perpignan), Languedoc, France; Lucena del Puerto (Huelva), San Lucar (Sevilla), Las Can˜as-Almun˜ecar (Granada), and Alicante, Spain. These sequences were all identical, which is typical for members of the same species of armored scale insects (Morse and Normark 2006). In addition, the same accessions were analyzed using the ITS-1 sequence and there were no differences in the sequences between populations. From this we conclude that all the scale accessions tested were members of the same species. To obtain neonate, mobile crawlers, mature mother scales were removed from the imported rhizomes and canes and placed in gel capsules. Gel capsules with 5Á10 mother scales were held at 28918C with a photoperiod of 14 h L:10 h D for emergence of the R. donacis crawlers. Capsules were checked daily for the presence of Aphytis parasitoids and discarded if parasitoids were found. Counts of crawlers per capsule were made from a subsample of 10 capsules from each cohort of imported scale. Estimates of the number of live crawlers per capsule were made to assure that 200 crawlers were released per replicate. Opened gel capsules were attached to test plants using pins (Figures 2 and 3). Test plants were held in the laboratory to confirm that the crawlers had moved onto the plants. We also confirmed that settling had occurred on the A. donax used for positive controls before transferring the test plants to the quarantine greenhouses, by examining the collars of leaf sheaths for the presence of ‘whitecaps’, indicative of settling, feeding initiation and production of waxy exudate by late first-instar scales. A subsample of plants was checked monthly for the presence of settled (dead or alive) scales. We did not count dead crawlers. At one month, the presence of a white cap surrounding a yellow exuvia of the first instar cuticle on the dorsal surface of the settled scale was used as an indication of live second instars. Over the next few months, each plant was observed for the presence of live, developing scale. In most cases, the crawlers died on the non-target test plants without developing white caps. On A. donax, the scales settled normally and continued development on the leaf collars, the bases of sideshoots, and the bases of rhizomes. At 90 days after transfer of crawlers, non-Arundo host range replicates were carefully cut from the pots and dissected. On the A. donax plants, a few leaves

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 and/or sideshoots were left on the intact canes to check for reproduction at around 6 months. Therefore, the numbers of scales reported on A. donax species in Table 1 are less than the actual numbers that would have completed development without repeated partial dissection of plants. After removal from plant tissue, scales were probed or dissected to determine if they were dead or live. The numbers of live and dead immatures and adults were counted for each test plant. In some cases, at 90 days the leaf or stem of the non-target plant with scale had died. It was therefore not possible to know if the scale would have survived if the plant had survived. Therefore, two columns are presented with live and total (livedead) adult female scale. For the R. donacis host range data presented in Tables 1 and 2, differences between plant species in counts of live early second-instar scales, live late second- instar females, adult males (as indicated by counts of empty male scale covers), live lo

Biocontrol Science and Technology 909

Figure 2. Gel capsules pinned to test plant to release scale crawlers.

adult females, combined live and dead adult females, and total live scales (all life stages summed) were assessed with SAS software (SAS Institute, Cary, NC, Version 9.1.3), specifically PROC GLIMMIX, using a Poisson distribution and log link function to examine the effect of plant species on counts of each stage. Plant species Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010

Figure 3. Gel capsules with scale crawlers moving onto test plant in host range testing. 910

Table 2. Results of no-choice host range tests for Rhizaspidiotus donacis in which 1000 crawlers were released per plant. Values are mean numbers of scale insects per plant*.

Live whitecaps/ Live late 2nd Live adult Livedead Total live Goolsby J.A. Test plant species Reps early 2nd instar instar Adult male** female adult female all stages

Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE Mean9SE

Arundo donax Laredo, TX 2 12.598.5a 6.0090.00 249924.0a 129940.0a 177953a 398925.5a tal. et Leptochloa fusca ssp. uninervia 3 0 0 1.0091.00b 0 0.6790.67b 1.0091.00b Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 January 6 15:14 At: Library] Agricultural National [USDA By: Downloaded Leptochloa panicea ssp. brachiata 3 0.3390.33b 0 1.6791.67b 0 7.0097.00b 2.0091.53b Leptochloa virgata 2 0 0 1.5091.50b 5.0095.00b 6.5096.50b 6.5096.50b Spartina alterniflora 3 0 0 0 0.3390.33b 1.6790.33b 0.3390.33b

*Means within the same column with the same letter are not significantly different in least-square comparisons of means to pooled A. donax from Laredo, TX (in bold above) (P0.05). Biocontrol Science and Technology 911

on which no scales of a given stage were found on any plants tested were excluded from the analysis of that stage. The LSMESTIMATE statement was used to specify a priori pairwise comparisons of least-square means of scale counts per plant on A. donax (pooled Laredo and San Juan plants) to counts on A. formosana and all non-zero non-A. donax species. A Bonferroni correction was applied to adjust for multiple comparisons, and experimentwise significance was set to P50.05.

High rate no-choice tests No-choice tests were repeated for non-target species that showed use by the scale. In these tests, 1000 crawlers were released per plant. The numbers of scale crawlers were increased from 200 to determine if this would increase colonization of the non-target plants. The plants were held for 3 months, at which time they were dissected to count the numbers and stages of R. donacis.

Field host range studies in Mediterranean Europe Field host range surveys To determine if the minor use of Spartina and of Leptochloa were quarantine artifacts (false positives), field studies were conducted in September 2008 in Spain and France where these non-target grasses are known to occur. Leptochloa fusca ssp. uninervia, has become invasive in rice production throughout Spain in areas that are sympatric with A. donax and R. donacis. Spartina versicolor and Spartina foliosa, some possibly hybrids with Spartina alterniflora, are also sympatric with A. donax and R. donacis in Spain and France. Populations of L. fusca ssp. uninervia in locations with A. donax were at least 16 years old, and likely much older since they were previously documented by Monte and Corte´s (2000). Spartina spp. and A. donax have co-evolved together in the same Mediterranean habitats. Diaspdidae are known to disperse as first instar crawlers both aerially over short distances and by walking across plant foliage. Therefore, both L. fusca ssp. uninervia and Spartina spp. in these field locations had likely been exposed to dispersing populations of R. donacis over many years. To test the hypothesis that Leptochloa fusca ssp. uninervia and Spartina spp. are not hosts of R. donacis under field conditions, plants were collected, dissected and examined under a microscope for the presence of this scale. Selected populations of

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 L. fusca ssp. uninervia were found growing in rice fields in Spain near Palomar (Valencia), Marismilla (Sevilla), and Amposta-Tortosa (Tarragona), Catalun˜a (Figure 4). More than 50 Leptochloa fusca ssp. uninervia plants were collected from multiple (3Á6) locations at each site. Leptochloa fusca ssp. uninervia plants that were selected for the study were found from 0 to 30 m from A. donax that contained normal levels of R. donacis. Spartina versicolor was collected within 300 m of A. donax in El Saler (Valencia), Valencia, Spain. Spartina foliosa was collected within 6 cm of A. donax near Leucate (Perpignan), Languedoc, France (Figure 5).

Field exposures of Leptochloa dubia plants in Spain To further evaluate the realized (field) host range of R. donacis, field populations of a naturalized Texas native grass, Leptochloa dubia were exposed to the scale. 912 J.A. Goolsby et al.

Figure 4. Picture of a field host range survey location in Spain with contiguous populations of the invasive Texas grass Leptochloa fusca ssp. uninervia (a species of concern from quarantine host range testing), rice, and Arundo donax infested with Rhizaspidiotus donacis.

Leptochloa dubia is naturalized in Spain and France. Seed was obtained in Europe and grown in pots. Twenty potted plants were transplanted into stands of A. donax in Villafranqueza, (Alicante), Spain (Figure 6). Plants were watered as needed from September 2008 to February 2009. During this time, several collections of scale were made from this site to determine if crawlers were being produced. Shipments of adult scale from Villafranqueza produced the following average numbers of crawlers per female: October 1, 2008, 0; October 9, 2008, 40; November 6, 2008, 66; and January 6, 2009, 100. Therefore, the L. dubia were exposed over several months to several cohorts of crawlers. All 20 plants were returned to US quarantine facilities on February 18, 2009 for dissection. Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010

Figure 5. Picture of a field host range survey location near Leucate (Perpignan), France with contiguous populations of Spartina foliosa infested with the armoured scale, Chortinaspis subterraneana growing adjacent to Arundo donax infested with Rhizaspidiotus donacis. Biocontrol Science and Technology 913

Figure 6. Leptochloa dubia potted plant in stand of Rhizaspidiotus donacis-infested Arundo donax for 6-month field host exposure test conducted at Villafranqueza, near Alicante, Spain.

Results and discussion Quarantine host range tests No choice tests Crawlers that did not settle on plant tissues died within 2Á3 days of release and thus were not expected to be observed at the time of plant dissection, 3Á4 months after release of 200 crawlers onto each plant. By this time, early second-instar scales (sex not determinable) were uncommon on Arundo donax (observed on five of 29 shoots with side stems), A. formosana and non-Arundo plants, and did not vary in abundance between plant species (F1.16, df4, 37, P0.34) (Table 1). Late second-instar females were also uncommon on A. donax (observed on four of 29 shoots), and did not differ in abundance between A. donax and the one non-Arundo plant on which they were observed, Cynodon dactylon (F0.02, df1,30, P0.902) (Table 1). Adult males (indicated by empty scale coverings) were significantly more abundant on A. donax than on any non-Arundo plant species (F10.85, df6,41, PB0.0001; P50.01 in all mean comparisons), while not differing from A. formosana (Table 1). Adult males were 2.5-fold more abundant on A. donax (316 adult males

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 found on 29 shoots) than on Spartina alterniflora (P0.014) (13 found on 3 shoots), and were 11Á33-times (1090Á3269%) less abundant on three Leptochloa spp. than on A. donax (Table 1) (P0.0011 for L. fusca ssp. uninervia, three adult males found on three shoots; P0.0072 for L. panicea ssp. brachiata, one adult male found on three shoots; P0.023 for L. virgata, one adult male found on two shoots). Live adult females, representing the most long-lasting and damaging scale stage, were found on only one non-Arundo species, Leptochloa virgata, with three adults found on two shoots. Average live adult female abundance per L. virgata plant was 13.8-times (1377%) lower than on A. donax, on which 599 adult females were found on 29 shoots (F26.55, df2, 31, PB0.0001; mean comparison P50.0002) (Table 1). Arundo donax was 6.9-fold higher than A. formosana in live adult female counts (Table 1). As an additional measure of development by females, counts of live and dead adult females were combined. Combined living and dead adult females were lo

914 J.A. Goolsby et al.

found on two Leptochloa species: L. fusca ssp. univervia (three dead females on one of three plants tested) and L. virgata (four dead adult females, in addition to the three live females noted earlier, on one of the two plants tested). Dead adult females were also found on Spartina alterniflora (20 across two of three plants). These values can be compared to A. donax, on which 669 live and dead adult females were found across 29 total plants. Average combined live and dead adult females per plant were 3.5-fold higher on A. donax than on Spartina alterniflora, 6.6-fold higher than on Leptochloa virgata, and 23-fold higher than on L. fusca ssp. uninervia (F28.35, df4,35, PB0.0001; mean comparison PB0.0001) (Table 1). Total live scales were significantly higher on A. donax than any other plant species (F37.07, df8, 44, PB0.0001) (Table 1). Forty of the 47 non-Arundo plant species (including three native genotypes of Phragmites australis) supported no R. donacis scales through any developmental stage. Total live scales on A. donax were 3-fold more abundant than on A. formosana, 7.6-fold more abundant than on Spartina alterniflora, 11-fold more abundant than on Chasmanthium latifolium, 16.6Á 25-fold more abundant than on Leptochloa spp., 55-fold more abundant than on Phragmites australis (exotic Rhode Island, USA genotype), and 100-fold more abundant than on Cynodon dactylon, all highly significant differences in mean comparisons (P50.0003).

High rate no-choice tests A follow-up no-choice test was performed involving A. donax from Laredo, TX, and the four non-Arundo plant species on which small numbers of R. donacis males and/ or females completed their immature development in prior host range tests. These species were further challenged by releasing 1000 crawlers on each plant. Early second-instar scales (F12.63, df1, 3, P0.038) and late second-instar females were encountered only on A. donax, with the exception of one early second-instar found on Leptochloa panicea ssp. brachiata (Table 2). The results for adult scales confirmed the prior general host range tests. Adult males developed on Leptochloa spp., but were at least 149-fold more abundant on A. donax than on the three Leptochloa grasses tested (F96.23, df3,6, PB0.0001; mean comparisons P5 0.0004) (Table 2). A total of five empty adult male scale covers were found on Leptochloa panicea ssp. brachiata, three on L. fusca ssp. univervia, and three on L. virgata (three plants tested per species), compared to 498 adult males found

Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 on two A. donax plants. No adult males emerged on Spartina alterniflora in this test (Table 2). Live adult females were found on Leptochloa virgata (10 on one of two plants), and on Spartina alterniflora (one on three plants), but average abundance per plant was 26 times (2580%) lower on L. virgata and over 100 times (38 780%) lower on S. alterniflora than on A. donax (F67.83, df2, 4, P0.0008) (Table 2), as 258 adult females were found on two A. donax plants. Combined live and dead adult females were found on Leptochloa fusca ssp. uninervia (two dead females on one of three plants tested), Leptochloa panicea ssp. brachiata (21 dead adult females on one of three plants), and Leptochloa virgata (three dead females, in addition to the 10 live females noted above, on one of two plants). All three Spartina alterniflora plants tested with 1000 crawlers had dead adult females, but in low numbers (one or two dead adult females per plant, plus the one live adult female noted above, total of five adult females found). Average combined living and dead adult female counts per Biocontrol Science and Technology 915

plant were at least 25-fold higher on A. donax than on any of these non-Arundo plant species (Table 2) (F119.7, df4,8, PB0.0001; mean comparison P  0.0002), as 354 total adult females were found across two A. donax plants. Across all life stages, live scales were at least 61-fold more abundant on A. donax than on the four non- Arundo species tested (F132.7, df4, 8, PB0.001) (Table 2). The minor development of R. donacis on Leptochloa does not fit a pattern of phylogenetic relatedness to A. donax. Leptochloa is in a separate subfamily of grasses (Chloridoideae). Within this subfamily is the tribe Cynodonteae, which includes many genera including Cynodon dactylon (Bermudagrass), Spartina spartinae (Gulf cordgrass) and Uniola paniculata (sea oats). No development was recorded on these species. In addition, no development was recorded on the more closely related Molinia caerulea (Moore Grass). Several very morphologically similar grasses were also tested and no development occurred. Survival and development of the Arundo scale on Spartina alterniflora and Leptochloa spp. was very low, less than 1% as compared to 43% development to the adult stage on A. donax. Mortality of crawlers under field conditions is likely to be much greater, thus further limiting the host range on R. donacis. To test this hypothesis field host range studies were conducted in Mediterranean Europe.

Field host range studies Field survey of non-targets in Mediterranean Europe Many hundreds of the non-target plant species of concern were collected and dissected in Europe. No R. donacis or any other diaspidid scales were observed on any Leptochloa fusca ssp. uninervia plants collected in Valencia, Sevilla or Tortosa (Figure 4). Conversely, R. donacis was common on A. donax at the above three sites. No R. donacis were observed on A. donax in the colder inland rice growing area of Merida/Badajoz where Leptochloa fasicularis was found. Therefore observations of L. fasicularis were not included in the field host range study. No R. donacis were observed on Spartina versicolor at El Saler (Valencia). This site was the most intact natural area on the Mediterranean coast, and the two species have been growing together for many thousands of years. Rhizaspidiotus donacis was common on all the A. donax stands in this natural area. In southeastern France near Leucate, two populations of Spartina foliosa were collected and examined one within 500 m and the second 6 cm of A. donax. Chortinaspis subterranea (Diaspidae) Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 individuals were collected from four of 11 stems at the second site, and heavy populations of R. donacis were observed on adjacent A. donax.NoR. donacis were observed on the S. foliosa. In addition, other grasses growing with A. donax identified as Agropyrum, Cynodon, Elymus, , Panicum, and Chloris, were sampled as available at the above locations in Spain. Ten to 30 of each species within 0.5 m of R. donacis populations were collected, dissected and evaluated. No R. donacis individuals were found on the above grass species.

Field host exposure test Twenty L. dubia plants were returned to quarantine facilities for dissection and inspection after six months in the field. The plants at this time were still green and 916 J.A. Goolsby et al.

healthy. Individual leaf blades and stems were separated and inspected for any evidence of R. donacis.NoR. donacis individuals of any life stage were detected. This indicates that despite repeated exposure to multiple cohorts of crawlers emanating from the adjacent A. donax, L. dubia was not a field host for the scale.

Conclusion Without biological control agents, we can be certain that A. donax will continue to cause major ecological damage throughout the warm temperate and subtropical regions of North America and potentially large parts of Central and South America with similar climates. To reduce the impact of this weed over the vast areas that are infested, biological control is needed. The results of these laboratory and field studies indicate that Rhizaspidiotus donacis is highly specific to Arundo. Very minor development was observed in quarantine tests only on common grasses Spartina alterniflora and Leptochloa spp. however, we did not observe development on any other non-target species. Development on Spartina alterniflora and Leptochloa spp. species was likely a quarantine artifact. Further testing at higher crawler infestation rates showed that mortality to the scale on Spartina and Leptochloa prior to adult development was greater than 99% under ideal quarantine conditions. Field surveys of the non-target species of concern and host exposures of potted Leptochloa plants in Europe confirmed that R. donacis is specific to Arundo under field conditions. Based on this information, we do not predict that any native or economic grasses will be at risk from R. donacis if released in North or South America.

Acknowledgements We wish to thank the following USDA-ARS/APHIS staff for technical support: Ann Vacek, Crystal Salinas, Bill Warfield, Reyes Garcia III, Amede Rubio, Matthew Rector, Albino Chavarria, Steven Rodriguez, Juan Garza, Andrew Parker, Tony Rodriguez, Daniel Rosas, Rupert Santos, and Alex Racelis. Thanks to Alex Gammon, Tim Cunningham, Eric McDonald and Mark Seagall, USDA-APHIS, Houston, TX for receiving and processing shipments. We also thank the following individuals for help collecting and shipping material from the native range: Europe, Dr Eduardo Galante, Gerhild Kirk, Arnaud Blanchet, Dominque Coutinot and Tim Widmer; Israel; Avinoam Danin and Dan Gerling; Algeria, Abida Zeddam; and Italy, Gaetano Campobasso (in memoriam). Downloaded By: [USDA National Agricultural Library] At: 15:14 6 January 2010 References Balachowsky, A.S. (1928), ‘Contribution a`l’e´tude des Coccoides de l’Afrique mineure (4e note) Nouvelle liste de Coccides nord-africaines avec description d’espe`ces nouvelles’, Bulletin de la Socie´te´ Entomologique de France, 14 (Nov. 1928), 273Á279. Balachowsky, A.S. (1930), ‘Contribution a l’e´tude des coccoides de France (3e note) Coccoides nouveaux ou peu connus de la faune de France’, Bulletin de la Socie´te´ Entomologique de France, 28 (May 1930), 178Á184. Balachowsky, A.S. (1932), ‘E´ tude biologique des coccides du bassin occidental de la Me´diterrane´e’, Encyclope´die Entomologique, XV P. Lechevalier & Fils, Paris, 214 pp. LXVII. Balachowsky, A.S. (1933), ‘Les coccides des Iles d’Hye`res (Contributio´nal’e´tude des coccids de France, 16e note)’, Annales de la Socie´te´ d’Histoire Naturelles de Toulon, 17, 78Á84. Balachowsky, A. (1935), ‘Les cochenilles d’Espagne’, Revue de Pathologie Ve´ge´tale et d’Entomologie Agricole de France, 22, 255Á269. Biocontrol Science and Technology 917

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