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Entomologist’s Monthly Magazine 151 : 0 –0
Five invasive mealybug species new for Ascension Island (Hemiptera: Pseudococcidae), with a revised checklist of scale insects for the island
BY CHRIS MALUMPHY, LIZA F. WHITE, JAYNE HALL, JENNIFER HODGETTS & MARTIN HAMILTON CM*, JH, JH: The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, U.K.; email: [email protected] MH: Royal Botanic Gardens, Kew, Richmond, Surrey. TW9 3AB, U.K. LW: Ascension Island Government, Georgetown, Ascension Island, ASCN IZZ Accepted: January 9th , 2015
ABSTRACT Five invasive mealybug species are recorded for the first time from Ascension Island: Antonina graminis (Maskell) was collected from Cyperus appendiculatus ; Chorizococcus rostellum (Lobdell) from Sporobolus caespitosus ; Dysmicoccus brevipes (Cockerell) from C. appendiculatus ; Phenacoccus solani Ferris from Euphorbia origanoides and Portulaca oleracea ; and Planococcus minor (Maskell) from E. origanoides . Two of these host plants, E. origanoides and S. caespitosus , are endemic to Ascension Island and classed as ‘Critically Endangered’ on the International Union for the Conservation of Nature (IUCN) Red List. The biology, host range, distribution and economic importance of these mealybugs are reviewed, and their potential impact discussed. An updated and revised checklist of scale insects of Ascension Island is presented in an appendix. Keywords: plant health, invasive species, biosecurity, UK Overseas Territory, South Atlantic
INTRODUCTION Ascension Island is a small (total area of 97 km 2), geologically young (1 million years), extremely isolated, volcanic island located in the equatorial waters of the South Atlantic Ocean (7º56′S, 14º22′W), approximately 1,600km from the coast of Africa and 2,250km from the coast of South America. It is governed as part of the UK Overseas Territory (UKOT) of Saint Helena, Ascension and Tristan da Cunha. During the 19th Century many species of plants, including tropical and European crops, were introduced to Ascension Island from the Royal Botanic Gardens, Kew, UK (Kew), and Cape Town, South Africa. Approximately 300 species of vascular plants were introduced, both deliberately and accidently (Cronk, 1980), which eventually dominated most of the island’s native plant communities. Inevitably, invasive plant pests were introduced along with their host plants. Colonisation of the island by non-native plants and animals pushed some of the endemic species, such as Oldenlandia adscensionis (DC.) Cronk, to extinction (Lambdon et al ., 2012b). Some species previously thought to be extinct, have been rediscovered during recent botanical surveys; for example, the Ascension Island parsley fern Anogramma ascensionis (Hook.) Diels was rediscovered in 2009 growing on unstable cliff faces (Lambdon et al ., 2010). Scale insects (Hemiptera: Coccoidea) are one of the most commonly transported groups of arthropods in international plant trade and among the most successful
*corresponding author 3746_Layout 1 26/02/2015 17:40 Page 2
0 Entomologist’s Monthly Magazine (2015) Vol. 151 invasive groups of insects (Miller & Miller, 2003; Pellizzari & Dalla Montá, 1997; Smith et al ., 2007; Thomas, 2006). In recent decades several species of mealybug (Peudococcidae) have proved highly invasive in tropical and subtropical areas resulting in detrimental impacts to agriculture, horticulture and the environment. Examples include: pink hibiscus mealybug Maconellicoccus hirsutus (Green), which has spread from Asia to Africa and the Americas (Williams, 1986; 1996); papaya mealybug Paracoccus marginatus Williams & Granara de Willink, which has spread from the Neotropics to West Africa, Asia and the Pacific region (Muniappan et al ., 2008); bougainvillea mealybug Phenacoccus peruvianus Granara de Willink, which has spread from South America to the Mediterranean (Beltrà et al ., 2010); and solenopsis mealybug Phenacoccus solenopsis Tinsley, which has spread widely in the Neotropical Region, and to Africa, Asia and Australia (Ben- Dov, 2014; Hodgson et al ., 2008). The scale insect fauna of Ascension Island was reviewed by Ashmole & Ashmole (1997) and Williams & Mendel (2007), resulting in 19 exotic species being recorded, including three species of mealybug. Collecting by the fifth author during 2007 and second author during 2013 revealed the presence of five species of mealybug new for Ascension Island. The purpose of this communication is threefold: to provide collection details for the invasive mealybug species new to Ascension Island; to review the biology, host range, distribution and economic importance of these mealybugs; and to discuss their potential impact to the island. A revised and updated checklist of the 24 scale insects now known to occur in Ascension Island is presented in Appendix 1.
METHODS A botanical survey of Ascension Island by Kew during 2007 discovered stressed and dead plants in the wild, and in cultivation at the Ascension Island Government conservation nurseries. Samples of scale insects were collected by the fifth author from endemic plants as part of this survey. Further samples of scale insects were collected during 2013 by the second author from endemic and introduced plants, as part of the Overseas Territories Environment Programme (OTEP) funded project: An Ecosystem Approach to Plant Conservation on Ascension Island. All of the samples were preserved in ethanol and submitted to The Food and Environment Research Agency (FERA), UK, where they were slide-mounted according to the procedures published by Malumphy (2002), and identified by the first author using diagnostic keys provided by Cox (1989), Granara de Willink (2003; 2009), Granara de Willink & Szumik (2007), Williams (1985; 2004), Williams & Granara de Willink (1992), and Williams & Watson (1988). Slide-mounted voucher specimens were deposited at FERA.
RESULTS Ten species of scale insect were identified in the samples collected in 2007 and 2013, including five species of mealybug recorded for the first time for Ascension Island. A summary of the distribution, host range, and economic importance of the new mealybugs is provided below. Detailed information on all the species of scale insect recorded from the island can be obtained from an online catalogue ScaleNet (http://www.sel.barc.usda.gov/scalenet/scalenet.htm). 3746_Layout 1 26/02/2015 17:40 Page 3
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MEALYBUGS NEW FOR ASCENSION ISLAND Antonina graminis (Maskell) – Rhodes grass mealybug Of Asiatic origin, A. graminis is a highly successful coloniser that has spread widely in the tropics and subtropics (Ben-Dov, 2014). It is parthenogenetic, ovoviviparous, and may have up to five generations a year, depending on climatic conditions. It is oligophagous on grasses (rarely on bamboo) (Poaceae), and has been recorded feeding on more than 50 grass genera (Hendricks & Kosztarab, 1999; Ben-Dov, 2014). It is a pest of pasture and turf grass and the most severe damage appears to be caused to Rhodes grass Chloris gayana . Infested plants turn brown and may die. It is an occasional pest of Bermuda grass C. dactylon , sugarcane Saccharum officinarum , Johnson grass Sorghum halepense , and St. Augustine grass Stenotaphrum secundatum . Collection data . Razor’s Edge (N: 0576065; E: 9122015): three adult females hidden at the base of the leaves of wild populations of Cyperus appendiculatus (Cyperaceae), 7.xi.2013, leg. C. Supple & L.F. White. Chorizococcus rostellum (Lobdell) – Bermuda grass mealybug Chorizococcus rostellum is suspected to be native to the Americas (Williams & Granara de Willink, 1992) and has spread to southern and Central Europe, South Africa, Australia and Hawaii. It is oligophagous on Poaceae, and occasionally found on herbaceous plants and other non-grass hosts (Ben-Dov, 2013). It is very common on numerous grass species, particularly Bermuda Grass Cynodon dactylon in the southern USA, and has been found on sugarcane in Hawaii (Beardsley, 1960), but has not been reported to be an economic pest. Collection data. Conservation Department’s Green Mountain conservation nursery: on Sporobolus caespitosus (Poaceae), 25.x.2007, leg. M. Hamilton. Dysmicoccus brevipes (Cockerell) – pineapple mealybug This species originated in tropical America (Rohrbach et al ., 1988) and has spread to all zoogeographical regions, mainly in the tropics and subtropics (CIE, 1972; Ben-Dov, 1994). It is broadly polyphagous, feeding on plants belonging to at least 63 families, with a preference for Arecaceae, Bromeliaceae, Cyperaceae, Fabaceae, Poaceae and Rubiaceae. It is a major economic pest of pineapple on which it transmits the Pineapple Mealybug Wilt Disease . Other crops affected include avocado, banana, celery, citrus, clover, cocoa, coconut, coffee, cotton, custard apple, figs, ginger, guava, maize, mango, oil palm, orchids, groundnut, peppers, pineapple, plantain, potato and sugarcane. Collection data . There were large numbers of mealybugs present in each of these samples. North East Bay Road: project site (N: 0572828; E: 9124167), on C. appendiculatus , 7.x.2013, leg. L.F. White. Razor’s Edge (N: 0576065; E: 9122015): on C. appendiculatus , 7.xi.2013, leg. C. Supple & L.F. White. White Horse Hill, Restoration Site (N: 0575843; E: 9121367): on C. appendiculatus, 12.ix.2013, leg. L.F. White. Phenacoccus solani Ferris – solanum mealybug This species is native to North America, and in recent years has spread widely throughout the tropical and subtropical parts of South and Central America, Caribbean, Africa, Asia, Australasia and Pacific. It is polyphagous, feeding on plants belonging to at least 31 families, with a preference for Asteraceae and Solanaceae. It is recorded as a pest of stored potato tubers in the USA, tobacco in Zimbabwe, Festuca forage crops in Iran, and as a major pest of tropical foliage plants in Florida. 3746_Layout 1 26/02/2015 17:40 Page 4
0 Entomologist’s Monthly Magazine (2015) Vol. 151 It is also recorded causing symptoms similar to damping-off to young Emilia and Portulaca oleracea plants in Hawaii, and large colonies can cause mature plants to collapse. Collection data. There were large numbers of mealybugs present in each of these samples and they were occasionally found feeding on the roots. North East Bay Road, project site (N: 0572828; E: 9124167): on Euphorbia origanoides (Euphorbiaceae) , 7.x.2013 and 10.x.2013, leg. L.F. White (attended by big-headed ant Pheidole megacephala (F.) (Hymenoptera: Formicidae)). White Horse Hill, Restoration Site (N: 0575843; E: 9121367): on E. origanoides and P. oleracea (Portucalaceae) , 12.ix.2013 , leg. L.F. White . Hummock Point, nursery (N: 0574053; E: 9124509): on E. origanoides , 4.xi.2013, leg. L. F. White . South Gannet Hill, project site (N: 0566703; E: 9118074): on E. origanoides , 1.xi.2013, leg. C. Supple & L.F. White . Mars Bay Flats (N: 0564710; E: 9123441): on E. origanoides, 1.xi.2013, leg. C. Supple & L.F. White. Comfortless Cove, Restoration Site (N: 0565958; E: 9125350): on E. origanoides, 11.ix.2013, leg. L.F. White. Planococcus minor (Maskell) – passionvine mealybug The origin of P. minor is unclear as it occurs widely in tropical and subtropical regions, with the exception of Africa. It is highly invasive and common on islands in the Caribbean, South Pacific, Indian Ocean and North Atlantic. Its full distribution (e.g., in Africa) is unclear due to confusion with the closely related cosmopolitan species P. citri . Planococcus minor is polyphagous, recorded feeding on more than 250 wild and cultivated host plants in nearly 80 families, including many important agricultural crops such as banana, citrus, cocoa, coffee, corn, grape, mango, potato and soybean (Stocks & Roda, 2011). However, although it has been recorded feeding on a wide range of plants, it is likely to be damaging only to a small selection of preferred hosts. It is a vector of Banana Streak Virus (Gloria Gonzalez et al ., 2002). Planococcus minor is morphologically very similar to the citrus mealybug Planococcus citri (Risso) and is frequently misidentified due to similarities in appearance, host range, and distribution (Williams & Granara de Willink, 1992). A morphological scoring matrix based on six diagnostic characters is used to distinguish these cryptic species, relying on a point scoring system to identify adult females (Cox, 1983). An attempt to confirm the identity of the Planococcus from Ascension Island using molecular data was made at FERA. Partial cytochrome oxidase I (COI) gene sequences were generated from five specimens of the putative ‘P. minor ’. The sequence from all specimens was identical and compared with sequences held at the National Centre for Biotechnology Information (NCBI). Similarity searches with the sample reveal a 99% match to P. minor , however, there was also a 98% match with P. citri . As P. minor was not always distinguished from P. citri in the past, it is possible that some published sequences were generated from misidentified specimens; a probable cause of the apparent degree of sequence similarity between the two species. Although identifying the mealybugs from the sequence data was inconclusive, results indicate that the specimens were more likely to be P. minor than P. citri . Collection data. North East Bay Road, project site (N: 0572828; E: 9124167): on Euphorbia origanoides, 7.x.2013, leg. L. F. White. Conservation Department’s Chicken Run conservation nursery: on Euphorbia origanoides (Poaceae), 25.x.2007, leg. M. Hamilton.
OBSERVATIONS ON OTHER SCALE INSECTS Five species previously recorded from Ascension Island were also collected in the 2007 and 2013 surveys (see Appendix 1 for references): 3746_Layout 1 26/02/2015 17:40 Page 5
Entomologist’s Monthly Magazine (2015) Vol. 151 0 Coccus hesperidum Linnaeus – soft brown scale (Coccidae) Collection data. North East Bay Area, near Project Site (N: 0572828; E: 9124167): on Psidium guajava (Mrytaceae), 4.xi.2013, leg. C. Supple & L.F. White. Ferrisia malvastra (McDaniel) (Pseudococcidae) Collection data. North East Bay Road, project site (N: 0572828; E: 9124167): collected from the roots of E. origanoides , 10.x.2013, leg. L.F. White. Hemiberlesia lataniae (Signoret) – latania scale (Diaspididae) Collection data . Comfortless Cove, Restoration Site (N: 0565965; E: 9125401): on E. origanoides, 11.ix.2013, leg. L.F. White. North East Bay Area, near Project Site (N: 0572828; E: 9124167): on P. guajava , 4.xi.2013, leg. C. Supple & L.F. White; large populations of scales on E. origanoides, 7.x.2013 and 10.x.2013, leg. L.F. White. Insignorthezia insignis (Browne) – Kew bug or Jacaranda bug (Ortheziidae) Collection data . NASA Road (N: 0572842; E: 9120235): on Tecoma stans (Bignoniaceae), 8.xi.2013, leg. C. Supple & L.F. White. Upper Nasa Road: on Vitex triflora (Lamiaceae), 20.ix.2013, leg. L.F. White. Pinnaspis strachani (Cooley) – lesser snow scale (Diaspididae) Collection data . Comfortless Cove, Restoration Site (N: 0565965; E: 9125401): on E. origanoides, 11.ix.2013, leg. L.F. White.
DISCUSSION Ten species of scale insects were collected from Ascension Island during 2007 and 2013; remarkably half of these (all mealybugs) were new to the island. All of these species must have been introduced by anthropogenic activities as mealybugs have a low natural dispersal potential (adult females are wingless) and the island is extremely remote. Two of the mealybug species ( D. brevipes and P. minor ) are important economic pests of tropical and subtropical crops, and could potentially have an economic impact in Ascension Island. These mealybugs can lower plant or fruit quality, stunt growth, cause discoloration and premature leaf loss, and reduce yield. Both of these species are vectors of plant viral diseases and even low density populations can therefore have an economic impact. Mealybugs excrete copious amounts of honeydew onto the plant which serves as a medium for the growth of sooty moulds which build up on the leaves, fruits and other plant parts. The mould can cover so much area that it interferes with the plant’s normal photosynthetic activity (Williams & Granara de Willink, 1992). Honeydew and sooty mould also cause cosmetic defects to plants and fruits, lowering their market value. Phenacoccus solani also has the potential for an economic impact to crops, but less is known about this species as it has only developed into an economic pest relatively recently. Three of the mealybug species could potentially have a significant environmental impact as they were found feeding on endemic plants classed as ‘Critically Endangered’ on the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species (http://www.iucnredlist.org): C. rostellum on S. caespitosus ; and P. solani and P. minor on E. origanoides . Euphorbia origanoides , commonly known as Ascension spurge, is a small, perennial shrub that grows at low elevations in the driest areas of the island. It is ‘critically endangered’ due to its extremely restricted range, declining population, and threats to its survival from introduced vegetation, grazing and pest insects (Gray et al ., 2012). Six species of exotic scale insect have been recorded feeding on E. origanoides on Ascension Island ( F. malvastra, H. lataniae, Icerya purchasi (Maskell) (Monoplebiidae) , P. 3746_Layout 1 26/02/2015 17:40 Page 6
0 Entomologist’s Monthly Magazine (2015) Vol. 151 solani, P. minor and P. strachani ); two of the species ( F. malvastra and P. solani ) may occur on roots, and are likely to be under-recorded. Sporobolus caespitosus is a perennial grass known only from two locations 600m above sea level, Green Mountain and Weather Post, where it occupies an area of less than 1km². It inhabits vertical and sloping cinder banks and is adapted to the exposed conditions found at these sites. It is ‘critically endangered’ due to its extremely restricted range and threats to its survival from introduced vegetation, grazing and habitat loss (Lambdon et al ., 2012a). The polyphagy of most of the mealybug species new for Ascension Island is likely to enable them to utilize additional new hosts, including other endemic plants on the island. Several non-native introduced species of scale insect have already had a serious impact in Ascension Island, most notably cottony cushion scale ( I. purchasi ) and ensign scale ( I. insignis ) (Ashmole & Ashmole, 2000). Cottony cushion scale caused serious damage to many trees and shrubs in the 1970s, and in 1976 the coccinellid Rodlia cardinalis (Mulsant) (Coccinelidae) was introduced to control the scale. Williams & Mendel (2003) reported that E. origanoides suffered badly with infestations of I. purchasi at Cross Hill. The ensign scale was introduced to Ascension Island in the 1980s and is causing substantial damage to the introduced Lantana camara (Ashmole & Ashmole, 2000). The five non-native mealybug species recorded here for the first time from Ascension Island have the potential to impact negatively the rich biodiversity of the island. Monitoring the mealybug populations and the impact they are having, particularly to endemic plants, is advisable for the future.
ACKNOWLEDGEMENTS Stedson Stroud of the Ascension Island Conservation Department must be thanked for assistance in the field accessing populations of threatened species and collecting samples for identification. His in-depth knowledge of the island and its biodiversity are unrivalled. Stedson’s determination and dedication have undoubtedly helped save many species from extinction. Natasha Williams of the Ascension Island Government Conservation Department (AIGCD) provided assistance in accessing population data and locality information. Ascension Island Government made the visit by Martin Hamilton possible through permission to visit and enabled material to be sent for identification through export permits. Catherine Supple and Jolene Sim of the AIGCD assisted Liza White with the surveys. Conservation work carried out in the Island was funded by the Overseas Territories Environment Programme (OTEP) and the Darwin Initiative (project 19–026). The identification of the scale insect samples was funded by the UK Department of Environment Food and Rural Affairs (Defra), Biodiversity Programme.
REFERENCES Ashmole, N.P. & Ashmole, M.J. , 1997, The land fauna of Ascension Island: new data from cave and lava flows, and a reconstruction of the prehistoric ecosystem, Journal of Biogeography , 24 : 549– 589. Beltrà , A., Soto , A., Germain , J.F., Matile-Ferrero, D., Mazzeo, G., Pellizzari , G., Russo, A., Franco, J.C. & Williams, D.J. , 2010, The Bougainvillea mealybug Phenacoccus peruvianus , a rapid invader from South America to Europe, Entomologica Hellenica , 19 : 137–143. Ben-Dov, Y., 2014, Pseudococcidae, ScaleNet, http://www.sel.barc.usda.gov/scalenet/scalenet.htm [accessed 1st December 2014]. 3746_Layout 1 26/02/2015 17:40 Page 7
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Cox , J.M. , 1989, The mealybug genus Planococcus (Homoptera: Pseudococcidae), Bulletin British Museum (Natural History). Entomology, 58 : 1–78. Cronk, Q.C.B. , 1980, Extinction and survival in the endemic vascular flora of Ascension Island, Biological Conservation , 17 : 207–219. Gloria Gonzalez, A., Caridad, F. & Miranda, E. , 2002, Planococcus minor Markell, vector del virus Estriado del Platano BSV, Fitosanidad , 62 : 47–48. Granara de Willink, M.C. , 2003, Nuevas especies de Chorizococcus de la Argentina y Uruguay (Hemiptera: Pseudococcidae), Revista de la Sociedad Entomológica Argentina , 62 (3/4): 83–88. ——— 2009, Dysmicoccus de la Región Neotropical (Hemiptera: Pseudococcidae), Revista de la Sociedad Entomológica Argentina , 68 (1–2): 11–95. Granara de Willink, M.C. & Szumik, C. , 2007, Phenacoccinae de Centro y Sudamérica (Hemiptera: Coccoidea: Pseudococcidae): Sistemática y Filogenia, Revista de la Sociedad Entomológica Argentina , 66 (1–2): 29–129. Gray, A., Stroud, S., Lambdon, P.W., Nissalo, M. & Renshaw, O., 2012, Euphorbia origanoides . In : IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. Hendricks, H. & Kosztarab, M., 1999, Revision of the Tribe Serrolecaniini (Homoptera: Pseudococcidae) , de Gruyter, Berlin & New York. xiv + 213 pp. Hodgson, C.J., Abbas, G., Arif, M.J., Saeed, S. & Karar, H. , 2008, Phenacoccus solenopsis Tinsley (Sternorrhyncha: Coccoidea: Pseudococcidae), a new invasive species attacking cotton in Pakistan and India, with a discussion on seasonal morphological variation, Zootaxa, 1913 : 1–33. Lambdon, P.W., Stroud, S., Gray, A., Niissalo, M., Renshaw, O. & Sarasan, V. , 2010, Anogramma ascensionis . In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1.
0 Entomologist’s Monthly Magazine (2015) Vol. 151 Appendix 1 CHECKLIST OF SCALE INSECTS (HEMIPTERA: COCCOIDEA) RECORDED FROM ASCENSION ISLAND
SCALE INSECT FAMILY Species References COCCIDAE Coccus hesperidum Linnaeus Williams & Mendel, 2007 Coccus longulus (Douglas) Ashmole & Ashmole, 1997 Coccus viridis (Green) Ashmole & Ashmole, 1997 Parasaissetia nigra (Nietner) Ashmole & Ashmole, 1997; Williams & Mendel, 2007 Pulvinaria psidii Maskell CABI, 1994; Williams & Mendel, 2007 Pulvinaria urbicola Cockerell Williams & Mendel, 2007 Saissetia coffeae (Walker) Williams & Mendel, 2007 DIASPIDIDAE Clavaspis herculeana (Cockerell & Hadden) Williams & Mendel, 2007 Diaspis echinocacti (Bouché) Williams & Mendel, 2007 Hemiberlesia lataniae (Signoret) Williams & Mendel, 2007 Lepidosaphes beckii (Newman) Ashmole & Ashmole, 1997 Lopholeucaspis cockerelli (Charmoy) Williams & Mendel, 2007 Pinnaspis strachani (Cooley) Williams & Mendel, 2007 ERIOCOCCIDAE Eriococcus araucariae Maskell Williams & Mendel, 2007 MONOPLEBIIDAE Icerya purchasi Maskell Ashmole & Ashmole, 1997; Williams & Mendel, 2007 PSEUDOCOCCIDAE Antonina graminis (Maskell) Reported here Chorizococcus rostellum (Lobdell) Reported here Dysmicoccus brevipes (Cockerell) Reported here Ferrisia malvastra (McDaniel) Williams & Mendel, 2007 Paracoccus burnerae (Brain) Malumphy, 1993; Williams & Mendel, 2007 Phenacoccus solani Ferris Reported here Planococcus minor (Maskell) Reported here Pseudococcus cryptus Hempel Williams & Mendel, 2007 ORTHEZIIDAE Insignorthezia insignis (Browne) Ashmole & Ashmole, 1997; Williams & Mendel, 2007