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Worldwide Biological Control of Arthropods from a Pacific Perspective

Worldwide Biological Control of Arthropods from a Pacific Perspective

Worldwide Biological Control of from a Pacific Perspective

Ross H. Miller Western Pacific Tropical Research Center University of Guam Characteristics of Many Small Pacific Islands

• Small in area • Tropical or subtropical climate • Relatively low plant & richness • Highly vulnerable to • Fragile and moderately resilient ecosystems • Relatively low fresh water supplies - fresh water lens and/or runoff from high islands • Subject to frequent tropical storms and typhoons • Small farms: many < 5 ha • Low GDP & per capita income – limited or no internal funds for BC exploration, quarantine, follow-up • Limited or no BC quarantine facilities • Limited expertise or capacity for BC • Varying access to technical expertise, training, capacity building • Limited and expensive transportation – for people or BC agents • Island groups organized into coalitions or federations; Often associated with a dominant regional power • Major industry – varies: fishing, tourism, agriculture, military Guam’s Agricultural Community

•Small family plots < 5 ha •Retirees – supplemental income •Subsistence farmers – immigrants •Relatively few commercial farmers - generally small scale compared to mainland •Golf courses – hotels/resorts •Small but vocal •Politically connected and very active •Very supportive of agriculture activities •Guardians of “traditional” cultural values E 90

120 Feb 60 DecJan Mar SE Nov Apr NE May Jun 150 30

Jul Oct

Direction Degrees Direction Aug Sep S 180 0 N 14 12 10 8 6 4 2 0 2 4 6 8 10 12 14 Wind Speed (m/s) Wind Speed (m/s)

60 40 Wind:Mean Rainfall Speed 1945-1997 and Direction

Temperature 1945-1997 35 50

30 40 25

30 20

Rainfall (cm) Rainfall 15 20 C Temperature 10 10 5

0 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 5. Rainfall and temperature data for Guam. Probability: Tropical Cyclone Within 180 Miles of Guam

Month Tropical Storm Typhoon January 1 every 15 years 1 every 15 years February 1 every 46 years 1 every 46 years March 1 every 46 years 1 every 46 years April 1 every 23 years 1 every 12 years May 1 every 23 years 1 every 9 years June 1 every 8 years 1 every 46 years July 1 every 4 years 1 every 23 years August 1 every 3 years 1 every 23 years September 1 every 2 years 1 every 8 years October 1 every 2 years 1 every 6 years November 1 every 2 years 1 every 7 years December 1 every 7 years 1 every 8 years Year 2.5 every 1 year 1 every 1 year

Probability of a Significant Storm Striking the Western Pacific Increases During El Nino Year (ie. Now) Obstacles to Biological Control in Small Pacific Islands • Annual Typhoons and Tropical Storms • High Pesticide Use on Small-Area Farms • Farmer community unaware of Biological Control • BC Obstructionists – anti Biological Control individuals or agencies - “I’ll do what I want types”

Opportunities for Biological Control in Small Pacific Islands

• Insular environment • Relatively simple species complexes • Nearly all species are exotic invasive species • Streamlined local permitting process The World’s Least Wanted

IUCN–The World Conservation Union recently released a list titled 100 of the World’s Worst Invasive Alien Species. Among the invertebrates included are these 14 now in North America. Argentine (Linepithema humile) Asian longhorned beetle (Anoplophora glabripennis) Asian tiger mosquito (Aedes albopictus) Big-headed ant ( megacephala) Common malaria mosquito (Anopheles quadrimaculatus) Common (Vespula vulgaris) Crazy ant (Anoplolepis gracilipes) Cypress ( cupressi) Formosan subterranean (Coptotermes formosanus shiraki) Gypsy moth (Lymantria dispar) Khapra beetle (Trogoderma granarium) Little (Wasmannia auropunctata) (Solenopsis invicta) Sweet potato (Bemisia tabaci) CTAHR University of Cooperative Extension Two Pacific BC Activities Based on Prior/Ongoing US BC Programs

Aphid Biological Control – Guam, CNMI, Palau: Outgrowth of Russian wheat aphid BC in western US using aphidiids collected worldwide and released in US

Papaya Biological Control – Guam, Palau: Based on APHIS BC project for and Caribbean using obtained via APHIS from Island surveys, quarantine introduction, mass rearing, release, follow-up Guam Releases: > 10 K aphidiids A. colemani A. gossypii (Chilean strain) T. citricida Recovered A. craccivora P. nigronervosa D. rapae A. gossypii ( state strain) T. citricida Recovered A. craccivora P. nigronervosa L. testaceipes A. gossypii (Oklahoma 1970’s) T. citricida Established on Guam A. craccivora P. nigronervosa A. gossypii A. colemani (introduced) Saipan A. craccivora D. rapae (introduced & recovered) P. nigronervosa L. testaceipes (introduced) T. citricida A. gossypii A. colemani (introduced) Tinian A. craccivora D. rapae (introduced) P. nigronervosa L. testaceipes (introduced) T. citricida A. gossypii A. colemani (introduced) Rota A. craccivora D. rapae (introduced) P. nigronervosa L. testaceipes (self introduced; T. Citricida established and spreading)

•, P. nigronervosa, A. craccivora No parasitoids

Palau •Guam reared L. testaceipes released against A. gossypii in Koror and Babeldaup

•Follow-up surveys indicate it is not yet established To Date: no significant control of aphids by aphidiids in Micronesia Why???????

Micro-satellite and COx1 barcoding of aphid collections worldwide Based on primers developed for apple aphid in Canada – Aphis pomi

Aphis gossypii – collection of distinct

Pentalonia nigronervosa – 2 distinct species P. nigronervosa – banana, taro (rarely) P. caladii – elevation of forma “caladii” to full species status (ginger, taro, others) Canonical Discriminant Analysis Ordination of A. gossypii from Guam on three hosts

Axis 2 contrasts between: Lengths of terminal process, tibia and siphunculus vs Lengths of rostrum, tarsus, and widths of appendages Scaevola

cucumber Axis 2 Axis taro

Axis1: contrasts between: Lengths of terminal process, setae, tibia and tarsus vs Lengths of siphunculus, rostrum, Axis 1 and antennal segment 5 1% COx1 Barcoding Data

COx1 sequence divergence among A. gossypii samples much less than } among diverse Aphis species.

Seq class 2 (on taro (+1 on melon)) } Seq class 8 (on Scaevola)

} Other frangulae group species soybean aphid Musa | USA: Florida (CNC#HEM056689, CNC#HEM057951) Musa | Guam (CNC#HEM050440, CNC#HEM050586, CNC#HEM050454, CNC#HEM050645, CNC#HEM050588, CNC#HEM050597, CNC#HEM050645, Pentalonia nigronervosa CNC#HEM054616, CNC#HEM057382, CNC#HEM057383, CNC#HEM057384, CNC#HEM057385, CNC#HEM057386, CNC#HEM057387, CNC#HEM057390,

Musa | CNMI: Tinian (CNC#HEM050482, CNC#HEM051909) Musa | Micronesia: Yap (CNC#HEM055095)

Musa | Micronesia: Kosrae (CNC#HEM051969, CNC#HEM051972)

Musa | Micronesia: Pohnpei (CNC#HEM057836, CNC#HEM057837, CNC#HEM057838)

Heliconia | Guam (CNC#HEM057389 Zingiber | CNMI: Rota (CNC#HEM050476, CNC#HEM050476.2)

Heliconia | Micronesia: Pohnpei (CNC#HEM057831) Cyrtosperma | Micronesia: .Pohnpei (CNC#HEM057827, CNC#HEM057828, , CNC#HEM057832, CNC#HEM057833) Colocasia esculenta | Micronesia: .Pohnpei (CNC#HEM057834) Alpinia | Micronesia.Pohnpei (CNC#HEM051824, CNC#HEM057825)

Musa | Micronesia: Pohnpei (CNC#HEM057826)

Zingiber | Micronesia: Pohnpei (CNC#HEM054529)

Alpinia | Guam (CNC#HEM057388)

Zingiber | Guam (CNC#HEM050456, CNC#HEM052080, CNC#HEM054584)

Zingiber | CNMI: Rota (CNC#HEM050473)

Hedychium | USA: Florida (CNC#HEM057500) Colocasia esculenta | Palau (CNC#HEM051902) Zingiber | Palau (CNC#HEM050519) Musa | Palau (CNC#HEM050520)

Hedychium coronarium | USA: Hawai (CNC#HEM051881, CNC#HEM058112, CNC#HEM058125)

Alpinia purpurata | USA: Hawai (CNC#HEM051823, CNC#HEM058113

Colcassia esculenta | USA: Hawai (CNC#HEM051862, CNC#HEM057377, CNC#HEM057379, CNC#HEM057381) Pentalonia caladii Zingiber | USA: Hawaii (CNC#HEM051859, CNC#HEM051894) Alpinia purpurata (USA: .Hawaii (CNC#HEM051823, CNC#HEM058113) Colocasia esculenta | USA: Hawaii (CNC#HEM058109)

1 % Papaya Mealybug - Paracoccus marginatus

On Papaya

On Plumeria

On Hibiscus Papaya Mealybug (PPMB)

•First described in 1992 from Florida & Caribbean •First reported in St. Martin 1995 •Spread to 13 Caribbean countries, 3 Central American countries, 3 South American countries, and Florida in US

USDA & Mexico Collectors Apoanagyrus nr. californicus •Initially screened by USDA-ARS in Delaware Anagyrus loecki •Env. Impact Assmt. performed by USDA-APHIS Acerophagous papayae •Mass reared in Puerto Rico (collaboration between Pseudaphycus sp. USDA & PR Dept. Agric.) Pseudleptomastix mexicana •Released in Dominican Republic, Puerto Rico, Florida

PPMB Established on Guam 2002, Palau 2003, Hawaii 2004 •Guam – Release of 46,200 BC agents, monthly for 5 months; pre & post Typhoon Chataan – 99% population reduction •Palau - Release of 24,568 BC agents; PPMB not detectable after 6 months

•Pseudoleptomastix mexicana •Acerophagus papayae •Anagyrus sp. Has Become a Model for Transfer of Classical Biological Control Between Caribbean and Pacific Basins Meyerdirk et al. 2004 Red Imported Fire Ant Solenopsis invicta

Photo; S. Porter •From Paraguay River drainage in South America (Brazil, Argentina, Paraguay) •Sting produces pustule •Monogyne or polygyne colonies •Exotic in Southern US, Caribbean, Australia, New Zealand, Taiwan Potential World Distribution of Solenopsis invicta based on Temperature & Precipitation*

Red = can survive White = unlikely Light green = sufficient rainfall Olive brown = insufficient rain Yellow = possible Location Specific Management Information From Global Invasive Species Database http://www.issg.org/database/species/management_info.asp?si=77&fr=1&sts=&lang=EN

Alabama ( (USA)) (United States (USA)) Arkansas (United States (USA)) Luchuan County (China) Auckland Region (New Zealand) (China) Australia tramp Mississippi (United States (USA)) Beiliu (China) (United States (USA)) (United States (USA)) (United States (USA)) Cayman Brac () Oklahoma (United States (USA)) China (Australia) Dayongqiao Park (China) Shanghang County (China) Dengta Town (China) (China) Dianbai County (China) South Carolina (United States (USA)) Dongguang (China) (United States (USA)) Florida (USA) (United States (USA)) (United States (USA)) (China) Wuchuan (China) (USA) (United States (USA)) (China) Grand Cayman (Cayman Islands) Yongxin District (China) (China) (China) Lianping County (China) (China) Little Cayman (Cayman Islands) Longyan (China) Phorid Fly decapitates RIFA after moving into head to pupate

Adult fly emerges from head

RIFA Porter & Morrison USDA-ARS, Gainesville FL Estimate that each Solenopsis species may have up to 6 Phorid species ( sp.) that attack it; Solenopsis populations generally low in home range of South and Central America due to natural enemies.

P. tricuspis & P. curvatus released in SE US in 1997, now covers 8,100 km2 in Florida

S. invicta S. richteri

RIFA threat to Pacific Islands, also S. richteri (black fire ant)

Solenopsis geminata already present and ubiquitous; dominant ant in disturbed habitats in Micronesia; may be amenable to BC Solenopsis geminata

– Tropical fire ant-() – Highest number of collections – Found with 7 aphid species – Native: Neotropics Solenopsis geminata

From Taber 2000 No Active Biocontrol Programs for S. geminata that I am Aware of, but the Potential is There. Other Invasive Ants to be Concerned About

Yellow crazy ant Bigheaded ant Ghost ant Anoplolepis gracilipes Pheidole megacephala melanocephalum

Little fire ant Whitefooted ant Wasmannia auropunctata Technomyrmex albipes Linepithema humule Many Other Activities Worldwide

1 Adelges tsugae Annand hemlock eastern Evans, 2002; Cheah and McClure, 1998; (hemlock woolly adelgid) McClure et al., 2000; Lu and Montgomery, 2001; Montgomery et al., 2002; Zilahi-Balogh et al., 2002, 2003 2 Agrilus planipennis ash Agents confirmed Bauer et al., 2007 (emerald ash borer) established and impact Classical Biological Control for being evaluated 3 Aulacaspis yasumatsui cycads Guam; control effective only Ross Miller and Aubrey Moore (pers. com.) the Protection of Natural (cycad scale) on mature plants, not seedlings 4 Cinara cupressivora East/South Africa Ecosystems: Past Achievements (cypress aphid) 1- control due to several factors and Current Efforts 5 Ceroplastes ceriferus diverse plants Queensland, Wilson, 1960; Waterhouse and Sands, 2001 (Indian wax scale) Van Driesche et al. (almost in press) 1-fortuitous biocontrol from another targeted scale 6 Ceroplastes destructor diverse plants Queensland, Sands et al., 1986 (white wax scale) 7 Ceroplastes rubens (pink diverse plants Queensland, Waterhouse and Sands, 2001 wax scale) 1-controlled on some native hosts but not others 8 Coleophora laricella larch North America Webb and Quednau, 1971; Ryan, 1990; (larch case bearer) Long, 1988 19 Dendroctonus micans spruce 1- region 2- western Europe Grégoire, 1988; Fielding and Evans, 1997 (spruce beetle) & region 10 Diprion similis (pine pine North America McGugan and Coppel, 1962 ) 11 Dryocosmus kuriphilus chestnut 1-Japan, USA Moriya et al., 2003; Cooper and Rieske, (chestnut gall wasp) 2007; Quacchia et al., 2008 2- Europe 12 hercyniae spruce North America Magasi and Syme, 1984 (European spruce sawfly) 13 Homalodisca vitripennis diverse plants 1-complete control in Tahiti; Grandgirard et al., 2008; Petit et al., 2009 (glassy winged 2-project in progress in sharpshooter) California, but control developing slowly 14 Icerya aegyptiaca diverse plants Kiribati, Federated States of Brancatini and Sands, 1997, Sands et al., Micronesia, the Marianas, 1999 Marshalls and Wake Island 15 Icerya purchasi (cottony diverse plants 1-control complete on Causton et al., 2006; Causton, unpub cushion scale) Ascension Island; 2-control ;Calderon Alverez, 2002; Fowler, unpub.; being evaluated in Ashmole and Ashmole, 1997 Galapagos, but appears effective 16 Icerya seychellarum diverse plants Seychelles Johnson and Threadgold, 1999; K. Beaver, pers. com 17 Jamella australiae Pandanus southern Queensland, Smith and Smith, 2000 tectorius Australia 18 Lymantria dispar (gypsy oak Successful control in the Van Driesche et al., 1996 (see pp. 85-88); moth) core infested area of New Webb et al., 1999; Gillock and Hain, 2001 England 19 Metamasius callizona bromeliads Florida (USA) Frank and Cave, 2005; Cave, 2008 (bromeliad weevil) 20 Operophtera brumata oak 1-Nova Scotia, British Embree, 1971; Embree and Otvos, 1984 (winter moth) Columbia, 2-Massachusetts 21 Paratachardina diverse plants Florida (USA) Pemberton, 2003; Schroer et al., 2008 pseudolobata (lobate lac scale) 22 Quadrastichus Erythrina spp. Hawaii; agents being Gates and Delvare, 2008 erythrinae(erythrina gall evaluation; one released maker) and established

Biological Control is Often the ONLY Logical Response to Invasive or Weed Pests on Small Pacific Islands

Biological Control on small Pacific Islands often relies on BC organisms from previous or ongoing mainland programs for similar crops, insect pests or weeds.

International and Inter-island Cooperation is Vital Thank Goodness For the Internet Thank You Si Yu’os ma’ase’ Mahalo

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