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Home , Adonidia, Aiphanes, Amblyseius, Dictyosperma, Dypsis decaryi, Dypsis lutescens

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CARIBBEAN FOOD CROPS SOCIETY 44 Forty Fourth Annual Meeting 2008

Miami, , USA

Vol. XLIV - Number 1 T-STAR Invasive Symposium

MEETING HOST:

TIP UNIVERSITY of UF FLORIDA IFAS 2008 Proceedings of the Food Crops Society. 44(1):80-174. 2008

SESSION III: TECHNICAL ISSUES RELATING TO INVASIVE SPECIES THREATS IN THE CARIBBEAN BASIN

A PEER REVIEWED PAPER

RED PALM SITUATION IN THE CARIBBEAN AND FLORIDA

Amy Roda1, Ashley Dowling2, Cal Welbourn3, Jorge Pena4, Jose Carlos V. Rodrigues5, Marjorie A. Hoy6, Ronald Ochoa7, Russell A. Duncan8 and Wayne De Chi9. 1 USDA APHIS PPQ CPHST, c/o ARS Subtropical Research Station, 13601 Old Cutler Rd„ Miami, FL 33158. [email protected] ; 2 Dept. of Entomology, University of Arkansas, Fayetteville, AR 72701; 3 Division of Industry, Florida Dept. Agriculture & Consumer Services, Gainesville, FL 32614-7100; 4 Dept. of Entomology and Nematology, University of Florida, TREC - IFAS, Homestead, FL ; 5 University of , Crop Protection Department Jardin Botânico Sur, 1193 Calle Guayacan, San Juan PR, 00926; 6 Dept. of Entomology & Nematology, University of Florida, Gainesville, FL 32611-0620; 7 SEL, USDA, ARS, PSI, Β ARC-West, 10300 Baltimore Ave., Beltsville, MD 20705; 8 USDA-APHIS-IS-Caribbean Area, Santo Domingo, ;9 USDA-APHIS-IS, Port of Spain, Trinidad

ABSTRACT: The red palm mite ( indica Hirst ), a pest of and ornamental palms in Asia and , was reported in the Caribbean in 2004. By 2008, it spread to at least twelve islands, to two counties in Florida and to Venezuela. Red palm mite causes yellowing and necrosis with severe reduction of leaf stomatal conductance. Growers are reporting > 70% reduction in yield. Genetic studies of red palm mite collected from multiple regions in Asia, Africa and the Caribbean revealed several distinct haplotypes. All Caribbean samples have the same haplotype, which matches samples from coconut in Réunion and palms in . The populations from coconut in India exhibited a different haplotype. Biological control and pesticide options are being studied to manage the pest. The efficacy of acaricides against red palm mite was tested to provide palm, and ornamental nursery growers with an updated list of acaricides with good control potential. Natural enemy studies in the Caribbean have shown that , phytoseiid, lacewing, and coccinelid predators attack red palm . Fungal infections have been reported in Puerto Rico, Dominica and Trinidad. Predatory mite numbers, especially in the , increase in response to higher numbers of red palm mites. However, these local predators are apparently not controlling red palm mite outbreaks. Foreign exploration for natural enemies is being conducted in and India. A phytoseiid predator is currently being evaluated in quarantine in Gainesville, Florida.

KEYWORDS: acaricides, biological control, predatory mite, foreign exploration

INTRODUCTION

The red palm mite ( Hirst Tenuipalpidae), an invasive pest of coconuts and ornamental palms in the Old World, has rapidly spread through the Caribbean. A pest risk analysis conducted by USDA APHIS PPQ Plant Epidemiology and Risk Analysis Laboratory

170 concluded that the red palm mite is a serious economic threat to the nursery palm industry and to both indoor and outdoor environments based on cumulative risk, host range, dispersal potential, economic impact, environmental impact and habitat suitability (Borchert, 2007). Due to the likelihood of the pest spreading throughout the Caribbean, , and the continental US, programs were developed in the Caribbean and Florida to identify potential pathways for the pest, optimize survey protocols, and determine mitigation strategies that would minimize the impact of red palm mite in the region.

RESULTS AND DISCUSSION

The red palm mite was first reported in the Western Caribbean in Martinique in 2004 (Flechtmann and Etienne, 2004). By 2008, it spread to at least 12 islands, two counties in Florida and to Venezuela. Red palm mite populations are extremely high and the mite is attacking multiple plant species within multiple monocot plant families (Table 1). Many of R. indica's hosts are new reports such as , and . However not all reported hosts are well suited for mite development and population growth. Higher populations were found on coconut (Cocos nucifera), Christmas palm ( merrilli), Washingtonia spp., Chinese fan palms ( chinensis) and others (Farzan Husin, unpublished data). Coconut production decreased over 75% on plantations in Trinidad one year after the detection of the mite in 2006 and has remained at this lower level for 2 years (Philippe Agostini, President Coconut Growers Assoc., personal communication). Susceptible palms show severe damage with bronzing and chlorosis of , however, no mass die-off of adult palms due to the mite has been documented in the Caribbean. Reports from Puerto Rico indicate that heavily infested small coconuts have died (Jose Carlos Rodrigues, personal observation). Jepson et al. (1975) and Sathiamma (1996) reported red palm mite as a serious pest to coconut seedlings in nurseries and young palms in the field. Although listed as a pest of date palms in , the mite was not considered economically important (Gerson et al., 1983; Zaid et al., 2002).

Red palm mite feeding causes a rapid yellowing of the leaf that has been confused with disease and nutrition problems (Kane and Ochoa, 2006). On coconut these symptoms take 2-3 months to manifest after initial infestation (Rodrigues et al., 2007a). Red palm mites are dispersed through trade of infested material and naturally by wind. They can live for prolonged periods on cut palm fronds and can remain on dry fronds for over 3 weeks, continuing to feed and reproduce as long as the palm frond remains green (Ron Ochoa, personal observation). The red palm mites may survive on craft items made of infested fronds or floral arrangements for an extended period of time.

Studies were conducted to determine the potential origin of the red palm mites found in the Caribbean (Ashley Dowling, unpublished data). Red palm mites were collected by researchers worldwide and a Bayesian analysis was used to determine how closely related were the various red palm mite populations. Raoiella indica was not found in . The Raoiella collected from Australia were different species and were used as an outgroup. These mites were very different from all R. indica collected (22-25% sequence divergence). The populations of red palm mite from the (UAE and ) each exhibited different haplotypes representing the earliest divergence R. indica populations and based upon current sampling, possibly the origins of the species. Red palm mites collected from coconuts in India possessed a different

81 haplotype than those collected from other palms as did populations from the . All Caribbean populations of the red palm mite shared the same haplotype that was identical to populations from Reunion and those found on Betel nut in India. Based on these results a diagram of the potential movement of red palm mite populations through out the world was developed (Fig. 1).

A red palm mite technical working group composed of technical experts, risk analysts and stakeholders was formed in 2006 to identify methods and strategies to survey, detect, identify, and manage red palm mite. Due to the difficulty of detecting the pest at low numbers, its wide host range and its capacity for wind dispersal, the group concluded that eradication was not a feasible option. Additionally, the economic impact of the pest remained unclear and did not warrant the expense for eradication given the limited understanding of the pest. The group recommended that survey efforts focus on early detection in order to institute programs to slow the spread of the pest and that high risk areas needed to be targeted (e.g. nurseries receiving imported material, and ports of entry). Information on the red palm mite needed to be provided to inspectors (both State and Federal), extension agents, pest surveyors and citizens using multiple media venues (websites, brochures, and training sessions). The only plausible wide scale mitigation option was biological control and the selection of resistant varieties of palms and spp. Local generalist predators and pathogens would likely provide a level of control with exotic natural enemies adding further suppression. Pesticide options were needed for growers and for limited use in the landscape (homeowners, botanical gardens). Chemical control needed to consider the end use of the material treated (e.g. coconuts used as ornamentals or for coconut water). Pesticides are currently registered for mite control on these commodities and preliminary studies have been conducted on their efficacy against red palm mites (Rodrigues et al., 2007b).

The red palm mite is a difficult pest to detect due to its small size (<100 microns), the height of palm trees, and the large number of highly dispersed host where the mite could first establish. The most common survey methodology was a visual inspection of fronds, looking for damage and the presence of red palm mite colonies with a hand lens. Additional techniques used include washing leaf samples in alcohol and inspecting the rinse under a dissecting microscope or wiping a white tissue on the underside of the frond looking for red stains. Suspect mites are placed in alcohol for later slide mounting and confirmation of identification. Photographs and samples are taken to verify unknown host plants. The Florida Cooperative Agriculture Pest Survey developed a survey methodology based on experiences in the Caribbean that was effective in detecting the presence of the pest in the U.S (Smith and Dixon, 2008). Initially an extensive educational outreach program was initiated to inform the nursery industry, local government, and homeowners about the likely incursion of the pest. These efforts included information brochures, websites, and extension/nursery association presentations. Field surveys were conducted in high risk or "hot zone" areas that had the highest potential for exotic pest introduction in Florida. The areas selected had the largest numbers of host plants as well as a large number of people traveling to and from the Caribbean islands. Nurseries with high numbers of palms were chosen with preference given to those bringing in coconut for propagation from . Using the information learned about red palm mite populations on different palms, coconut, Christmas palm and bananas were specifically selected because of the increased likelihood of finding the pest on these species. Permanent inspection sites or "sentinel sites" were established in hot zone areas that were easily accessible (parks with open admission, public

82 waterways), had several host plants for inspection, contained palm trees with fronds that can be reached by the surveyor, and were located in or around a point of entry. The sentinel sites were checked at least once a month and surveyed extensively after major weather events such as hurricanes and tropical storms. Often these sites were linked to other regular survey efforts such as fly monitoring.

On November 29, 2007 the first U.S. continental red palm mites were collected in Palm Beach County from a site that was part of the CAPS/Fruit Fly Detection Sentinel Survey Program (Smith and Dixon, 2008). At the time of the first find, 579 sentinel sites had been established in 12 counties in southern Florida. After the detection, delimiting surveys were conducted in the environs and nearby nurseries. Additional sentinel sites were set up in 3 more counties. Working with the Florida Nursery Association, the Florida Division of Plant Industry developed a nursery compliance agreement that outlined survey and chemical practices needed to allow intra/inter State movement of host plant material. As of July 2008, the red palm mite spread was confined to two counties (Palm Beach and Broward). By January 2009, the mite had spread to two additional counties (Miami-Dade and Monroe).

Due to their large population sizes, host range, and dispersal patterns, the only feasible wide- scale mitigation of red palm is biological control. Throughout the Caribbean, efforts have been made to monitor for local natural enemies and to determine their impact on red palm mite populations. In one study, changes in red palm mite and predatory mite populations were monitored at a coconut estate in Trinidad and along the coast in Puerto Rico (Amy Roda, unpublished data). Samples that represented the upper, mid and lower canopy were taken and all mobile mite stages were counted. Red palm mite populations have increased dramatically since 2006, doubling each sample period. Initially more mites were found in the lower canopy but as the quality of these fronds decreased, red palm mite populations shifted to upper portions of the canopy. Interestingly, a predatory mite, (Muma) (: Phytoseiidae), increased in numbers as the red palm population grew, and it followed the red palm mite to new locations in the coconut canopy. The other predators seen feeding on red palm mites, Aleurodothrips fasciapennis (Franklin, 1908) (Thysanoptera: Phlaeothripidae), Bdella sp. (Acari: Bdellidae), Cheletomimus sp. (Acari: Cheyletidae), Ceciodmyiidae and Chrysopidae, did not increase in numbers nor did they follow R. indica movement to other locations in the canopy. The predators not identified to species are likely new species. Other natural enemies found in the Caribbean included predacious mites (Amblyseius spp. Amblyseius longispinus (=Neoseiulus longispinus Evans 1952) (Acari: Phytoseiidae), and Armascirus taurus (Kramer, 1881) (Acari: Cunaxidae)), predacious , Telsimia ephippiger Chapin (Coleoptera: Coccinellidae) and a possible pathogenic fungus (Hirsutella)

Red palm mite is not considered a serious pest in India where natural enemies are reported to control mite populations (as cited in Pena et al., 2006). These natural enemies include ladybird beetles and predatory mites (phytoseiids). Phytoseiid mites are considered more amendable to a classical biological control program due to their relative prey specificity. In October 2007, scientists from the University of Florida and Mauritius collected candidate exotic predatory mites in Mauritius. They found that red palm mite populations were low and confined to coconut trees. The predatory mites they found in association with the red palm mite were brought to Florida for testing in quarantine. Laboratory studies will determine if the exotic predators can feed and reproduce on a diet composed solely of red palm mite. The predatory mites were identified

83 morphologically as Amblyseius largoensis (Muma), a species found throughout the Caribbean and USA. Current genetic studies are indicating that the predators collected in Mauritius are in fact a different, cryptic species distinct from those found in the USA. Further exploration for natural enemies in other countries where red palm mite is not economic pest may produce additional candidates for eventual release in the Caribbean and USA.

RED PALM MITE WEBSITES OF INTEREST

Chemical recommendations (Accessed January 2009): http : //mrec. ifas.ufl. edu/lso/RPM/RPM.htm

Florida Department of Agriculture and Consumer Services (Accessed January 2009): http://www.doacs.state.fl.us/pi/enpp/ento/red_palm_mite.htrnl

USDA APHIS RPM Site (Accessed January 2009): http://www.aphis.usda.gov/plant health/ plant pest info/red palm mite/index.shtml

REFERENCES

Borchert, D. 2007. Risk Analysis of Potential Consequences Associated with the Introduction of the Red Palm Mite, Raoiella indica, into the . USDA APHIS Plant Protection and Quarantine Pest Risk Assessment. Flechtmann, C. H. W., and J. Etienne. 2004. The red palm mite, Raoiella indica Hirst, a threat to palms in the (Acari: : Tenuipalpidae). Systematic and Applied Acarology 9:109-110. Gerson, U., A. Venezian and D. Blumberg. 1983. Phytophagous mites on date palms in Israel. 38:133-135. Jepson, L. R., H. Keifer, and E. W. Baker. 1975. Mites injurious to economic plants. University of California Press, Berkeley. 614 p. Kane, E., and R. Ochoa. 2006. Detection and identification of the red palm mite Raoiella indica Hirst (Acari:Tenuipalpidae). USDA, ARS, Beltsville, MD. Pena, J. E., C. M. Mannion, F. W. Howard and M. A. Hoy. 2006-2008. Raoiella indica (Prostigmata: Tenuipalpidae): The red palm mite: a potential invasive pest of palms and bananas and other tropical crops of Florida. University of Florida. Publication Number: EENY-397. http://edis.ifas.ufl.edu/IN681. Accessed January 2009. Rodrigues, J. C. V., R. Ochoa, and E. Kane. 2007a. First Report of Raoiella indica Hirst (Acari: Tenuipalpidae) and its damage to coconut palms in Puerto Rico and Culebra Island. International Journal of Acarology 33:3-5. Rodrigues, J. C. V, J. E. Pena and A. L. Roda. 2007b. Impact of the Invasion of the Red Palm Mite, Raoiella indica, in Puerto Rico. Proceedings of the Caribbean Food Crops Society. 43:134. Sathiamma, B. 1996. Observations of the mite fauna associated with the coconut palm in Kerala, India. J. Plantation Crops 24:92-96.

84 Smith, T. R. and W. N. Dixon. 2008. 2007 Florida CAPS Red Palm Mite Survey 2nd Interim Report. October 2006 to January 2008. Florida Cooperative Agriculture Pest Survey. Program Report No. 2007-02-RPM-02. Welbourn, C. 2007. Pest Alert: Red Palm Mite Raoiella indica Hirst (Acari: Tenuipalpidae). Florida Department of Agriculture and Consumer Services. Division of Plant Industry. http://www.doacs.state.fl.us/pi/enpp/ento/r.indica.html. Accessed January 2009. Zaid, A. and E. J. Arias-Jimenez. 2002. Cultivation. FAO Plant Production and Protection Paper. 156 Rev. 1. Rome Italy. http://www.fao.Org/docrep/006/Y4360E/v4360e00.htm#Contents. Accessed Jan. 2009.

Table 1 : A list of reported host plants for the red palm mite in the Caribbean Region (Welbourn 2007)

Family Scientific Name Common Name(s) Acoelorraphe wrightii (Grises. & H. Wendl.) Everglades palm Arecaceae Adonidia merrilli (Becc.) Becc. (=) Manila palm, Christmas palm Arecaceae spp. Multiple crown palm, ruffle palm Arecaceae L. betel nut palm Arecaceae Areca spp. Arecaceae plumeriana Mart. Coco macaco, prickly pole Arecaceae mitis Lour. fishtail palm Arecaceae spp. chamaedorea palm Arecaceae Cocos nucifera L. Coconut palm Arecaceae album (Bory) H. Wendl. & princess palm, hurricane palm Drude ex Scheff. Arecaceae decaryi (Jum.) Beentje & J. Dransf. triangle palm Arecaceae (H.Wendl.) Beentje & areca palm, golden cane palm, J.Dransf. (=Chrysalidocarpus) butterfly palm Arecaceae grandis H. Wendl. Licuala palm, ruffled fan palm Arecaceae Livistona chinensis (Jacq.) R. Br. Chinese fan palm Arecaceae hort. ex Chabaud Canary Island date palm Arecaceae Phoenix dactylifera L. date palm Arecaceae Jacq. date palm Arecaceae pacifica B.C. Seem. & H. Wendl. fan palm Arecaceae sargentii H.Wendl. ex Sarg. buccaneer palm Arecaceae (Mart.) Becc. Cacheo, katié Arecaceae elegans (R.Br.)Blume solitaire palm, Alexander palm Arecaceae (H.Wendl. ex Macarthur palm H.J.Veitch) H.Wendl. ex Hook.f. Arecaceae (Thunb.) A. Henry ex Rehder lady palm, bamboo palm Arecaceae borinquena O.F. Cook. royal palm

85 Table 1 continued

Family Scientific Name Common Name(s) Arecaceae (Cham.) Glassman queen palm Arecaceae Syagrus schizophylla (Mart) Glassman arikury palm Arecaceae H. Wendl Mexican fan palm Heliconiaceae psittacorum L. f. parrot Heliconiaceae Heliconia caribaea Lam. wild plantain, Balisier Heliconiaceae Ruiz & Pavon lobster claw heliconia Heliconiaceae (L.) L. Macaw flower Colla edible banana, plantain Musaceae Colla wild banana Musaceae Musa uranoscopus Lour red-flowering banana Musaceae Musa χ paradisiaca L. edible banana, plantain Musaceae Musa sapientum L. ( of the above) edible banana, plantain Musaceae Musa corniculata Rumph. red banana Musaceae Musa spp. banana, plantain utilis Bory screw reginae Banks ex Dryard bird of paradise, crane flower Strelitziaceae madagascariensis traveler's tree Zingiberaceae (Jack.) M. Sm. (=Nicolaia) red torch Zingiberaceae (Vieill.) K. Schum red ginger, jungle king/queen

86 Fig. 1 : Hypothetical routes of introduction for the red palm mite, Raoiella indica. These routes are based on sequence analysis of the cytochrome oxidase gene. Haplotypes found in Australia belong to numerous undescribed species of Raoiella and data suggests Australasian origins for the . Raoiella indica appears to have originated from an Australian ancestor, possibly after introduction to the Middle East where multiple haplotypes of R. indica persist.

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