Integrated Control of Plant-Feeding IOBC/wprs Bulletin Vol. 50, 2009 pp. 69-79

Predator-prey dynamics and strategies for control of the red palm (Raoiella indica) (: Tenuipalpidae) in areas of invasion in the Neotropics

Jorge E. Peña1, Jose Carlos V. Rodrigues2, Amy Roda3, Daniel Carrillo1 and Lance S. Osborne4 1 University of Florida, Tropical REC, Homestead, FL 33031, USA; 2 University of Puerto Rico, 1193 Calle Guayacan, San Juan 00926 Puerto Rico; 3 USDA, APHIS, Plant Protection & Quarantine, Miami, FL 33158, USA; 4University of Florida, Mid-Florida- REC, Apoka, FL., 32703, USA

Abstract: The red Palm mite, Raoiella indica (Acari: Tenuipalpidae) invaded the new world around 2004 and is now reported from the Caribbean islands, Florida, USA and northern South America (Venezuela). Surveys to determine generalist fauna prior to its arrival during the end of 2007 in Florida, reported the predators Amblyseius largoensis, Stethorus utilis, Chrysoperla spp., Aleurodo- thrips fasciapennis and Bdella distincta in association with diaspidids, aleyorids and tetranychids. Predator density increase was not observed until 6 months after the arrival of R. indica in Florida. Studies on predator composition after the initial detection in 2006 of R. indica in Trinidad and Tobago, indicated that the predaceous mite, A. largoensis increased its densities as the red palm mite grew and spread to new locations. Other reported predators were A. fasciapennis, Bdella spp., Cheletomimus sp., and species of the families Cecidomyiidae and Chrysopidae. Amblyseius largoensis, while preying on the red palm mite in Puerto Rico, has not substantially reduced the high numbers of R. indica. Studies to find exotic and more effective predators of the red palm mite should be intensified.

Key words: , red palm mite, phytoseiid mites, biological control

Introduction

The red palm mite (RPM), Raoiella indica Hirst, (Acari: Tenuipalpidae), also known as the mite (Somchoudhury & Sarkar, 1987), coconut red mite (Jalaluddin & Mohana- sundaran, 1990), red date palm mite (Elwan, 2000), leaflet false spider mite (FAO, 2005), frond crimson mite, scarlet mite (Gassouma, 2005) is an important pest of coconuts, date palm, other palm species (PROSEA, 2006), and bananas, beans, and durian in different parts of the world. Previous to its arrival in the New World, the mite was found in India, Philippines, Mauritius, Reunion, Malaysia, Israel and Egypt. Raoiella indica was found in Martinique and St. Lucia in 2004. During 2005, RPM was found in Dominica and during 2006 on the islands of Trinidad, Guadeloupe and Saint Martin (Kane et al., 2005; Etienne & Fletchmann, 2006), and in Puerto Rico (Rodrigues et al., 2007). The mite was discovered in Florida during December 2007 (Peña et al., 2008). Damages to coconut, ornamental palms and bananas are extensive. It is considered that the pest has serious consequences for the coconut, ornamental palm and banana industries of the Caribbean islands. Damage to coconuts results in a 70% yield reduction and possibly job losses, which lead to a major socio-economic problem for some of the islands (Mr. Philippe Agostini, President Trinidad and Tobago Coconut Growers Assoc., Pers. Comm). In Florida, cost of regulatory actions, such as precautionary sprays before shipping R. indica hosts to other states, will represent an

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additional production cost of more than half a million dollars to palm nursery producers per year. Raoiella indica is found on the underside of the leaves of the host plant in very large numbers. On coconuts, attacked leaves display on the upperside uneven dark patches that correspond with the area where the mites are located, this is followed by necrosis of the patches; when seen from a distance, the fronds become yellowish to bronze-orange, followed by necrosis. Heavy mite infestations result in the death of young plants. Management programs for this mite in areas where it is present, as well as preventative programs for areas where it has not yet arrived, are urgently needed. Past chemical control tactics against R. indica were proven inefficacious and costly in India and Egypt, but they are considered necessary for regulatory purposes in infested palm exporting areas (Florida & Puerto Rico). Biological control is one of the most important alternatives to conventional pesticide use in pest management. Classical biological control, or the introduction of natural enemies from the areas of origin for R. indica has been initiated under the auspices of APHIS, PPQ (Marjorie Hoy, pers. comm.), resulting in the quarantine screening of one classical biocontrol candidate. Prior to release of any exotic predator, it is necessary to put greater emphasis on other areas of biological control, such as natural enemy conservation and augmentation. The objectives of this study were 1) to determine the density of predators and herbivorous micro- associated with palms and bananas in Florida before the arrival of R. indica and record the response of the current beneficial fauna to the invading mite in Trinidad, Puerto Rico and Florida.

Materials and methods

Generalist fauna prior invasion by the red palm mite in Florida A survey for natural predators infesting palms and bananas was carried out in South Florida, where most of the palm, Musa, gingers and heliconid production is concentrated. Monthly surveys were conducted in Miami-Dade and Monroe counties in the landscape on coconut palms and on bananas from the end of 2005 until 2008. Twenty pinnae per frond were collected per palm species while 20 sections (ea. ~ 60 cm2) were removed from a banana leaf. Samples were taken to the laboratory, where densities of microarthropods, i.e., tetranychids, tenuipalpids, diaspidids, phytoseiids, bdellids and others were recorded, labeled and mounted and sent for identification by specialists.

Predator composition in Trinidad and Tobago. A study was conducted at the St. Andrews Estate coconut plantation,-Cedros, Trinidad, to determine the distribution of R. indica and predators in the canopy of a coconut tree. Fronds were collected from the upper (leaf 3), mid (leaf 9) and lower (leaf 13) canopy from 5 trees and 9 pinna from each frond representing the top, middle and base were sampled. All motile RPM and predators were counted under a steromicroscope. A predator was determined by having observed it to feed on R. indica.

Predator abundance in Puerto Rico Samples were taken monthly in 8 different sites around Puerto Rico by collecting 10 leaflets, 3 replicates per site, and washing them in 80% ethanol. Ethanol wash samples were then inspected in the laboratory under a stereomicroscope to record presence and abundance of red palm mites and potential predators.

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Naturally occurring generalist predators currently preying on R. indica in Florida Eight coconut palms were selected in two areas in West Palm Beach (26°42′54″N 80°02′22″W) and Broward (26°07′28″N 80°14′58″W). Once each month, since the time of the discovery of the R. indica invasion on December 2007, a single pinna was collected from each of two fronds per palm, totaling 16 samples per site. Each pinna was placed in a plastic bag, sealed and placed in a refrigerated cooler, and frozen before evaluation. Each sample was examined under the microscope, and number of red palm mite, tetranychids, diaspidid scales, whiteflies, mealybugs and different predaceous arthropods (Phytoseiidae, Neuroptera, Thripidae, Coccinellidae) was recorded.

Preliminary tests to determine the efficacy of commercial predators that show potential for control of R. indica Several commercially produced predators will be tested for efficacy to feed, survive and reproduce on R. indica (i.e., Amblyseius swirskii, Phytoseiulus persimilis, Neoseiulus longipes, N. californicus, Galendromus occidentalis). The predator Amblyseius swirskii was selected for a preliminary trial under laboratory conditions. The arena consisted of a 5 cm petri dish placed inside of a 12 cm petri dish. Water was added to the larger petri dish to prevent predator or prey escape from the arena. A 4 cm2 section of a coconut frond that held a known number of different stages of R. indica was added. Then, presumably mated 1 to 2 day old single females were individually placed inside of the arena. The number of eggs, nymphs and adults consumed daily was calculated and new food sources added daily.

Results and discussion

Generalist fauna prior to invasion by the red palm mite in Florida The scale, Aonidiella orientalis (Newstead) (Heteroptera: Diaspididae), the whitefly, Aleuro- canthus woglumi Ashby (Heteroptera: Aleyrodidae) and the spider mites, Tetranychus spp., Tetranychus gloveri Banks (Acari: Tetranychidae), were the most common microarthropods inhabiting coconuts, while Tetranychus sp., and Brevipalpus spp., were the most common inhabiting bananas from 2006 to 2008 in areas before the arrival of RPM (Figures 1 and 2). On coconuts, the predators, Amblyseius largoensis (Muma) (Acari: Phytoseiidae), Stethorus utilis (Horn) and Chrysoperla spp., (Neuroptera: Chrysopidae) were the most common predators followed by Bdella distincta (Barker and Bullock) (Acari: Bdellidae) and Aleurodo- thrips fasciapennis (Franklin) (Thysanoptera: Phlaeothripidae). On bananas, the predators Amblyseius spp., and Stethorus utilis were recorded (Figures 3 and 4). Amblyseius largoensis was the only phytoseiid on coconuts, while the identification of the Amblyseius sp. found in bananas is pending. Amblyseius largoensis is a generalist feeding not only on mites, but also on pollen (Yue & Tsai, 1996). A study conducted in Brazil to determine the survival of A. largoensis on guerreronis (Acari: Eryophidae), a pest of coconuts and on other food sources (pollen and honey), determined that a mixed diet of A. guerreronis, or T. urticae + pollen and + honey increased the predator's fertility parameters (Galvao et al., 2008). Although A. largoensis is one of two predators found earlier in The Philippines in association with Rarosiella cocosae Rimando (= Raoiella indica) (Gallego et al., 2002), its efficacy has not been determined yet. Amblyseius. largoensis was also found in association with Aceria guerreronis (Acari: Eryophidae) on coconuts fruits, but no clear prey preference has yet been determined for this species on that plant (Reis et al., 2008). The predaceous thrips, A. fasciapennis, was previously reported feeding on eggs of diaspidid scales such as Chrysomphalum aonidum and Aspidiotus nerii and on eggs of the pyralid moth, Corcyra cephalonica (Watson et al., 2004; Beshear & Nakahara, 1975).

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Stethorus utilis is cited as a common predator of tetranychid mites (Chazeau, 1985). In general, because of the high densities of both diaspidids and aleroydids present on coconuts, the prey preference for the native predators needs further study under Florida conditions.

Figure 1. Dynamics of herbivorous micro-arthropods inhabiting coconuts prior to establish- ment of R. indica in south Florida (Miami-Dade).

Figure 2. Dynamics of natural enemies inhabiting coconuts prior to establishment of R. indica in south Florida (Miami-Dade).

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Figure 3. Dynamics of herbivorous micro-arthropods inhabiting bananas prior ot establish- ment of R. indica in south Florida (Miami-Dade)

Figure 4. Dynamics of natural enemies inhbiting bananas prior to establishment of R. indica in south Florida (Miami-Dade).

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Predator composition in Trinidad and Tobago Raoiella indica rapidly spread throughout Trinidad after its initial detection in May 2006. Since September 2006, changes in RPM and predatory mite populations were monitored at the St. Andrews coconut estate, Cedros, Trinidad. Red palm mite populations increased dramatically, doubling at each sampling period. More mites were initially 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. largoensis increased in numbers as the RPM population grew and it followed the pest to new locations in the coconut canopy. However, the increase in A. largoensis numbers did not cause a corresponding decrease in R. indica numbers. The other predators seen feeding on red palm, Aleurodothrips fasciapennis, Bdella sp., Cheletomimus sp (Acari: Cheyletidae), Ceciodmyiidae and Chrysopidae (Figure 5), did not increase in numbers nor did they follow RPM movement to other locations in the canopy. The predators not identified to species are likely new species.

A B C

Figure 5: Predators observed preying upon R. indica included Aleurodothrips fasciapennis (A) pictured feeding on a R. indica larvae, Cheletomimus sp. (B) pictured feeding on a R. indica adult female, and a possible ceciodmyiid larvae (C) pictured feeding on a R. indica egg.

Predator abundance in Puerto Rico Raoiella indica was first reported from eastern Puerto Rico in late October, 2006 (Rodrigues et al., 2007) and has since spread through the island. Both R. indica and natural enemy populations have been monitored. Four months after the first report in Puerto Rico the pest was observed around Ponce (central south part of the island) about 50km from the original detection sites. Later, in December 2007, RPM populations were seen on the extreme west side of Puerto Rico. Phytoseiids mites, crisopids and predatory thrips species were observed in association with R. indica populations (Figure 6). Samples from adult coconut palms (10 leaflets, 3 replicates per site) were washed in 200mL of 80% ethanol, which was then inspected in the laboratory under a stereomicroscope for the presence of red palm mites and potential phytoseiid mite predators. Mite specimens were slide mounted for species confirmation. Amblyseius largoensis was the most common potential predator observed associated with RPM in the palm samples. Variations of the pest populations among different localities and over time were observed (Figure 7). Comparing the different sites, one saw that the arrival of RPM was followed by an increase in phytoseiid mites (data not shown). Correlation between populations of phytoseiid mites and the occurrence of red palm mite on coconut were statistically significant.

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Despite the increase of Amblyseius after the reported arrival of R. indica, the predator has not substantially reduced the high numbers of RPM. In order to control the pest's outbreaks and minimize the its damages, work to find exotic natural enemies should be intensified. In addition, we developed a PCR-based method to identify the phytoseiid mites feeding on RPM. This method could be applied to identify R. indica predators in samples taken directly from the field.

Figure 6. Predator species observed in Puerto Rico associated with Raoiella indica. Left: Amblyseius largoensis; observe the coloration inside, the mite's digestive tract after it has fed on a red palm mite. Right: a chrysopid larva observed feeding on R. indica .

Naturally occurring generalist predators currently preying on R. indica in Florida The relationships between phytoseiid predators, i.e., A. largoensis and the potential new prey were erratic. For instance, while an increase in predator density was observed following an increase in the prey during January-February, and May -June, 2008, numbers of predators were still consistently low, compared to the number of prey present.

2500 25 Site - Humacao

2000 20

1500 15

RPM Number of Numbe of Phyt. 1000 10

500 5

0 0 Oct-07 Nov-07 Dec-07 Jan-08 Feb-08 Mar-08 Apr-08 May-08 Jun-08 Jul-08 Aug-08 Figure 7. Population dynamics of Raoiella indica and Amblyseius largoensis in coconut palms, Humacao, Puerto Rico. Average of number of mites per 10 leaflets, three repetitions.

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West Palm Beach - 2008 4500 8

4000 Raoiella indica Phytoseiid Mites 3500 6 3000

per Pinna 2500 4 2000

1500 Mites Phytoseiid 2 Raoiella indica 1000 500

0 0 Jan Feb Mar Apr May Jun

2008

Figure 8. Raoiella indica populations and phytoseiid densities after the invasion of the red palm mite in West Palm Beach, FL, USA.

Broward - 2008

1800 2.5

1600 Raoiella indica Phytoseiid Mites 1400 2.0

1200 1.5 per Pinna 1000

800 1.0

600 Mites Phytoseiid

Raoiella indica 400 0.5 200

0 0.0 Jan Feb Mar Apr May Jun 2008

Figure 9. Raoiella indica populations and phytoseiid densities after the invasion of the red palm mite in Broward, FL, USA.

In the area of Palm Beach a total of 45,280 RPM were collected per pinna between January and June, 2008; this is a much higher density than that found in Broward, where average R. indica densities fluctuated ca. 100 to 1,600 mites per pinnae (Figs 8 and 9). A total of 22 A. largoensis was collected between January to June, 2008 in that area. Increase of predator density was not observed until June, approx. 6 months after the detection of the pest.

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No significant correlations were determined between the population levels of natural enemies and the population levels of R. indica (F1, 3 = 2.36; P = 0.21; F1,2 = 1.3; P = 0.49) for Broward and Palm Beach, respectively. While at this point we have not reached one year from the discovery of the infestation of R. indica in Florida, it is doubtful whether A. largoensis will be capable of maintaining the prey under lower densities than those observed until now (Figs 8 and 9). No significant correlations between abiotic factors (temperature, precipitation) and the population levels of R. indica were observed during these months at either site (Temperature: F1,3 =5.83; P= 0.09 for Broward and F1,3 = 1.70; P= 0.28 for Palm Beach. Precipitation: F1,3=0.08; P = 0.79 for Broward and F1,3 = 1.75; P= 0.27 for Palm Beach).

Preliminary tests to determine the efficacy of commercial predators that show potential for control of R. indica A female A. swirskii consumed a daily average of 7.06 ± 0.61 eggs, 2.49 ± 0.21 larvae, 3.25 ± 0.29 nymphs and 8.90 ± 0.55 RPM adults. Female longevity was 11.54 ± 0.72 days with an average daily oviposition of 1.1 ± 0.10 eggs. It is not known what would be the predation potential of immatures of this species on R. indica.

Preliminary field trials with a commercial predator A significant reduction of RPM numbers was observed one month after releasing 250 A. swirskii per palm in the area of Manalapan (F 1,18 = 13.66, P= 0.001). However, no significant increases in phytoseiid densities were recorded (Fig 10). Further studies are needed to determine the effectiveness of A. swirskii as a predator of R. indica under field conditions.

160 140 120 Number of R. 100 indica / section 80 R.indica of pinna 60 Phytoseiidae 40 20 0 June July

Fig 10. Monthly average of R. indica densities before and after release of A. swirskii, Palm Beach, FL, 2008.

Acknowledgments

We like to thank Aixa Ramirez, Puerto Rico Department of Agriculture for continuing support, Dr. Gilberto De Moraes and Calvin Welbourn for identification of the phytoseeid mites. This work receives partial support from USDA/APHIS Cooperative Agreement 07- 8372-0544-CA and H-427.

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