Within-season dynamics of red palm mite (Raoiella indica) and phytoseiid predators on two host palm species in south-west India

Transcription

1 DOI /s Within-season dynamics of red palm mite (Raoiella indica) and phytoseiid predators on two host palm species in south-west India B. Taylor P. M. Rahman S. T. Murphy V. V. Sudheendrakumar Received: 9 September 2010 / Accepted: 23 July 2011 Ó Springer Science+Business Media B.V Abstract Field surveys were conducted monthly between December 2008 and July 2009 in Kerala, south-west India to compare the population dynamics of the red palm mite Raoiella indica (RPM) on two host plants Areca catechu and Cocos nucifera during one non-monsoon season when, in general, RPM populations increase. The aim was to examine the effects of host plant, host plant locality and the impact of climatic factors on RPM and related phytoseiid predators. There were significantly higher RPM densities on areca in peak season (May/June) compared to coconut; although significantly more coconut sites were infested with RPM than areca. Although no one climatic factor was significantly related to RPM numbers, interactions were found between temperature, humidity and rainfall and the partitioning of host plant locality showed that where conditions were warmer and drier, RPM densities were significantly higher. Specifically on coconut, there was a significant relation between RPM densities and the combined interaction between site temperature, site humidity and phytoseiid densities. There was a marked difference in the density of phytoseiids collected between areca and coconut palms, with significantly more on the latter, in several months. Amblyseius largoensis was the most commonly collected phytoseiid in association with RPM, although Amblyseius tamatavensis species group and Amblyseius largoensis species group were collected in association with RPM also. There was also evidence of a weak numerical response of the combined phytoseiid complex in relation to RPM density the previous month on coconut but this was not observed on areca. Keywords Raoiella indica Areca catechu Cocos nucifera Biological control Phytoseiids Within-season dynamics B. Taylor (&) S. T. Murphy CABI Europe UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK b.taylor@cabi.org P. M. Rahman V. V. Sudheendrakumar Kerala Forest Research Institute (KFRI), Peechi, Thrissur, Kerala, India

2 Introduction The red palm mite (RPM), Raoiella indica Hirst (Tenuipalpidae), has become a major concern to the coconut and banana industries in the New World since it was first reported as an invasive species in Martinique by Flechtmann and Etienne (2004). The mite has since spread widely throughout the Caribbean islands and has now been reported in South Florida (Smith and Dixon 2008), North Venezuela (Vásquez et al. 2008), Mexico (Estrada-Venegas et al. 2010), Brazil (Navia et al. 2010) and Colombia (Carrillo et al. 2011). RPM causes damage to a wide variety of hosts in the orders Arecales and Zingiberales (Cocco and Hoy 2009), which were previously unreported as hosts prior to its introduction. The mite was first described in the Old World, from Coimbatore, India in the early part of last century (Hirst 1924) and has now been widely reported on areca nut (Areca catechu L.) and coconut (Cocos nucifera L.) in India. Other host plants reported prior to its introduction into the New World are the Date Palm (Phoenix dactylifera L.) (Sayed 1942) and the Hurricane Palm (Dictyosperma album (Bory) H.A. Welland & Drude) (Moutia 1958). Management of RPM in the New World has proved difficult because of its ubiquitous spread, and literature available on chemical control methods from the Old World is not applicable in the New World (Pena et al. 2006). Classical biological control is seen as a possible alternative as a number of natural enemies associated with RPM have been reported in the Old World (Kapur 1961; Moutia 1958; Daniel 1979; Somchoudhury and Sarkar 1987; Yadavbabu and Manjunatha 2007). Little quantitative information exists, however, on the dynamics of RPM and its natural enemies. Studies on RPM in the Old World have generally focused on the phenology of the mite in relation to one host plant and the impact of climatic factors; study has also been made of associated natural enemies. Positive relationships between RPM numbers and temperature have been reported in India by several authors (Sarkar and Somchoudhury 1989; Nagesha-Chandra and Channabasavanna 1983 on coconut; Yadavbabu and Manjunatha 2007 on areca). The relationship with relative humidity and rainfall has varied in significance depending on the study. Negative relationships were reported by Yadavbabu and Manjunatha (2007) on areca nut and on coconut by Nagesha-Chandra and Channabasavanna (1983), who demonstrated that there was a difference in effect of rainfall depending on the life stage; adults were not significantly affected by rainfall whereas nymphs and eggs were. In contrast, no significant relationship with rainfall or humidity was reported by Sarkar and Somchoudhury (1989) on coconut during their study. Moutia (1958) from qualitative observations reported that heavy rain and violent gales restricted the build-up of RPM populations in Mauritius. Several studies have investigated the natural enemy fauna associated with RPM. In West Bengal, on coconut, Somchoudhury and Sarkar (1987) found the most commonly recorded predators were Phytoseius sp. (Mesostigmata: Phytoseiidae), Amblyseius sp. (Mesostigmata: Phytoseiidae) and Oligota sp. (Coleoptera: Staphylinidae), and found that Oligota sp. and Phytoseius sp. populations were positively correlated to RPM populations whereas Amblyseius sp. was negatively correlated. A study by Daniel (1979) on areca nut in Karnataka, India, showed there to be an increase in numbers of the phytoseiid Amblyseius channabasavanni (Gupta and Daniel) in response to an increase in RPM populations. On coconut in Mauritius, the natural enemy fauna recorded included Amblyseius caudatus (Berlese) (Moutia 1958) but no empirical population data of RPM was given to correlate with predatory mite levels. In the New World, Amblyseius largoensis (Muma) (Acari: Phytoseiidae) has been reported in association with RPM in the Caribbean and Florida (Pena et al. 2009). From the natural enemy surveys completed to date, it appears that phytoseiid predators seem to play an important role in this system.

3 It is not clear from the publications what the reasons are for the differences in species composition of common natural enemies associated with RPM within regions apart from differences due to geography, but palm host and climate may be important factors. McMurtry and Croft (1997) commented on the life history adaptations of generalist predatory mites such as Amblyseius spp. and postulated that they may have evolved more in response to plant host than specific prey. This would have great bearing on the effectiveness of a possible biological control agent as the host range of RPM is so broad in the Caribbean region. The aim of the study was to compare the within-season dynamics of RPM and the associated phytoseiid mite fauna on two different host palms, both in two separate areas. This was to determine the relative influence of host palm species, geography and climatic factors and the nature and impact of the phytoseiid mite fauna on RPM populations. The implications of the results for the potential of biological control are then discussed. Materials and methods Two separate areas for coconut and for areca nut were selected for the study. The areas for coconut were the Vadakkencherry area near Palakkad and Peechi near Thrissur, and the areas for areca nut were Kunnamkulam and Nilambur. All sites were situated in Kerala, south-west India. Area specific data was gathered onsite during surveys, as the only functioning weather station available in the area during the survey period was located at Kerala Forest Research Institute, Peechi. Thus, site temperature and humidity were collected at the time of leaflet sampling at every site in each area throughout the study and the averages from all sites per area were calculated (±1 SE). Data on area-wide rainfall was taken from a weather station located at KFRI, Peechi. In each survey area, 20 palms were selected within a 10 km strip (apart from Kunnamkulam where 10 palms were selected due to lack of availability of areca palms). Palms were mainly located at smallholder farms situated within a few hundred meters of narrow roadsides. As access to palms was difficult because of the few winding roads and hilly terrain, the following protocol was adopted to select palms in an unbiased manner. A start point for each area was chosen, and then palms were selected during trips by car every s; at each stop the nearest palm was selected. To standardise sampling in terms of age of palms and age of fronds, young palms no taller than four metres were selected and one lower frond was sampled. To calculate the density of RPM and phytoseiids per leaflet, each frond sampled was divided into three sections, upper (tip), middle and lower (base) and a leaflet was chosen at random from each of these sections. The three selected leaflets were then removed from the frond (at the leaflet base, adjacent to the rachis) and labelled, giving three leaflets in total for each frond. Leaflets were stored separately in cotton bags and returned to the laboratory to be examined using a stereo microscope. Numbers of RPM mobile stages and eggs were counted and noted. Leaflet dimensions for both areca and coconut were taken by measuring the length and width (latter at widest point), then the area was converted using a standard multiplier (Rao and Sebastian 1994), which was 0.74 for areca and 0.63 for coconut. Leaflets were also inspected for phytoseiid mites present. Numbers of these per leaflet were noted and voucher specimens were stored in 80% ethyl alcohol. The sampling protocol was carried out monthly between December 2008 and July 2009 (with exception of May and June which were combined). Voucher specimens of RPM and phytoseiid mites were sent to Dr B Mallik (University of Agricultural Sciences, Bangalore, India) for species confirmation. Further specimens

4 were slide mounted using Heinze media and identified by the senior author with the assistance of Dr. D. A. Griffiths (UK). Analysis of data Numbers of RPM from the three leaflets per palm were summed and divided by the total converted area of the three leaflets to give a mite density per cm 2. Where leaflet measurements were not taken, an average leaflet size from that area for that month was used. The densities from each of the 20 palms per area were then transformed using log (x? 1) (natural log) before statistical analysis; other conversions were investigated but log (x? 1) was found to be the most suitable as it stabilized the variance. Anti-logged data displaying the geometric mean was plotted on graphs, using 80% confidence limits as this was sufficient to determine major changes in mite numbers (Southwood and Henderson 2000). Differences in densities of RPM and phytoseiids on the two different host palm species and the different sites in the study were determined monthly using ANOVA from individual site replicates within the study areas. A generalised linear model with binomial errors was used to analyse the difference in proportion of sites with RPM present per month on both host palms; quasibinomial errors were used when there was evidence of overdispersion in the model. To analyse the impact of climatic factors on RPM, population data were analysed using the log (x? 1) converted data averaged from each of the areas, each month to avoid zero values in data. These data were not considered to be temporally pseudoreplicated as destructive sampling methods were employed each month; thus the response of different colonies on separate leaflets were analysed. Analyses were carried out largely using ANCOVA and multiple regressions in the R-statistics package (R Development Core Team 2009). Results from statistical analyses were considered significant at the 5% level. Results Study area climatic features For the coconut growing areas, Palakkad was significantly warmer than Peechi in all months apart from January and July (Fig. 1a) and in terms of humidity; Peechi was significantly more humid than Palakkad in all months apart from January and July (Fig. 1b). For the areca growing areas, Kunnamkulam was significantly warmer than Nilambur apart from in December and July (Fig. 1a). In the areca areas, Nilambur was more humid than Kunnamkulam in most months, but only significantly in January, February and March (Fig. 1b). Overall, there was no significant difference in temperature and humidity between coconut and areca growing areas, apart from January where the coconut growing area was significantly warmer and drier than areca growing areas (Tukey HSD P \ 0.01). Little rainfall was observed in the region between December and April, however significant rainfall commenced in May/June and July (Fig. 1c). General population trends on the two host palm species and between the study areas Data from the two areas for each host palm (Peechi and Palakkad for coconut and Nilambur and Kunnamkulam for areca) were combined to compare temporal changes throughout the season in each host palm growing area. There was a gradual build up in

5 Fig. 1 Climatic conditions in study areas during season a average site temperature (±1 SE), b average site humidity (±1 SE), c area wide rainfall. Significant differences (P \ 0.05) are indicated with different letters RPM densities from December 2008 onwards, peaking in April on coconut and May/June for areca (Fig. 2a, b). Populations dropped significantly the following month on both hosts. Of the 40 sites observed for coconut and 30 for areca, the proportion of sites in each study area in which RPM was found increased throughout the observation period, peaking in March (Fig. 3). This was the case for both host palms but on coconut there was a significantly higher proportion of RPM positive sites in February (t = 2.01, P \ 0.05), March (t = 2.03, P \ 0.05) and April (t = 2.89, P \ 0.05) when compared to areca. On coconut, in May/June, there was a significant drop in RPM density (Fig. 2a), but not in the number of sites where RPM were observed, indicating a drop in density across all coconut sites. There were significantly higher densities of RPM observed on areca than coconut in May/June (F = 5.78, P = 0.02) and marginally more in March (F = 2.97, P = 0.09).

6 Fig. 2 Temporal population densities of Raoiella indica (RPM) (eggs and mobile stages) and phytoseiids (mobile stages) on a coconut and b areca nut, December 2008 July Data is expressed as the geometric mean calculated from reconverted data mean (with 80% confidence limits) of mites or eggs per cm 2 leaf area sampled Fig. 3 Proportion of sites with Raoiella indica (RPM) on areca and coconut throughout the season Observations from the field in May/June showed that dense colonies of RPM could also be found on the stem on the areca palm, no such observations were made on coconut. A monthly comparison of RPM in the two study areas for each host palm showed there was a significant difference in RPM density between Peechi and Palakkad (F = 5.57, P = 0.04, Fig. 4a) with Palakkad consistently showing higher densities of RPM per cm 2 every month. Even though there was no significant difference between RPM densities

7 Fig. 4 Difference in Raoiella indica (RPM) densities through the season (80% confidence limits) in a Palakkad and Peechi (coconut sites), b Nilambur and Kunnamkulam (areca sites). Data is expressed as the geometric mean calculated from reconverted data mean of mites per cm 2 leaf area sampled between the areca areas overall (F = 0.09, P = 0.78, Fig. 4b), there was a time difference in the rise/decline of populations between areas, with Kunnamkulam having significantly higher density of RPM in January (t =-2.37, P = 0.02), February (t =-2.15, P = 0.04) and Nilambur having significantly higher densities in May/June (t = 2.34, P = 0.02) and marginally in April (t = 1.93, P = 0.06). Overall, the density of phytoseiid individuals (all spp.) collected from sites peaked in December on coconut and January on areca, and densities dropped significantly in the following month on both host plants (Fig. 2a and 2b); there were significantly higher densities phytoseiids on coconut than areca in December, March, April and May June (t = 3.94, P \ 0.01; t = 2.78, P \ 0.01; t = 1.98, P = 0.05; t = 2.06, P = 0.04; t = 2.8, P = 0.04, respectively) and significantly higher on areca in January (t = 2.78, P \ 0.01). The number of phytoseiids found on areca dropped significantly in February and to zero from March onwards. There was a negative relationship between phytoseiid density and RPM density on areca and a positive relationship on coconut, however, these were not significant (F = 0.90, P = 0.36; F = 0.33, P = 0.58 respectively) (Fig. 5a). A regression of RPM density from both host palms the previous month and phytoseiid density the current month (combined data) showed RPM density to be related to a significant interaction between host palm, phytoseiid density (t = 2.15, P = 0.04). In relation to the individual palms, a positive relationship was found on coconut (t = 1.90, P = 0.09) although only marginally significant. Population densities showed a negative relationship that was not significant on areca (t =-1.17, P = 0.27; Fig. 5b).

8 Fig. 5 a Relationship between log phytoseiid density and log Raoiella indica (RPM) density in the same month throughout the season on areca and coconut. Areca: Intercept = , slope = , Multiple R 2 = 0.07, F 1,12 = 0.9, P = Coconut: Intercept = , slope = , Multiple R 2 = 0.03, F 1,12 = 0.33, P = b Relationship between log RPM density the previous month and log phytoseiid density the current month on both areca and coconut. Areca intercept = , slope = , Multiple R 2 = 0.12, F 1,10 = 1.36, P = Coconut intercept = , slope = , Multiple R 2 = 0.27, F 1,10 = 3.62, P = 0.09 Phytoseiid identification Phytoseiids collected during the sampling of the leaflets were identified as Amblyseius largoensis, A. largoensis species group, Amblyseius tamatavensis species group and Euseius ovalis; other predatory mites collected included the families Cunaxidae, Bdellidae and Stigmaeidae. Non-acarine predators included Stethorus keralicus and an unidentified dipteran larva (Cecidomyiidae). All these non-phytoseiid predators were very scarce during the study. The only phytoseiids found in association with RPM colonies were A. largoensis, A. largoensis species group and A. tamatavensis species group, although the last two species were only found in direct association with RPM on one occasion each. RPM consumption by A. largoensis was confirmed in laboratory feeding trials (data not shown). The A. largoensis specimens identified were all sampled from leaflets in the Palakkad area and were found in association with RPM in the majority of cases. Amblyseius largoensis species group were generally sampled from areca in December and

9 January, however those specimens from areca were never found in association with RPM. Amblyseius largoensis species group was also found in association with RPM on one occasion on coconut in Palakkad (January). Euseius ovalis was found on both areca and coconut (Kunnamkulam and Peechi) in January but not in association with RPM. Relationship between site temperature, site humidity and local rainfall on RPM and phytoseiid densities on both host palms within the study areas There was a significant interaction between host palm, site temperature and humidity and area-wide rainfall on RPM density throughout the season (F = 8.16, P = 0.01). On the individual host palms, however, a regression showed that the above climatic factors had no significant effect on RPM densities on coconut (F = 2.41, P = 0.15). On areca, there was a significant interaction between temperature, humidity and rainfall (F = 11.61, P = 0.01). When factors were investigated individually none were found to be significant on their own, although there was a negative relationship between rainfall and RPM density and positive relation with temperature (Fig. 6). Humidity was negatively related on coconut, and not related on areca. Data was also examined using climatic factors from the previous month (Fig. 7) as these may exert a more significant influence on RPM densities observed in the current month. When both host palms and all climatic factors were fitted to the regression model, there was a significant interaction between host palm, site temperature and site humidity Fig. 6 Relationship between log Raoiella indica (RPM) per cm 2 and local climatic factors on areca and coconut (fitted with a regression line). a Temperature: Areca intercept =-0.45, slope = 0.016, Multiple R 2 = 0.05, F 1,12 = 0.56, P = Coconut intercept =-0.19, slope = , Multiple R 2 = 0.11, F 1,12 = 1.49, P = b Humidity: Areca intercept = 0.086, slope = , Multiple R 2 \ 0.01, F 1,12 \ 0.01, P = Coconut intercept = 0.099, slope = , Multiple R 2 = 0.09, F 1,12 = 1.19, P = 0.30, c Rainfall: Areca intercept = 0.10, slope = , Multiple R 2 = 0.01, F 1,12 = 0.15, P = Coconut intercept = 0.047, slope \ , Multiple R 2 = 0.17, F 1,12 = 2.41, P = 0.15

10 Fig. 7 Relationship between log Raoiella indica (RPM) per cm 2 and local climatic factors from the previous month on areca and coconut (fitted with a regression line). a temperature. Areca intercept = -0.27, slope = 0.011, Multiple R 2 = 0.023, F 1,10 = 0.23, P = Coconut intercept =-0.18, slope = , Multiple R 2 = 0.11, F 1,10 = 1.20, P = b Humidity: Areca intercept = 0.38, slope = , Multiple R 2 = 0.13, F 1,10 = 1.44, P = Coconut intercept = 0.13 slope = , Multiple R 2 = 0.20, F 1,10 = 2.43, P = c Rainfall: Areca intercept = 0.13, slope = , Multiple R 2 =-0.13, F 1,10 = 1.47, P = Coconut intercept = 0.049, slope \ 0.001, Multiple R 2 = 0.14, F 1,10 = 1.65, P = 0.23 (t = 2.13, P \ 0.05) which was less significant than data regressed using data from the current month. On coconut alone it was found that there were marginally significant interactions between temperature, humidity and rainfall the previous month (t =-2.87, P = 0.08) which was more significant than current month data. On areca, no significant relationship was found between climatic factors the previous month. Again, when individual factors were examined, no one factor was found to be significantly related (Fig. 7) but there was evidence of a positive relationship with temperature and negative relationship with humidity and rainfall on both host palm species. For phytoseiids, none of the climatic factors were shown to have a significant effect on phytoseiid density both coconut and areca nut (data not shown). The relationship between climatic factors the previous month and phytoseiid number was also examined and it was found that on coconut, there was a weak relationship between temperature, humidity and rainfall the previous month on phytoseiid densities (F = 5.98, P = 0.07, Fig. 8). On areca, temperature the previous month had a significant negative relationship with phytoseiid densities (t = 2.25, F = 5.06, P \ 0.05). To investigate the relationship between site temperature, site humidity and phytoseiid density on RPM density (current month); a multiple regression was performed on nonaveraged RPM densities when in association with phytoseiids on coconut. Zero RPM and phytoseiid values were removed from the dataset. Rainfall was not included as there was no site specific information. The results showed there to be a significant relation between RPM density and humidity, site temperature and phytoseiid density on coconut (t =-3.28,

11 Fig. 8 Relationship between log phytoseiid per cm 2 and local climatic factors from the previous month. a Temperature: Areca, Intercept = , Slope = , Multiple R 2 = 0.34, F 1,10 = 5.06, P = Coconut regression line, intercept = , slope = , Multiple R 2 = 0.04, F 1,10 = 0.46, P = 0.51, b Humidity: Areca intercept = , Slope = , Multiple R 2 \ 0.01, F 1,10 = 0.04, P = Coconut intercept = , slope = , Multiple R 2 = , F 1,10 = 0.07, P = c Rainfall: Areca intercept = , slope = , Multiple R 2 = 0.05, F 1,10 = 0.52, P = Coconut intercept = , slope = , Multiple R 2 = 0.11, F 1,10 = 1.26, P = 0.29 P \ 0.01 for the interaction; Multiple R 2 = 0.44; F 7,23 = 2.6, P = 0.04 for the model). Other significant interactions were site temperature and phytoseiid density (t = 2.99, P \ 0.01); humidity and phytoseiid density (t = 3.22, P \ 0.01) and phytoseiid density (t =-2.89, P \ 0.01). A similar analysis was not conducted with the data from areca as phytoseiids were only found in association with RPM on one occasion (December 2008). Discussion The study reported covered one non-monsoon season (December July) in the dynamics of RPM and associated phytoseiid complex, thus further sampling work would improve the robustness of the results. Nonetheless, some important points and conclusions did emerge. Both host palms showed a trend whereby populations increased from December, early in the inter-monsoon season, onwards to either April or May/June and then displayed a significant drop in numbers, as shown by previous authors (Yadavbabu and Manjunatha 2007; Nagesha-Chandra and Channabasavanna 1983). There were likely host level effects on populations, as areca had significantly higher numbers of RPM per cm 2 than coconut in certain months (peak areca RPM densities were 8.60/cm 2 (Kunnamkulam, March), compared peak densities of 0.94/cm 2 on coconut (Peechi, March), and coconut palms had a higher percentage of infested palms than areca. Reasons for these differences may be host palm associated physiological or physical differences such as leaf stomatal density or

12 canopy area available for colonisation. No data is available comparing stomatal density between areca and coconut however; there is a difference in the number of fronds on 1 year old seedlings of areca (4 5) and coconut (8 10) (Purseglove 1972) which could partly explain the difference in densities reported here. Differences in RPM densities between study areas on the same host palm were also shown for both areca and coconut indicating that other factors influence RPM density. Although no one factor was found to be significantly related to population growth, interactions between all climatic factors were evident on areca for the current month and marginally for coconut the previous month. There was also a non-significant positive relationship with temperature on both host plants, which is in line with findings by Yadavbabu and Manjunatha (2007) on areca, Sarkar and Somchoudhury (1989) and Nagesha-Chandra and Channabasavanna (1983) on coconut. Although the regression against mite number and climatic factors showed complicated interactions, by blocking the areas by temperature and humidity between regions it enabled patterns in RPM density to be observed in relation to regional climatic factors. For example, on coconut, climatic site observations showed Palakkad to be significantly warmer and drier than Peechi and this was associated with a significantly higher density of RPM. Also, on areca, the months shown to be significantly warmer and drier had significantly denser RPM populations in general. Whether the small regional differences in climatic factors are enough to affect RPM populations on their own remains to be proved but, the same relationship between lower humidity and higher temperature and RPM density was also reported by Nagesha- Chandra and Channabasavanna (1983) on coconut. During the population growth phase on coconut, there appeared to be evidence that as well as increasing in density, the mites were either dispersing among sites and/or being detected on a higher frequency of sites compared to previous months between December and March. Welbourn (2006) postulated that RPM move on wind currents as they are found on the tops of palms in the invasive range. Observations during the study on surrounding banana plants at coconut sites found very low numbers of RPM individuals on some plants (data not shown). Thus it is likely that the individuals were windblown onto these plants, as they were collected in Feb-March when colonies were fully formed on surrounding coconut palms. Similar to results from previous studies, rainfall was shown to be negatively related to RPM density (Nagesha-Chandra and Channabasavanna 1983; Sarkar and Somchoudhury 1989; Yadavbabu and Manjunatha 2007) but it was not a significant factor on its own and results indicated an interaction between temperature and humidity. The significant drop in RPM density in Peechi and Kunnamkulam (April) coincided with the first appreciable rainfall since December 2008, but whether this is the reason for the crash is not clear. Nonetheless, high levels of rainfall were observed in May/June (867.6 mm) and July (1,188 mm) coinciding with the crash in populations in Palakkad and Nilambur, which was more likely to explain the population crashes in these cases. Klubertanz et al. (1990) found that normal intensity rainfall did not significantly affect density of Tetranychus urticae (Koch) on soybean. Nagesha-Chandra and Channabasavanna (1983) found no significant relationship between rainfall and total population of RPM, although egg, larval and nymphal stages were found to be significantly affected. Other factors such as changes in plant physiology from stressed to unstressed induced by drought conditions may also have impacted on RPM densities. No entomopathogens were observed during this study. The relationship between phytoseiid density (all spp.), temperature and humidity and RPM density was also investigated but just on coconut as data was not sufficient on areca nut. This showed that there was a positive and significant interaction between all three factors on RPM density, and thus the importance of phytoseiids as a factor in this system.

13 Phytoseiids were the most abundant predator collected during the surveys even though the related phytoseiid complex had little impact on the RPM densities on areca. It was found that in four out of the seven months of the study period, there were significantly more phytoseiids on coconut. On coconut, phytoseiid densities were marginally significantly related to RPM density the previous month on coconut indicating a weak numerical response. More detailed experimental work is now needed to clarify the exact impact of phytoseiids on RPM on coconut. The most abundant predator collected in association with RPM was A. largoensis which supports findings by other studies where predators have been sampled in association with RPM (Pena et al. 2009; Ramos-Lima et al. 2010; Zannou et al. 2010), but contradicts findings by previous research in the area where A. channabasavanni was found to be the most abundant predator (Daniel 1979). Amblyseius tamatavensis species group was sampled on two occasions (one in association with a RPM colony) and both specimens were female. Amblyseius tamatavensis species group consists of A. tamatavensis and A. channabasavanni and using the key by Denmark and Muma (1989), the specimens identify as A. tamatavensis. But the specimens are also consistent with the type description of A. channabasavanni (Gupta 1978). As it stands, the descriptions of A. channabasavanni by Denmark and Muma (1989) and Gupta (1978) do not agree; thus further investigations into the taxonomy of this group and inspection of type specimens are required before a species name can be confirmed. Previous phytoseiid predators collected in association with RPM in south India have included Amblyseius raoiellus (Denmark and Muma 1989) from South Kanara district in Karnataka state and A. channabasavanni (Daniel 1979) on areca in Kerala. It is not clear why only two specimens of A. tamatavensis species group were collected during the present surveys, if indeed it is synonymous with that observed by Daniel (1979). It is also unclear as to why A. largoensis has not been collected in previous surveys and found in abundance in this study. Further surveys throughout successive seasons would confirm whether this is an anomalous year or whether this is generally the case. With reference to the other species collected (A. largoensis species group and E. ovalis), it is unlikely that they play an important role, if any in the regulation of RPM populations as they were rarely (A. largoensis species group) or never (E. ovalis) found in association with RPM. The lack of phytoseiids collected on areca from March onwards warrants further investigation and as this study only spanned one season, further collections may find different results. McMurtry and Croft (1997) stated that generalist predators such as Amblyseius spp. may be more evolved towards the conditions on the host plant rather than the prey itself and may also be strongly influenced by leaf anatomy. The high localised RPM populations on areca may represent those not regulated by the phytoseiid complex and the significantly lower numbers on coconut showing the opposite. Weakness of numerical response to prey is common for generalists such as Amblyseius spp. (a type III generalist) (McMurtry and Croft 1997), however the general predation pressure appears to have kept populations lower on coconut than areca. It has been suggested that as part of a biological control programme generalists should be integrated with specialists on stable long term perennial crops (Croft et al. 2004), but no specialist species were found during the surveys in Kerala. The weak numerical response of the species observed may suggest that they are feeding on other prey also and are not a biotype specifically adapted for predation on RPM, however there was evidence to suggest that A. largoensis was strongly associated with the presence of RPM. Climatic factors may also be important in influencing predation. Holtzer et al. (1988) demonstrated that the lack of synchrony between spider mites and a generalist predator may be related to different responses to leaf

14 micro-environment. As leaf temperature increases, the relative humidity of the boundary layer decreases (exacerbated by low stomatal conductance and aided by higher wind speeds), and the survival of eggs of generalist phytoseiid predators and the longevity of female lifespan have been shown to decrease at lower relative humidity. In the present study, notably on areca, there was a positive relationship with temperature for RPM population growth and a significant negative relationship for phytoseiids against temperature. The implications of these findings for a future classical biological control of RPM in the New World suggest that phytoseiid predators might be best chosen on the basis of host plant specificity as species differed between coconut and areca; it is not clear however, whether there is a geographical element to these observations and studies where the two different host plants are grown in the same area would give insight into whether species differences were related more to geography or host plant. In addition, it is not clear how much these predators might be limited by local climatic conditions and thus their performance under a range of temperatures and humidities also need further study. Acknowledgments This study was funded by the USDA, Agricultural Research Service. (Agreement no F041). The authors thank: the Director, Kerala Forest Research Institute, Peechi, Kerala for hosting the project and facilitating the transfer of specimens for identification under an Indian material transfer agreement; Dr B Mallik, University of Agricultural Sciences Bangalore and Dr Don Griffiths for mite identifications and advice on taxonomic points. References Carrillo D, Navia D, Ferragut F, Pena JE (2011) First report of Raoiella indica (Acari: Tenuipalpidae) in Colombia. Fla Entomol 94:370 Cocco A, Hoy MA (2009) Feeding, reproduction, and development of the red palm mite (Acari: Tenuipalpidae) on selected palms and banana cultivars in quarantine. Fla Entomol 92: Croft BA, Blackwood JS, McMurtry JA (2004) Classifying life-style types of phytoseiid mites: diagnostic traits. Exp Appl Acarol 33: Daniel M (1979) Survey of the indigenous predators of arecanut phytophagous mites. In: Venkata CS (ed) Proceedings of the second annual symposium on plantation crops: plant protection (entomology, microbiology, nematology, plant pathology and rodentology), pp Denmark HA, Muma MH (1989) A revision of the Genus Amblyseius Berlese, 1914 (Acari: Phytoseiidae). Occ Pap Florida St Coll Arthr 4:1 149 Estrada-Venegas E, Martinez-Morales H, Villa-Castillo J (2010) Raoiella indica Hirst (Acari: Tenuipalpidae): first record and threat in Mexico In: de Moraes GJ, Castilho RC, Flechtmann CHW (eds) Abstract book: XIII international congress of acarology, August Recife-PE, Brazil, p 77 Flechtmann CHW, Etienne J (2004) The red palm mite, Raoiella indica Hirst, a threat to palms in the Americas (Acari: Prostigmata: Tenuipalpidae). Sys Appl Acarol 9: Gupta SK (1978) Some Phytoseiidae from South India with descriptions of five new species. Oriental Ins 12: Hirst S (1924) On some new species of red spider. Ann Mag Nat Hist 14: Holtzer TO, Norman JM, Perring TM, Berry JS, Heintz JC (1988) Effects of microenvironment on the dynamics of spider mite populations. Exp Appl Acarol 4: Kapur AP (1961) A new species of Stethorus Weise S. keralicus (Coleoptera-Coccinellidae), feeding on arecanut palm mites Raoiella indica Hirst. in Kerala, southern India. Entomophaga 6:35 38 Klubertanz TH, Pedigo LP, Carlson RE (1990) Effects of plant moisture stress and rainfall on population dynamics of the two-spotted spider mite (Acari: Tetranychidae). Environ Entomol 19: McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Ann Rev Entomol 42: Moutia LA (1958) Contribution to the study of some phytophagous Acarina and their predators in Mauritius. Bull Entomol Res 49:59 75

15 Nagesha-Chandra BK, Channabasavanna GP (1983) Studies on seasonal fluctuation of the population of Raoiella indica (Acari: Tenuipalpidae) on coconut with reference to weather parameters. Indian J Acar 8: Navia D, de Moraes GJ, Marsaro A, Gondim M, da Silva FR, De Castro T (2010) Current status and distribution of Raoiella indica (Acari: Tenuipalpidae) in Brazil In: de Moraes GJ, Castilho RC, Flechtmann CHW (eds) Abstract book: XIII international congress of acarology, August Recife-PE, Brazil, p 173 Pena J, Mannion CM, Howard FW, Hoy MA (2006) 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 IFAS extension document EENY-376 (IN680). Accessed March 2010 Pena JE, Rodrigues JC, Roda A, Carrillo D, Osborne L (2009) Predator-prey dynamics and strategies for control of the red palm mite (Raoiella indica) (Acari: Tenuipalpidae) in areas of invasion in the Neotropics. Integrat Control Plant Feeding Mites IOBC/WPRS Bull 50:69 79 Purseglove JW (1972) Tropical crops: monocotyledons, 2nd edn. Longman Group Limited, London R Development Core Team (2009) R: A language and environment for statistical computing (version 2.7.2). Vienna, Austria, R Foundation for Statistical Computing. Available from Ramos-Lima M, Gonzalez A, Gonzalez M (2010) Management strategy of Raoiella indica Hirst in Cuba, based on biology, host plants and seasonal occurrence and use of acaricide. In: de Moraes GJ, Castilho RC, Flechtmann CHW (eds) Abstract book: XIII international congress of acarology, August Recife-PE, Brazil, pp 218 Rao PGSLHV, Sebastian S (1994) Estimation of leaf area in tree crops. J Plant Crops 22:44 46 Sarkar PK, Somchoudhury AK (1989) Influence of major abiotic factors on the seasonal incidence of Raoiella indica and Tetranychus fijiensis on coconut. In: Channabasavanna GP, Viraktamath CA (eds) Progress in Acarology, vol 2. Oxford and IBH Co. Pvt. Ltd., New Delhi, pp Sayed MT (1942) Contribution to the knowledge of the Acarina of Egypt: I. The Genus Raoiella Hirst (Pseudotetranychidae-Tetranychidae). Bull Soc Fouad I Ent 26:81 84 Smith TR, Dixon WN (2008) 2007 Florida CAPS red palm mites survey 2nd interim report, October 2006 January Florida Cooperative Agricultural Pest survey Programme Report No RPM-02 Somchoudhury AK, Sarkar PK (1987) Observations on natural enemies found in association with coconut mite, Raoiella indica Hirst. Bull Entomol (New Delhi) 28: Southwood TRE, Henderson PA (2000) Ecological methods, 3rd edn. Blackwell, Oxford, UK Vásquez CN, de Quirós G, Aponte O, Sandoval DMF (2008) First report of Raoiella indica Hirst (Acari: Tenuipalpidae) in South America. Neotrop Entomol 37: Welbourn C (2006) Red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae). Pest alert. Accessed March 2010 Yadavbabu RK, Manjunatha M (2007) Seasonal incidence of mite population in arecanut. Karnataka J Ag Sci 20: Zannou I, Negloh K, Hanna R, Houadakpode S, Sabelis M (2010) Mite diversity in coconut habitat in West and East Africa. In: de Moraes GJ, Castilho RC, Flechtmann CHW (eds) Abstract book: XIII international congress of acarology, August Recife-PE, Brazil, p 295