Seasonal Abundance of Brevipalpus phoenicis ( Acari : Tenuipalpidae ) and Its Predators and Their Effects on Gerbera jamesonii Morphology

Citation: Egypt. Acad. J. Biolog. Sci. (A. Entomology) Vol.9 (4)pp. 129140(2016) Egyptian Academic Journal of Biological Sciences is the official English language journal of the Egyptian Society for Biological Sciences, Department of Entomology, Faculty of Sciences Ain Shams University. Entomology Journal publishes original research papers and reviews from any entomological discipline or from directly allied fields in ecology, behavioral biology, physiology, biochemistry, development, genetics, systematics, morphology, evolution, control of insects, arachnids, and general entomology. www.eajbs.eg.net Provided for non-commercial research and education use. Not for reproduction, distribution or commercial use.


INTRODUCTION
Ornamental plants are grown widely to enrich the beauty of home gardens and parks but nowadays it represents a threat to the environment after being attacked by several insects and mites.Such mites mainly belong to families Tetranychidae, Tenuipalpidae, Eriophidae, Acaridae and Tarsonemidae (Ripka, 1998;Zhang, 2003).
Gerbera jamesonii Bolus is an ornamental member of the sunflower Asteraceae (Compositae) of great commercial value.Because of its colour, long vase life and ability to rehydrate after long transportation, it became in demand from floral industry as cut flower as well as potted plant (Lorenzi & Souza, 2000;Kanwar & Kumar, 2008).It is one of the ten most popular commercial cut flowers in the world ranked the fifth after rose, carnation, chrysanthemum, and tulip (Solgi et al., 2009).Besides its great commercial value it was recorded as the best air-filtering houseplants that absorbs the indoor gases and increased the quality of indoor air, according to NASA (Wolverton et al., 1989;Richard, 2012).It was also used as a control strategy in many crops, either as a trapping/banking plant or as a trapping/killing plant (Blumthal et al., 2005).
Nowadays, B. phoenicis has been registered on G. jamesonii which is famous being attacked by Tetranychus urticae worldwide and it is as one of its main pests (Burdajewicz & Pelczynska, 1978;Nucifora & Calabretta, 1986;Bolland et al., 1998;Krips et al., 2001;Silva et al., 2009;Sulzbach et al., 2015).B. phoenicis feeds on the lower surface of leaf, in particular on the sap then inject toxic saliva into fruits, leaves, stems, and bud tissues of their host plant.Severe infestations lead to yellowing and drought in the plants affecting its growth thus their product quality reduced and lacking its marketability (Lazarova, 1975;Childers & Rodrigues, 2011).
It was known that Brevipalpus sp. was not important as spider mites according to Baker (1949) who first described Brevipalpus species but after various studies, it was evident that the genus Brevipalpus can be serious plant pests (Childers et al., 2001;Parrella et al., 2014) as they are vectors of one or more cytoplasmic or nuclear plant viruses (Childers & Rodrigues, 2011;Alberti & Kitajima, 2014).So that because of its potential threat of introduction of one or more serious viral diseases into other crops, it is essential to shed light on this dangerous family as they are known to be long-lived and maintain their abilities to move from their main host (citrus or coffee) to other host plants (Childers et al., 2003 a, b).
The goal of this study is to obtain a more complete picture of the monthly variations on abundance and prevalence of B. phoenicis life stages, its predators and other pests infesting G. jamesonii under the influence of temperature, humidity, wind speed, rainfall, and sunshine hours.Additionally, the effects of mite's infestation on morphology and photosynthetic pigments of G. jamesonii were studied.

Study site
The field experiments were conducted in a nursery of Faculty of Agriculture, Suez Canal University, Ismailia, located in Ismailia-Cairo desert road north-eastern Egypt.

Experiment (1): Seasonal abundance & prevalence of B. phoenicis life stages and its associated predators on G. jamesonii
The effect of monthly variations in temperature, relative humidity, sunshine hours, wind speed and rain on abundance and prevalence of B. phoenicis life stages and its associated predators on G. jamesonii were conducted for one year 2015.
Twenty leaves were collected monthly from the studied plants.Five leaves were selected from 4 plants, collected randomly and carried to the laboratory using separate polythene bags.Every plant served as a replicate.They were examined under stereo-binocular microscope in the laboratory.Different stages of flat mite viz.eggs, larvae, nymphs and adults, were counted.Field temperature (in degree Celsius), relative humidity (in percent), sunshine hours (in hrs.), wind speed (in Kilometers/hour) and rain (in millimeters) were obtained from the Central Laboratory for Agricultural Climate (CLAC), Agriculture Research Center, Egypt.

Experiment (2): Effects of B. phoenicis infestation density on morphological characteristics and photosynthetic pigments of G. jamesonii
For studying the possible effects of mite infestation density on some morphological characteristics of G. jamesonii, the leaf, flower, and bud numbers were counted in addition to the deformation in the flowers and length of main stem.G. jamesonii plants were divided into four groups: heavy, moderate, and mild infestations beside the control groups within a complete randomized block design consisting of five replicates per treatment at the same selected nursery.At each sampling date, ten leaves per plant were examined under a stereomicroscope and the egg, nymph, and adult stages of B. phoenicis per leaf were counted.The experiment was conducted during spring.

Estimation of photosynthetic pigments
At the end of experiment (last week of sampling), plant leaves were collected for photosynthetic pigments test.The level of chlorophyll a (Chl.a), chlorophyll b (Chl.b), total chlorophylls (Chl.) and carotenoids (Car.) in leaves were determined from acetone extract after Wettstein (1957) and expressed as mg g -1 leaf fresh mass.Each sample was consisted of 5 leaves per repetition.The absorbance was recorded at 645 and 663 nm for chlorophyll assay and 480 nm for carotenoids assay by spectrophotometer (Unico UV/VIS 2100, USA).

Statistical analysis
The percentage of infested leaves to non-infested one was calculated.Abundance, the number of individuals found per sample, was calculated and represented as Mean (±SE).To satisfy the assumption of statistical analysis used, all the data were normalized by log (x+1) transformation to achieve linearity.Analysis of variance was used for studying the significant differences between groups regarding the effects of monthly and site variations.All the statistical tests were performed by using the software packages SPSS 15.0.0 (USA).

RESULTS AND DISCUSSION
Unfortunately, Gerbera sp.make excellent host for different insect pests to the extent of being used as a trap plant for different pests especially western flower thrips, Frankliniella occidentalis which is its main pest with spider mites (Blumthal et al., 2005;Spiers et al., 2006).
Until very recently, little data dealing with interactions between G. jamesonii and false spider mites were available.All the studies dealt with the fact that T. urticae is key pest of Gerbera sp.In contrast to our findings, that the B. phoenicis is the main pest affecting G. jamesonii.This was in agreement with Silva et al. (2009) and Sulzbach et al. (2015) who evaluated in Brazil the abundance of T. urticae in three varieties of G. jamesonii Adlam.Also, in Iran and India the T. urticae was recorded on Gerbera sp.(Pal & Sarkar, 2009;Haghghadam & Arbabi, 2012).
Regarding the effect of monthly variations on abundance and percentage of infested leaves with different stages of B. phoenicis and other pests on G. jamesonii, results showed significant effects as shown in Tables (1 & 2).B. phoenicis adults density per leaf was found maximum in January (50.25±6.08)whereas it was minimum in October (4.10±0.83)(P <0.000).The infestation rate of leaves with B. phoenicis adults was ranged from 85 to 100%.Eggs density per leaf was found maximum in May (71.85±8.57)whereas it was minimum in September (10.30±2.09)(P <0.000).The infestation rate of leaves with B. phoenicis eggs was 100%.The larval population density per leaf was maximum in January (31.40±4.71)and minimum during August (1.95±0.46)(P <0.000).The infestation rate of leaves with B. phoenicis larvae was ranged from 75 to 100%.The nymphal population density per leaf was maximum in July (74.43±8.73)and minimum in August (16.10±2.50)(P <0.000).The infestation rate of leaves with B. phoenicis nymphs was 100%.

Mealy bugs
These findings were in agreement with Rezk (2001) who recorded the Brevipalpus obovatus as a major pest of citrus trees in Egypt with a peak in February (21.23±0.8mites/30 leaves) then decreased in September-November ranging between (15.7±1.2 and 18.39±0.9mites/30 leaves) then declined sharply in August.In accordance, the results also agree with the findings of Rizk et al. (1978), Raizer et al. (1988), andSadana &Kumari (1991).
On the contrary, Karmakar & Saha (2005) found that B. phoenicis increased during October (15.l3 mites/leaf) and thereafter decreased with a minimum level in January (0.20 mites/leaf).Also, a peak of B. phoenicis population on guava was reported on November-December by Kumari & Sadana (1995).These observations were in similarity with the earlier findings of Patel & Karmakar (2005) who recorded that maximum population of B. phoenicis in pointed gourd was in September.Also, Pal & Sarkar (2009) recorded T. urticae on Gerbera sp. in June, July, August, and September.In addition, Shah & Shukla (2014) found that T. urticae on Gerbera sp. was maximum in July (12.86 mites/leaf).
In Egypt, tenuipalpidus are the most important fruit tree pests (Zaher & EL-Badry, 1964;Yousef, 1967;Wafa et al., 1969).The genus Brevipalpus was first recorded in Egypt by Attiah (1956) on pear, quince, vines and ornamental plants with no males of B. inornatus, B. phoenicis or B. lewisi have been observed in Lower and Upper Egypt.B. phoenicis has been registered lately on Gerbera sp.(Childers et al., 2003b) with no studies on its abundance and prevalence on ornamentals as they weren't preferred hosts.B. phoenicis population varied significantly on different months of the year on G. jamesonii as being a perennial herb host they persist on it throughout the year.
A. cucumeris was recorded in February, May, June, and November.Its density per leaf was maximum in November (0.25±0.09) whereas it was minimum in February (0.10±0.07) (P <0.000).Concerning H. wellsina, it was recorded in April, June, July, September, October, and December.Its density per leaf was maximum in October (1.20±0.54)whereas it was minimum in December (0.04±0.03) (P <0.000).Concerning Tydeus sp., it was recorded all the year except September.Its density per leaf was maximum in February (11.85±4.33)whereas it was minimum in October (0.05±0.05) (P <0.000).Concerning S. longicornis, it was recorded in April, July, September, October, November, and December.Its density per leaf was maximum in July (0.50±0.18) whereas it was minimum in December (0.04±0.03) (P <0.000).Negative correlations were found between B. phoenicis egg or larvae was recorded with S. longicornis (-0.122, -0.168), respectively.
However, the population decline of B. phoenicis happened also without being affected by predators.In contrast to our results, Lacordaire (2011) recorded the following predators Phytoseiulus persimilis and Feltiella acarisuga on G. jamesonii who are not always sufficient for a good control of T. urticae.In addition, De Moraes & Tamai (1997) stated that Tetranychus sp. and P. persimilis was commonly found attacking ornamentals in production plants and indoor landscaping.In Iran, Haghghadam & Arbabi (2012) recorded Tydeus sp.only on ornamental plant (Acalypha hispida) which is similar to the present study.However no previous studies were found concerning the effects of temperature on predators.
The impact of environmental factors on mite population abundance were studied and illustrated in Table (3) and Figure (1).The B. phoenicis adult had a highly significant negative correlation with TºC, RH% and sunshine hrs.whereas it had a positive correlation with wind speed and rain.B. phoenicis eggs had only a positive significant correlation with sunshine (hrs.) while larvae had a highly significant negative correlation with TºC and a significant positive correlation with rain and sunshine hrs.B. phoenicis nymphs had a highly significant positive correlation with TºC, RH% and sunshine (hrs.) and a negative significant correlation with wind speed and rain.The changes of the climatic conditions have determined the proliferation and dispersion of several pests associated with parks and ornamental gardens like tetranychid, eriophyid and tarsonemid mites (Gutue et al., 2012).The B. phoenicis adults and larvae had a negative significant correlation with temperature this was in agreement with Gupta et al. (1976) and Baradara et al. (2001) who indicated the negative correlation between TºC and T. cinnabarinus developmental stages and also female longevity studied on Gerbera sp.On the other hand, Shah & Shukla (2014) showed a non-significant negative correlation between T. urticae populations and temperature.
Concerning humidity, B. phoenicis adults had a significant negative correlation with relative humidity in agreement with Sağlam & Çobanoğlu (2010) who found a negative correlation between B. phoenicis density and relative humidity on pelargonium in Turkey.In contrast, Karmakar & Saha (2005) found that B. phoenicis had a positive correlation with temperature and relative humidity whereas correlations with other meteorological parameters were found to be non-significant.The positive influence of relative humidity on the population of mites was also reported by Gupta et al. (1976) and Shah & Shukla (2014) who showed a significant positive correlation between relative humidity and T. urticae population on Gerbera sp.Hence our study reflects great variations of temperature effects on B. phoenicis life stages and also on its predators.
The effect of B. phoenicis adult, egg, and nymph stages on the morphological characteristics of G. jamesonii during spring was shown in Tables ( 4) and ( 5).There were high significant negative correlations between B. phoenicis life stages and leaf, flower, bud numbers, and length of flowering stem while a positive significant correlation was found with deformed flower numbers.The physiological and morphological changes of plants caused as a result of mites' infestation that lead to various biochemical changes in plants minerals, inorganic and organic compounds (Shree & Nataraja, 1993).Polyphagotarsonemus latus (Tarsonemidae) are often found damaged Gerbera leaves which split have a rugged appearance followed by discoloration or blistering.It also injured flowers which became distorted with discoloured rays.Cyclamen mite, Phytonemus pallidus (Banks) (Tarsonemidae) in addition to damaging leaves, reducing its size; it affects rays of flower which are deformed when attacked in the bud stage.Also Bulb mite, Rhizoglyphus echinopus, when feeding in the bud stage, results in malformation of the flower base (Zhang, 2003).Breviplapus californicus when feeding resulted in the formation of rounded leaves that were severely stunted, marginal necrosis appeared and end with burned leaf tip.Mite also affected the new shoot growth with the formation of corky swollen buds referred to as Brevipalpus gall by Knorr & Denmark (1970).Table ( 6) showed the effect of B. phoenicis adult's infestation on total Chl., Chl.a, Chl.b and carotenoids in G. jamesonii leaves.There is high significant negative correlation between adult mite numbers and total Chl.while positive significant correlation was found with Chl.a, Chl.b, and carotenoids.The decrease in chlorophyll level is due to mechanical damage of chloroplasts of leaves due to mite feeding or it may be due to discoloration of chloroplasts.In agreements with our results, Kolodoziej et al. )1979 ( indicated positive correlation between increases in mite density with decrease of chlorophyll.Chatterjee & Gupta (1997) reported chlorophyll damage to the extent of 33.62% on Luffa acutangula due to infestation of Tetranychus ludeni.Parađiković et al. (2008) showed that Chl.b concentration was correlated to longer flower stem length in G. jamesonii.A reduction in the chlorophyll content is a primary response to spider mite infestation and has been reported in many plants including rose (Landeros et al., 2004), cotton (Reddall et al., 2004), and bean (Farouk & Osman, 2011).It was found that decrease in Chl. a was more pronounced than Chl.b at different stages of T. urticae infestation.Also, a great loss in leaf carotenoid content of bean leaves as a result of T. urticae infestation was reported by Farouk & Osman (2011).In corroboration with our studies, Landeros et al. (2004) reported that the chlorophyll content of rose was negatively correlated with T. urticae population density.The change in amount and rate of the chlorophyll depend on T. urticae density and duration of feeding (Alatawi et al., 2007).Since little data dealing with interactions between Gerbera sp. and false spider mites were available, few data on mite's infestation effects on chlorophyll contents are available.
In conclusion, G. jamesonii is recorded as a new host for B. phoenicis with a marked deformation in the plant morphology.In addition, environmental factors had a great effect on its abundance hence further studies are needed to assess most congenial period for this mite to develop better management strategy for pest control to increase ornamental plants productivity.

Table 1 :
Monthly variations of B. phoenicis life stages (mean ± SE), its predators, and other pests infesting G. jamesonii during one year survey 2015.

Table 2 :
Percentage of infested leaves with B. phoenicis (life stages), its predators, and other pests infesting G. jamesonii during one year survey 2015.

Table 3 :
Correlation between B. phoenicis (life stages), its predators, other pests infesting G. jamesonii, and weather factors during one year survey 2015.

Table 4 :
Effect of B. phoenicis adult, egg, and nymph stages on the morphological characteristics of G. jamesonii during spring 2015.

Table 5 :
Correlation between density of B. phoenicis adult, egg and nymph stages and the morphological characteristics of G. jamesonii during spring 2015.Gerbera sp. is infested with different mite species causing a great morphological deformation in leaf, flowers, and even buds.Broad mites,

Table 6 :
Effect of B. phoenicis adult's infestation on Total Chl., Chl.a, Chl.b, and carotenoids in G. jamesonii leaves.Adult mite no.expressed as average no. of mites/ sq.cm leaf.