Predatory Spiders Associated with the Two Spotted Spider Mite Tetranychus urticae on Two Field Crops in Qalubyia Governorate, Egypt

Citation: Egypt. Acad. J. Biolog. Sci. (A. Entomology) Vol.9 (4)pp. 7181 (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
Spiders are considered to be one of the most important predators which can be used as biological control agents regulating populations of mites, insects and other important agricultural pests by feeding on all life stages of the prey (Nyffler et al., 1994;El-Naggar et al.,1999;El-Erksousy et al., 2002;Ibrahim et al. 2012).In Egypt, biological, ecological and taxonomical studies concerning spiders as predators of the spider mites have not yet been adequate to determine which species can be used as a biological control agent of the two spotted spider mite, Tetranychus urticae (Hussein et al., 1998;El-Naggar et al., 1999;El-Erksousy, 2000).
The present study determines percent occurrence of spider families associated with the two spotted spider mite, T. urticae and their abundance on clover and cotton crops at Qaha research station in Qalubyia governorate during two successive years, 2013 and 2014.Also, laboratory studies investigate the life duration, food consumption and predation rate of immature stages and adult females of three spider species (representing 3 of the most abundant spider families) when fed on adults of T. urticae.The present study offers basic knowledge of some ecological and biological aspects which are required for further understanding and in the assessment of the mite-predator relationships between T. urticae and naturally associated spiders.

Ecological studies:
Different life stages of Tetranychus urticae and associated spiders on cotton and clover crops at Qaha research station in Qalubyia governorate, Egypt were collected from 10-20 plants bi-weekly during two successive years, 2013 and 2014 as described by Ibraheem (2016).Spiders were mostly identified to their families (Katson, 1978;El-Hennawy, 2002).Monthly temperature and relative humidity were obtained from the meteorological station in the form of maximum, minimum and average monthly temperature and relative humidity.

Biological studies: Spider laboratory colony:
Laboratory colonies of 3 species of the most abundant predatory spider families associated with the collected mite T. urticae were established.Adults of 20 males and 20 females of each of the selected species, Thanathus albini, Steatoda triangulosa and Thomisus spinifer were placed in pairs into glass tubes and supplied with newly hatched preys of the first larvae of Spodoptera littoralis and adult T. urticae, then each tube was thoroughly covered by a muslin cloth.The tubes were kept in an incubator at 27± 2˚ C and 60 -70 % RH and feeding was continued till the spiders laid the egg sacs.The newly hatched spiderlings were transferred to separate tubes and supplied with preys to complete their life cycle till adult stage.

Predation of spiders on Tetranychus urticae:
Egg-sacs of the selected spiders were kept in the laboratory at 27 ± 2˚C & 60 -70% RH till hatching of spiderlings.The progeny of 20 newly hatched spiderlings were separated individually in glass tubes of 7 cm long and 3 cm diameter then covered by a muslin cloth fixed by a rubber band.The first spiderlings were provided daily with 5 preys of adult females or males Tetranychus urticae.The number of preys was increased to 10 at the second spiderling and to 15 at the third spiderling daily till the end of the experiment.
Ten adult females were placed individually in glass tubes of 7 cm long and 3 cm diameter then covered by a muslin cloth and kept at 27 ± 2˚C & 60 -70% RH.Each female was provided daily with 25 to 30 adult males or females T. urticae till the end of the experiment.The number of consumed prey, daily predation rate and duration of each life stage was calculated.

Statistical analysis:
The obtained results from seasonal abundance of T. urticae and spiders movable life stages on the clover and cotton crop were analyzed by statistical package of Social Science (SPSS), version 20 for windows.In the experiments of spider stages duration, food consumption and predation rate, data were subjected to analysis of variance (ANOVA) and the means were compared by L.S.D. test mostly at 0.05 level, using SAS program.
Most of the families started appearance with small numbers on clover in early winter in January (Dictynidae, Saltcidae, Lycosidae, Philodromidae, Thomisidae, Therdiidae, Linyphiidae, and Araneidae) in one or both years of study.Others appeared late in March (e.g Eutichuridae (Miturgidae) and Agelenidae).The monthly collected total number of spiders gradually increased to reach peaks of 58 and 23 spiders in May constituting 45.67% and 28.05% of the season total collected spiders (127 & 82) on clover in 2013 and 2014 , respectively.
Most of the families started appearance with small numbers on cotton in late spring in May (Salticidae, Eutichuridae (Miturgidae), Thomisidae, Philodromidae, Theridiidae) and others appeared in summer in June (Dictynidae and Gnaphosidae), July (Araneidae), and August (Linyphiidae) in one or two seasons.The total monthly collected spiders gradually increased to reach peaks of 62 & 52 spiders on cotton in September constituting 31.16% and 34.67% of the season total collected spiders on cotton (199 & 150) in 2013 and 2014, respectively, then decreased in October at the end of the cotton season.
In comparison with clover, the total numbers of spiders collected in the two years of study and in each of 2013 and 2014 were higher on cotton (349, 199 & 150, respectively) than on clover (209, 127 & 82, respectively) and in 2013 than 2014 on each of clover and cotton.

Population density of spiders and their prey of Tetranychus urticae on clover and cotton:
Figs. (1a, 1b) show that the monthly population density of the predatory spiders (movable stages) collected on clover in 2013 and 2014 gradually increased with the increasing number of monthly population of the prey T. urticae nearly up till the prey peak in March.This was followed by a decrease of the prey population in next months (April & May) at the end of the clover season.However, the monthly collected predatory spiders continued increasing to reach a maximum of 58 and 23 spiders in May 2013 and 2014, respectively, while the climate mean temperature was increased.On cotton, the pattern of changes of the population density of the monthly collected predatory spiders ran nearly in parallel to that of the prey population throughout each season (Figs.2a, 2b).Both the prey and predator increased to reach their population peaks of 28 mites & 62 spiders and 34 mites & 52 spiders in September 2013 and 2014, respectively followed by a decrease in October.During the cotton season the climate mean temperature gradually increased from May to August followed by a slight gradual decrease in September and October in each of 2013 and 2014.

Life stage duration, food consumption and predation rate of immatures and adult females of spiders fed on Tetranychus urticae:
Thanatus albini, Steatoda triangulosa, Thomisus spinifer were selected as representative species of three of the most common families (Philodromidae, Theridiidae, Thomisidae, respectively) of predatory spiders collected in the present work.Life stage duration, food consumption and predation rates of early immatures and adult females of the selected three spiders species fed on adult male and female T. urticae are shown in Tables (1-4).

Life stage duration, food consumption and predation rate of early immatures of Thanatus albini, Steatoda triangulosa and Thomisus spinifer fed on adult T. urticae:
The duration of the first, second and third spiderlings of the 3 tested spider species varied and was the shortest (p<0.05) in the first spiderling of T. albini and T. spinifer and the third spiderling of S. triangulosa in comparison to the other two spiderlings.Also, the spiderling duration of each stage was slightly longer (p<0.05)when fed on female T. urticae than male with the longest total duration in T. spinifer followed by S. triangulosa and T. albini, respectively.
Results in Tables (1-3), showed that the 3 early immature stages of the 3 tested spider species consumed different numbers of adult female and male T. urticae during the life period of the spiderlings.The number of consumed adults of T. urticae per spider was the least in the first spiderling and gradually increased in the second and third spiderlings (p<0.001) with more consumption of adult females than males T. urticae (p<0.05).The highest total consumption of the adult mites was in T. spinifer followed by T. albini and S. triangulosa,respectively.The predation rate (no. of preys consumed/ spider/ day) of the early immatures of the tested spider species was the lowest (p<0.05) in the first spiderling and gradually increased in the second and third spiderlings of each species but mostly with no significant difference (p>0.05) between predation rates of the corresponding spiderling stages which were fed on T. urticae females and males in each species.The highest predation rates occurred in the 3 rd & 2 nd spidrlings (p<0.05) of T. albini followed by T. spinifer and S. triangulosa, respectively.

Life stage duration, food consumption and predation rate of adult female spiders fed on adult Tetranychus urticae:
Results represented in table (4) showed that adult females of the three selected spider species, T. albini (F.Philodromidae), S. triangulosa (F.Theridiidae), and T. spinifer (F.Thomisidae) were able to survive for relatively short periods 2.9-8 days when fed solely on adult T. urticae.The duration of survival periods was the longest in female T. albini followed by T. spinifer then S. triangulosa (p<0.05),respectively, when they were fed on adult females or males of T. urticae.During the relatively short survival period, female T. albini consumed the largest numbers of female and male T. urticae followed by T. spinifer then S. triangulosa with more consumption of females than males T. urticae (p<0.001) in the three species.
The predation rates of the 3 tested female adult spiders (p<0.05) was the highest in T. when fed on female and male T. urticae followed by T. albini and S. triangulosa with slightly higher predation rates on females than males T. urticae except in case of S. triangulosa where no significant difference (p>0.05) was observed.

Spider families associated with Tetranychus urticae on clover and cotton crops
Ecological and biological studies have been carried out on spiders in Egypt (e.g.El-Heneidy et al., 1996;Metwally et al., 2002;Abo-zaed, 2008;Ibrahim et al., 2012).However, studies on spiders associated with T. urticae or other acarine pests are scarce (El-Erksousy, 2000).In the present study, 558 spiders belonging to 11 families of order Araneae associated with T. urticae were collected on clover and cotton at Qaha research station in Qalubyia governorate, Egypt during two successive years, 2013 and 2014.Salticidae was the most abundant of the total collected spiders on the two crops, followed by Theridiidae, Thomisidae, Philodromidae, Dictynidae, Eutichuridae (Miturgidae), Araneidae, Linyphiidae, Lycosidae, Agelenidae, and Gnaphosidae.Many of these families were recorded in different governorates, localities and crops in Egypt (Gabboiur et al., 1996;Hussein et al., 1998;El-Erksousy, 2000;Metwally et al., 2002, Abo-zaed, 2008).The numbers of the collected spiders, percent occurrence and hence abundance of each family varied on each of the two studied crops in 2013 and 2014.
On clover, nine and seven of the aforementioned 11 spider families were collected in 2013 and 2014, respectively.The collected families did not include Gnaphosidae in both years in addition to Araneidae in 2013 and Lycosidae, Philodromidae, and Agelenidae in 2014.However, during the period of study, Theridiidae was the most abundant family on clover followed by Salticidae, Thomisidae, Philodromidae, Dictynidae, Linyphiidae, Lycosidae, Eutichuridae (Miturgidae), Agelenidae, and Araneidae.In accordance with the present study, Negm et al. (1976) found that Salticidae, Thomisidae, and Tetragnathidae were the best represented families of Araneae in clover fields in Assiut, Egypt.On cotton, nine and eight of the aforementioned 11 spider families were collected in 2013 and 2014, respectively.The collected families did not include Lycosidae and Agelenidae in both years in addition to Gnaphosidae in 2014.In contrast to the present findings Lycosidae was represented in Menofyia as the most dominant family on cotton and other plants in summer season (Gabboiur et al., 1996).The present study showed that Thomisidae was the most abundant family on cotton during the period of study followed by Salticidae, Theridiidae, Philodromidae, Araneidae, Eutichuridae (Miturgidae), Dictynidae, Linyphiidae, and Gnaphosidae.In Egypt, occurrence of spiders on cotton has been recorded in many governorates and localities (El-Heneidy et al., 1996;El-Erksousy, 2000;Abo-zaed, 2008;Ibrahim et al., 2012).Furthermore, many of the spider families on cotton in the present work were collected from other plants such as vegetables (Gabboiur et al., 1996;Soliman, 2003) fruits (Metwally et al., 2002) and field crops (Ibrahim et al., 2012).
Most of the spider families started appearance with low numbers on clover and cotton in winter (January) and late spring (May), respectively in both years of study.The monthly collected number of spiders gradually increased to reach maximum on clover and cotton at the relatively high temperature in May and September 2013and 2014, respectively. Li Diaqin & Jackson (1996) found that spiders live in warmer climates and their rate of growth, development and life history traits were affected by change in temperature.
In comparison with clover, the total numbers of spiders collected in both years of study and in each of 2013 and 2014, respectively, were higher on cotton than clover and in 2013 than 2014 on each crop.Qu et al. (1986) reported that spiders of order Araneae are closely correlated with the crop, occurrence of insect pests, farming practice, chemical application and climatic factors.In the present study, the relatively higher temperatures during cotton season (24.2-30.6˚C)than clover (11.9-25.5˚C)and preying of spiders on cotton pests might have contributed to the higher population densities of the spiders collected on cotton.The spiders feed well on the major cotton pests of noctuid larvae, the pink bollworm, Pectinophora gossypiella (El-Erksousy & Amer, 2007) and the cotton leaf worm Spodoptera littoralis (El-Erksousy, 2000;Abo-zaed, 2014) and other cotton pests as the aphid, Aphis gossypii and the leaf hopper, Empoasca sp.(Hendawy & EL-Mezzayen, 2003).Larvae of both noctuids are used for laboratory rearing of the spiders in Egypt (El-Erksousy, 2000).

Interrelationships of spiders and their prey Tetranycus urticae on clover and cotton:
Appearance of spiders and their prey of T. urticae started on clover in winter (January) and on cotton in late spring and summer (May & June), respectively in both 2013 and 2014.In each season, the numbers of the collected spiders and prey were the lowest at the start and gradually increased in next months.The increased monthly population density of the spiders continued together with that of T. urticae nearly in parallel during the whole cotton seasons with maximum in September (then decreased in October) and up till the prey peak in March in each clover season.However, although the population density of T. urticae on clover was decreased in next months following the peak (April & May), the monthly collected numbers of predatory spiders continued increasing to reach maxima at the higher mean temperatures in May (24.2 & 25.5˚C) than in March (19 & 21.58˚C).The continued increased density of the predator after the decrease of the prey density suggested a relative independence of the predatory spiders from T. urticae as a prey and pointed to another factor (s) or reason (s) of the observed increase.Climatic conditions especially temperature and relative humidity have been found to be the main factors affecting changes of population densities of the spiders (Costa, 1995;Abo-zaed, 2008) and T. urticae (Cai, 1987).In the present study, the low temperature in winter (January & February) might be the main reason of the low densities of T. urticae and spiders on clover and the increasing temperatures in spring contributed to the increased densities of T. urticae and spiders to peaks in March and May, respectively.
In comparison of the associated predatory spiders with T. urticae, the higher total numbers of the spiders movable stages on each of the clover and cotton in 2013 than in 2014 and on cotton than on clover in each year of study might have contributed to the lower number of T. urticae collected on clover and cotton in 2013 than 2014 and to the lower number T. urticae on cotton than clover in each year (Ibraheem, 2016).

Life stage duration, food consumption and predation rate of immatures and adult females of spiders fed on adult Tetranychus urticae:
Life stage duration, food consumption and predation rates of the 3 early immature stages and adult females of Thanatus albini, Steatoda triangulosa and Thomisus spinifer were determined by feeding the spiders on adult females and males of T. urticae.Generally the 3 parameters increased gradually by increasing age of the spiderlings from the first to the third stage (except duration in S. triangulosa).These results conform to most studies on other spider species fed on T. urticae (El-Erksousy, 2000) or other preys such as Pectinophora gossypiella (El-Erksousy & Amer, 2007) and Spodoptera littoralis (Abo-zaed, 2014).In the present study, food consumption and to less extent duration of spiderlings and adult females were higher when the spiders were fed on female than male adult T. urticae, but mostly no significant difference in the predation rates were observed on consuming male and female T. urticae.
In the present study, T. urticae as the only consumed food could not maintain the life of the female adult spider except for few days (2.9-8 days) or enable the early 3 spiderlings to complete the life cycle to adult stage which is similar to findings of Ibrahim et al. (2012).On the other hand El-Erksousy (2000) succeeded to complete the life cycle of the spiderlings of the Theridiid Crustulina conspicua (5-6 spiderlings) by feeding the predator on huge numbers of adult T. urticae (about 1822 & 2453 mites for male & female spiderlings).

Fig. 1a :
Fig. 1a: Population density of spiders and their prey of Tetranychus urticae on clover crop at Qaha station, Qalubyia governorate during 2013 season.
Fig. 2a: Population density of spiders and their prey Tetranychus urticae on cotton crop at Qaha station, Qalubyia governorate during 2013 season.

Table 1 :
Stage duration, food consumption and predation rate of the 3 early immature stages of Thanatus albini (F.Philodromidae) fed on adult male and female Tetranychus urticae at 27± 2˚C and RH 60-70%.

Table 2 :
Stage duration, food consumption and predation rate of the 3 early immature stages of Steatoda triangulosa (F.Theridiidae) fed on adult male and female Tetranychus urticae at 27± 2˚C and RH 60-70 %.

Table 3 :
Stage duration, food consumption and predation rate of the 3 early immature stages of Thomisus spinifer (F.Thomisidae) fed on adult male and female Tetranychus urticae at 27± 2˚C and RH 60-70%.

Table 4 :
Stage duration, food consumption and predation rate of female adult spiders fed on adult male and female Tetranychus urticae at 27± 2˚C and RH 60-70 %.