Host selection behavior of Diaeretiella rapae McIntosh (Hymenoptera: Braconidae) attacking cereal aphids

 in Upper Egypt

Alaa El-Deen A. A. Salem

Plant Protection Research Institute, Agricultural Research Center, Dokki, Giza, Egypt

Email address: alaazag @ yahoo.com

ABSTRACT :

      The present investigation was carried out in Assiut Governorate to study the relative abundance of cereal aphid parasitoids and evaluate the host selection and host-instar preference of Schizaphis graminum (Rondani) and Rhopalosiphum padi L. by the braconid parasitoid, Diaeretiella rapae McIntosh during 2015 wheat growing season. The obtained results revealed that the dominance percentages of the primary parasitoids were so high and presented by 81.53 % of the total caught parasitoids. However, the secondary parasitoids showed low dominance percentages and presented by 18.47 %. The parasitoids, D. rapae and Alloxysta australiae (Ashmead) revealed the highest dominance percentage and presented by 76.38 and 47.93 % of the total collected primary and secondary parasitoids, respectively. The aphid, S. graminum appeared as more relatively preferred for D. rapae than R. padi species. The development of D. rapae was found to be possible in any instar of S. graminum and R. padi. The second and third instars of S. graminum presented the optimal response for D. rapae growth and survival, while the third and fourth instars of R. padi presented the optimal response for parasitization by the same parasitoid species. The averages of the development times from oviposition until the appearance of the mummified aphid were 7.68 and 8.01days for S. graminum and R. padi, respectively. Offspring production per female was high in the adult stage than others. Nymphs parasitized and mummified by D. rapae during the first and second instars may be reach to maturity but not produce any progeny.

INTRODUCTION

Wheat is one of the main crops in cereal groups. Many pests attack wheat plants from planting up to harvest. The main insect pests attacking wheat are aphids (Kindler et al., 1991). In Egypt, four aphid species were recorded amongst cereal insect pests, i.e. Schizaphis graminum (Rondani), Rhopalosiphum padi L., R. maidis (Fitch.) and Sitobion avenae (Fab.). Also, five primary parasitoid species, i.e.

Aphidius colimani Viereck, Aphidius matricarae Haiday, Diaeretiella rapae

McIntosh, Ephedrus spp. and Praon spp. were recorded as important parasitoid species associated with cereal aphids on wheat plants (Abdel-Rahman, 1997; El-Heneidy et al., 2001; Salem, 2007; 2012 and Salem and Mahmoud, 2012).

Many aphidiine wasps showed distinct preferences for particular aphid

species and/or instar which reflect acceptability of the host quality for the immature parasitoid (Cloutier et al., 2000; Colinet et al., 2005; Lukouressis et al., 2009 and Rehman and Powell, 2010).           

The parasitoid, D. rapae is reported to be successfully parasitize several economically important cereal aphids including the green-bug and the bird cherry-oat aphids (Ali et al., 2001; Salem, 2007 and Salem and Mahmoud, 2012). This parasitoid has been observed parasitizing a number of aphid hosts other than small grain aphids (Elliott et al., 1994).Throughout the last two decades, entomologists confirmed the use of the Integrated Pest Management (IPM), to control the insect pests when their population reaches the economic threshold injury level by using all other control methods and emphasized on biological control (Schuler et al., 1999).

Therefore, this study aimed to identify the primary and secondary parasitoids attacking the principal cereal aphid species in wheat fields in Upper Egypt. Also, the host selection and specifiety of the parasitoid D. rapae to the different aphid instars in addition to its parasitization influence on the aphid population growth rates was the corner stone of this investigation.

Materials and Methods

An area of about ½ feddan was cultivated with wheat cultivar (Seds 1) at Abnoub location, Assiut Governorate during 2015 wheat growing season. The normal agricultural practices were performed and insecticides were completely prevented.

1 – Field activities:

Survey of cereal aphid parasitoids:

Samples of live individuals of S. graminum and R. padi (all forms) were collected from the wheat field. The specimens were kept in paper bags and transferred to the laboratory. Individuals of S. graminum were separated from those of R. padi using a fine hair Bruch. About 250 individuals of each species were caged on wheat seedlings in plastic pots (7.5 cm in diameter and 8 cm in high). Aphids were then reared under laboratory conditions 23± 2°C, 65 ±5% RH and observed daily for more than 10 days to record the development of mummies. Any observed mummies were removed and individually placed in small vials provided with sterile cotton and covered with muslin cloth. The arenas were observed until the adult parasitoid emergence. Emerging adult parasitoids were identified according to Pike et al. (1997).

Dominance degrees for the parasitoid species were calculated according to Facylate equation (1971) as follows:

D = t / T. 100,            where

t= Total number of each species collected during the study period.

T= Total number of all species collected during the study period.

2 - Laboratory activities:

2-1- Rearing of aphid species:

One colony from both of S. graminum and R. padi was established dependent on one female collected from the wheat field. Each colony was maintained continuously as parthenogenetic females on wheat seedlings under the abovementioned laboratory conditions and continuous light. To obtain groups of the same age, apterous were caged on plants for six hours. Any offspring produced during this period has been transferred to fresh plants and maintained as a synchronous colony until they reached the desired instar for experimentations.

2-2- Rearing of D. rapae parasitoid:

The braconid D. rapae colony used in this study was established from individuals emerged from S. graminum mummies collected from wheat fields in 2015 season. Mummified aphids were maintained under the same laboratory conditions. To obtain D. rapae mated females, mummies were placed together in plastic tubes (3 cm diameter) so that newly emerged males and females could be mate. Adult parasitoids were provided with a solution of equal parts of honey and water as food. The used nymphs and adult aphids (equal in age) were provided by fresh wheat seedlings and moistened small cotton pieces.

2-3- Host selection:

Ten pots (10 cm diameter), each contained 10 wheat seedlings infested with 250 nymphs (second and third instar) of both S. graminum and R. padi species which were taken from laboratory culture. Pots were transferred to the field and placed on 10 m distance between each one. The pots were left to expose to the natural attack by the cereal aphid parasitoid species for 24 hours. After exposure the pots were transferred to the laboratory and covered with a cage of glasses and left under the laboratory conditions to allow the parasitoids to develop until mummification. Any observed mummies were removed and recorded. The experiment was repeated four times, 1st, 15th and 1st, 15^th of February and March, respectively. Aphids that did not show any evidence of parasitism within 10 days following attack were discarded and any data relating to them were not considered in the evaluation. Data taken were the number of mummies and parasitism (%).

2-4- Host-instar preference:

In this experiment, individuals of the first, second, third, fourth nymphal instars and adult stage of S. graminum and R. padi were collected from the laboratory stock culture (125 individuals / instar /species). Aphid individuals were transferred to wheat seedlings growing at 10 cm diameter plastic pots (4 replicates) placed in a box (60 cm in width, 80 cm in length and 50 cm in high). Ten mated D. rapae females were placed into the box and left to attack the aphids for 24 hours as described by Jones et al. (2003).  After the exposure the parasitoid females were removed and the pots were covered with a cage of glasses and left under the laboratory conditions to allow parasitoids to develop until mummifications. The effect of parasitism on aphid instars and reproduction were assessed. Data taken were the number of mummies, average days to mummification, average days request to developing to adult stage, parasitism (%) and mean number of progeny per female.

Statistical analysis

Data of the host preference and host-instar selection and specifiety were tested for differences by T- test at 0.05 probability using (MSTAT_C 1988, Michigan University, Version, 2, 10), and presented as mean ± SD (standard deviation).

Results and Discussion

Relative abundance of cereal aphid parasitoids:

Data in Table (1) indicate the dominance percentages of cereal aphid parasitoid species inhabiting wheat plantation. The dominance percentages of the primary parasitoids were so high and presented by 81.53 %. However, the dominance percentages of the hyperparasitoid species were low and presented by 18.47 %. The parasitoid, D. rapae revealed the highest dominance percentage and presented by 76.38 %. The rest of the primary parasitoid species were presented in low dominance percentages and ranged between 0.55 and 10.27 %. On the other hand, the secondary parasitoid species, Alloxysta australiae (Ashmead) revealed the highest dominance percentage and presented by 47.93 %, followed by Chalcids sp. (23.79 %). The megaspilid Dendrucerus carpentrea (Curtis) and the incyrtid Aphidencyrtus sp. were presented by an average of 16.72 and 11.55%, respectively. These results confirmed those obtained by Pike et al. (1997); Ali et al. (2001) and Salem (2007) who reported that the parasitoid, D. rapae was recorded in high numbers on cereal aphids than other species. Also, D. rapae seem to be the most important primary parasitoid species as biological control agent due to its highest values of dominance and abundance degrees followed by A. colemani and P. necans. On the other hand, Salem (2007) and Salem and Mahmoud (2012) reported that Alloxysta sp. appeared as the most common and abundant primary parasitoids species on cereal aphids. 

Host selection:

Data in Table (2) expressed about the relative abundance of mummies that emerged from live S. graminum and R. padi in different sampling dates during 2015 season in the field. The results indicated that the rate of parasitism ranged from 12.00 to 87.60 % for S. graminum with an average of 50.20 % and from 4.00 to 68.40 % for R. padi with an average of 37.40 %. The rate of parasitism was relatively low during the beginning of February being 12.00 % and 4.00 % for S. graminum and R. padi, respectively. It is important to note that; parasitism rate was increased gradually by time in both aphid species. Statistical analysis showed significant differences between the two aphid species.

In conclusion, it seemed that the aphid species, S. graminum was relatively preferred for the cereal aphid parasitoid, D. rapae than R. padi species. Similar results were previously recorded by several investigators on different aphid parasitoid species e.g. Schelt (1994) and Jones et al. (2003). In this approach, Elliott et al. (1994) reported that the percentage of nymphs parasitized was markedly different among species whereas, significantly greater percentage was performed by S. graminum than Diuraphis noxia, R. maidis and R. padi. Also, Colinet et al. (2005) reported that Aphidius ervi females accepted the aphid Myzus persicae for oviposition and their progeny developed successfully in all host ages.

Host-instar preference:

Data in Table (3) show the number of mummies and percentage of parasitism in different instars of S. graminum and R. padi by the aphid parasitoid, D. rapae during 2015 season. The number of S. graminum and R. padi that died and became mummified by D. rapae varied among the five tested aphid instars. The percentages of parasitism were 20.80, 76.00, 69.60, 44.80 and 40.80 % and 9.60, 28.00, 56.00, 55.20 and 31.20 % for the first, second, third, fourth instars and adult stage of S. graminum and R. padi, respectively. The highest parasitism percentage (76.00 %) was recorded during the second instar of S. graminum and during the third instar of R. padi (56.00 %). Meanwhile, the lowest was recorded during the first instar for both S. graminum and R. padi, by 20.80 and 9.60 %, respectively. Statistical analysis of the data revealed significant differences in the number of mummies in the first and second instars between the two aphids species (P ≥ 0.05), while no significant differences in the third, fourth instars and adult stage in both aphid species (P ≤ 0.05).

In conclusion, the development of the parasitoid, D. rapae is possible in any instar of S. graminum and R. padi but not necessary to produce any progeny. The second and the third instars of S. graminum were appeared as the optimal for parasitoid growth and survival, while the third and the fourth instars of R. padi were appeared as the most preferred instars for parasitized by D. rapae. This finding was previously approved by Shirota et al. (1983) who found that the second and third instars of Sitobion avenae and Metopolophium dirhodium were preferred for oviposition by Aphidius rhopalosiphi females. Also, Ibrahim (1996) and Chau and Mackauer (2001) observed that female parasitoids were parasitized and development successfully until the mummy stage in all host ages from young nymphs to adult.

Development period and reproduction of D. rapae:

As shown in Table (4) development times of D. rapae from oviposition until mummified aphid appearance took 7.97 days inside the third instar and 7.45 days inside the fourth instar of S. graminum. However, it tooks 8.50 days inside the first instar and 7.26 days inside the second instar of R. padi. The averages of the development times from oviposition until the appearance of the mummified aphid were 7.68 and 8.01days for S. graminum and R. padi, respectively. It is important to note that, nymphs parasitized and mummified by D. rapae during the first and second instars may able reaching to maturity but not produce any progeny. However, S. graminum and R. padi parasitized during the third, fourth instars and adult stage were found to be able to produce an average of 7.07, 10.96 and 17.14 and 5.81, 10.77 and 16.74 nymphs before being mummified, when compared with the average production of 68.56, 57.55 and 63.05 and 58.11, 78.33 and 70.26 nymphs per a non-parasitized aphids at the same instars of both aphid species, respectively. On the other hand, development times from oviposition to adult eclosion ranged from 12.23 to 12.66 days for D. rapae emerged from S. graminum, while ranged from 12.29 to 13.07 days for those emerged from R. padi.

It could be generally concluded that, development times from oviposition to mummy or to adult stage varied between the different instars. Offspring production per female was high in the adult instar than others. No offspring produced in the first and second instars. These results are in agreement with those obtained by Salto et al. (1983) who found that the parasitoid, Lysiphlebus testaceipes needed an average of 8.1 days to complete the egg and larval development periods. On the other hand, the parasitoid, L. testaceipes spent an average of 12.4 days from oviposition to emergence. In the same approach, Ibrahim (1996) reported that Aphis craccivora parasitized by Lysiphlebus gracilis in the fourth instar produced 3.5 nymphs as an average after reaching adult stage, while, adult parasitized inside adult stage produced 5.8 nymphs as an average before being mummified when compared with the average production of 29.8 nymphs per a non-parasitized aphids. Also, Krespi et al. (1997) stated that the adult aphid parasitoids, Praon volucra and Ephedrus plagiator emerged from mummies within 15 days of collection.

So, the present results provide essential baseline information for assessing the future changes in cereal aphid parasitoid species dynamics and possible using in the biological control of cereal aphids in the wheat agroecosystem in the studied area.

REFERENCES

Abdel-Rahman. M. A. A. 1997. Biological and ecological studies on cereal aphids and their control in Upper Egypt. Ph. D. Thesis, Fac. of Agric., Univ. of Assiut, 231 pp.

Ali, A. M.; Nasser, M. A. K.; Abdel-Rahman, M. A. A. and Ahmed, A. E. A. 2001. Host preference of some small-Gran aphid parasitoids (Hymenoptera: Aphidiidae) in southern Egypt. Bull. Fac. Agric. Cairo Univ., Special Edition, 171 – 178.

Chau, A. and Mackauer, M. 2001. Host-instar selection in the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): assessing costs and benefits. Can. Entomol ., 133: 549 – 564.

Cloutier, C.; Duperron, J.; Tertuliano, M. and McNeil, J. N. 2000. Host instar, body size and fitness in the koinobiotic parasitoid Aphidius nigripes. Entomol. Exper. Applic., 97: 29 – 40.

Colinet, H.; Salin, C.; Boivin, G. and Hance, T. H. 2005. Host age and fitness-related traits in a koinobiont aphid parasitoid. Ecol. Entomo., 30: 473 – 479.

El-Heneidy, A. H.; Gonzalez, D.; Stary, P.; Adly, D. and El-Khawas, M. A. (2001). A survey of primary and secondary parasitoid species of cereal aphids on wheat in Egypt. Egypt. J. Biol. Pest Cont., 11 (1/2): 193-194.

Elliott, N. C.; French, B. W.; Burd, J. D.; Kindler, S. D. and Reed, D. K. 1994. Parasitism, adult emergence, sex ratio and

size of Aphidius colemani (Hymenoptera:

Aphidiidae) on several aphid species. The Great Lakes Entomologist, 27: 137 – 142.

Facylate, K. K. (1971). Field studies of soil invertebrates. 2nd edition Vishia Shkoola Press, Moscow, USSR

Ibrahim, A. M. A. 1996. On the biology of Lipolexis forster (Hymenoptera: Aphidiidae), a parasitoid of Aphis craccivora Koch (Homoptera: Aphididae). Bull. Ent. Soc. Egypt., 74: 81 – 89.

Jones, D. B.; Giles, K. L.; Berberet, R. C.; Royer, T. M.; Elliott, N. C. and Payton, M. E. 2003. Functional responses of an introduced parasitoid and an indigenous parasitoid on greenbug at four temperature. Environ. Entomol., 32(3): 425 – 432.

Kindler, S. D.; Breen. J. P. and Springer, T. I. 1991. Reproduction and damage by Russian wheat aphid (Homoptera: Aphididae) as influenced by fungal endophytes and cool season turfgrasses. J. Econ. Entomol., 84(2): 685 – 692.

Krespi, L.; Dedryver, C. A.; Creach, V.; Rabasse, J. M. Ralec A. L. and Nenon, J. P. 1997. Variability in the development of cereal aphid parasitoids and hyperparasitoids in Oceanic regions as a response to climate and abundance of hosts. Environ. Entomol. 26(3): 545 – 551.

Lykouressis, D.; Garantonakis, N.; Perdikis, D.; Fantinou, A. and Mauromoustakos, A. 2009. Effect of female size on host selection by a koinobiont insect parasitoid (Hymenoptera: Braconidae: Aphidiinae). Eur. J. Entomol., 106: 363 – 367.

MSTAT- C Software program. 1988. MSTAT-C Michigan State University, Version 2. 10.

Pike, K. S.; Stay, P.; Miller, T.; Allison, D.; Boydston, L.; Graf, G. and Gillespie, R. 1997. Small-grain aphid parasitoids (Hymenoptera: Aphelinidae and Aphididiiae) of Washington: distribution, relative abundance, seasonal occurrence, and key to known North American species. Environ. Entomol., 26(6): 1299-1311.

Rehman, A. and Powell, W. 2010. Host selection behavior of aphid parasitoids (Aphidiidae: Hymenoptera). J. Plant Breeding and Crop Science, 2(10): 299 – 311.

Salem, A.A.A. 2007. Population dynamics and seasonal distribution of cereal aphids and their parasitoids in wheat fields in Upper Egypt. Ph.D. Thesis, Fac. Agric. Assiut Univ.

Salem, A. A. A. 2012. Hymenopterous parasitoids associated with cereal aphids in wheat fields at Assiut. Ass. Univ. Bull. Environ. Res., 15(2): 51 – 61.

Salem, A.A.A. and H.H. Mahmoud 2012. Population fluctuations of cereal aphids and their associated hymenopterous parasitoids in wheat fields. Minia J. of Agric. Res. & Develop. 32(2): 279-296.

Salto, C. A.; Eikenbary, R. D. and Starks, K. J. 1983. Compatibility of Lysiphlebus testaceipes (Hymenoptera: Braconidae) with greenbug (Homoptera: Aphididae) Biotypes "C" and "E" reared on susceptible and resistant oat varieties. Environ. Entomol., 12: 603 – 604.

Schelt, J. van. 1994. The selection and utilization of parasitoids for aphid control in glasshouses. Proc. Exper. & Entomol., N.E.V. Amsterdam, 5: 151 – 158.

Schuler, T. H.; Poppy, G. M.; Potting, R. P. J.; Denhoim, I. and Krray, B. R. 1999. Interactions between insect tolerant genetically modified plants and natural enemies. Gene flow and agriculture: relevance for transgenic crops. Proceedings of a symposium held at keele, UK on 12 – 14 April, 197 – 202; BCPC. Symposium Proceedings No. 72.

Shirota, Y.; Carter, N.; Rabbinge, R. and Ankersmit, G. W. 1983. Biology of Aphidius rhopalosiphi, a parasitoid of cereal aphids. Ent. Exp. & Appl., 27 – 34