J. Ent. Res. Soc., 10(3): 35-46, 2008 ISSN:1302-0250

Natural Enemies of Ceroplastes Species (Homoptera: ), Their Efficiency and Population Movement in Citrus Orchards in the Eastern Mediterranean Region of Turkey

Sevcan ÖZTEMÝZ Mehmet KARACAOÐLU Ferda YARPUZLU

Plant Protection Research Institute, 01321, Adana, TURKEY e-mails: [email protected]; [email protected]; [email protected]; [email protected],

ABSTRACT This study was carried out to determine natural enemies of Ceroplastes species, their efficiency and population movement due to increasing in population of the Floridae wax scale (Homoptera: Coccidae) in citrus orchards in the Eastern Mediterranean region of Turkey, recently. Survey was carried out in citrus orchards and non-cultivated areas in the provinces of (Adana, Mersin, Osmaniye and Hatay) the Eastern Mediterranean region according to the systematic sampling method, in terms of 0.01 % in totally numbers of tree. Moreover, natural enemies of the pest and population movement were determined in three citrus orchards infected with Ceroplastes spp. Sampling of each orchard was made in 10 citrus trees with 5 shoots and 20 leaves in different directions of each tree in every forthnight from April to October. The natural enemies were determined as Scutellista sp. (Hymenoptera: Pteromalidae), toddaliae (Risbec) (Hymenoptera: Eulophidae), Microterys neitneri (Motschulsky) (Hymenoptera: Encyrtidae), Chyrsoperla carnea (Steph.), Conwentzia sp. (Neuroptera: Chrysopidae), Paraseiulus soleiger (Ribaga) (Acarina: Phytoseiidae), Scymnus rubromaculatus (Goeze), Coccinella spp., Rodolia cardinalis (Muls) and Stethorus sp. (Coleoptera: Coccinellidae) species. The highest parasitation rate was found in the third stage larvae followed by the second stage larvae and mature female individuals, respectively. The parasitation rate was 1-10 % in citrus orchards, 20-30 % on hosts (laurel) around the orchards. Key words: Citrus, Floridae wax scale, natural enemies, parasitation rate, population movement.

INTRODUCTION Wax scale is a group of the most important pests of citrus orchards, fruit trees and ornamental plants in Turkey (Ülgentürk et al., 2001; Kaydan et al., 2004). Florida wax scale (Homoptera: Coccidae) has become an important problem in citrus of Mediterranean Region in recent years. Wax scales damage the plants by sucking the juices. Heavily infested plants appear unhealthy and decrease new growth. Scales fed on leaves, fruit, twigs, branches, and/or tree trunks, excrete large amounts of 36 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F. honeydew, excretion is an excellent medium for the growth of a fungus that coats the top side of leaves, reducing the photosynthetic capability of the leaves and low external fruit quality. It is difficult to control them due to their wax cover playing a protective role. Chemical control is frequently followed by recurrent infestations of the target pests and outbreaks of non-target organisms. For these reason, alternative pest control methods are being sought. Scale has many natural enemies, such as predators, parasites, and pathogens (Erler & Tunç, 2001; Ülgentürk et al., 2004). Under most conditions, predators and parasites suppress scale pest populations to a level where chemical intervention is unnecessary. When scale insects are not controlled, high populations damage leaf, fruit, twig, branch and trunk of tree. In these situations, integrated pest management (IPM) is used since it reduces negative effects on natural enemies (Futch et al., 2001). Data on the natural enemies observed and collected with the scale samples provide an important and useful role for biological control initiatives for IPM programs. The purpose of this study was to determine natural enemies of Florida wax scale, their efficiency and population movement in citrus orchards, during the years of 2003-2005 in the Eastern Mediterranean Region (Adana, Mersin, Osmaniye and Hatay) of Turkey. The study will be helpful for biological control of this pest based on the information on the natural enemy and its efficiency.

MATERIALS AND METHODS

Determination of Natural Enemies of Ceroplastes Species The provinces where citrus growing is widespread are divided into subregions; Adana (Seyhan, Yüreðir, Karataþ, Kozan), Mersin (Center, Tarsus, Erdemli, Silifke), Hatay (Erzin, Dörtyol, Ýskenderun, Samandað) and Osmaniye (Kadirli, Sumbas). Survey was conducted according to the systematic sampling method based on 0.01% of the total trees (Bora & Karaca, 1970; Table 1). In these subregions, the numbers of the tree sampled in citrus orchards was determined with respect to Lazarov and Grigorov (1961). Determining of Parasitoids: The shoots (15-20cm long) contaminated with Ceroplastes floridensis Comstock and Ceroplastes rusci (L.) were cultured after cleaning from pests except Ceroplastes sp. By making use of the light seeking feature of C. floridensis and C. rusci parasitoids, the shoots contaminated with Ceroplastes sp. were placed in darkened (with black polyethylene) plastic bottles to obtain parasitoids. A glass tube was placed to the open side of the bottle to collect the parasitoids and controlled twice a day. Moreover, the bush, fig and bay laurel plants were observed to determine the natural parasitation throughout. Natural Enemies of Ceroplastes Species (Homoptera: Coccidae) 37

Table 1. Research Conducted in Provinces and Villages and the Numbers of Tree in the Eastern Mediterranean Region of Turkey

Provinces Subregions The numbers of The numbers of citrus total citrus tree tree surveyed

Seyhan 1.152.800 115

Yüreðir 2.951.500 295

Adana Karataþ 294.960 29

Kozan 1.743.400 174

Total 6.142.660 613

Center 2.960.060 296

Tarsus 1.355.920 135

Mersin Erdemli 1.887.050 188

Silifke 387.625 38

Total 6.590.655 657

Erzin 1.626.200 162

Dörtyol 1.488.000 148

Ýskenderun 503.000 50 Hatay Samandað 576.000 57

Total 4.193.200 417

Kadirli 70.386 7

Osmaniye Sumbas 140.772 14

Total 211.158 21

Determining of Predators: The “visual sampling” and “beat sheet sampling” were used to determine the predators. In visual sampling three trees were observed for three minutes; in beat sheet sampling, 15 to 20 trees were chosen and the sample were collected by using Japan umbrella (1x1m²) and each tree was stroke 3 times (totally 45-60 strikes). Among the insects, the predators were collected and recorded to be identified.

Population Movement of Natural Enemies of Ceroplastes Species The population observation of pests was carried out in an orange orchard including 1550 orange trees contaminated with pest in Adana (Zaðarlý) and in a lemon orchard including 10.000 trees in Mersin (Erdemli) in the first year; in a lemon and orange orchard including 550 trees in Adana (Kozan) in the second year. Sampling in each 38 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F. orchard was made in 10 citrus trees with 5 shoots and 20 leaves in different directions of each tree in every forthnight from April to October (Ben-Dov, 1976) and examined in the laboratory (Ben-Dov, 1976; Soylu, 1976).

RESULTS AND DISCUSSION

Determination of Natural Enemies of Ceroplastes Species Three parasitoids species belonging to three families (Pteromalidae, Eulophidae, Encyrtidae) of Hymenoptera and seven predators species belonging to four families (Chrysopidae, Cocinellidae, Phytoseiidae, Coniopterygidae) were collected from scale insects (Table 2). The parasitoids belonging to order of Hymenoptera were determined as Scutellista sp. (Hym.: Pteromalidae); Aprostocetus toddaliae (Risbec) (Hym.: Eulophidae) and Microterys neitneri (Motschulsky) (Hym.: Encyrtidae). Soylu (1976) found that Scutellista cyanea Motsch. (Hym.: Pteromalidae), Coccophagus scutellaris Dalm. (Hym.: Aphelinidae), Tetrastichus sp. (Hym.: Eulophidae) as parasitoids species of C. floridensis. Huang & Huang (1988), found eight parasitoids species belonging to order of Hymenoptera among the natural enemies of C. floridensis and the most widespread families were observed as Encyrtidae, Eulopidae, Aphelinidae and Pteromalidae. The most common species of C. floridensis was found as Tetrastichus ceroplastae (Aprostocetus ceroplastae), Microterys flavus, Metaphycus flavus Howard (Hym.: Encyrtidae), Moranila californica Howard (Hym.: Pteromalidae) and Scutellista cyanea Motsch. by Argov et al., (1992). Two parasitoids determined in the study were similar to the other survey studies. The most common species was Scutellista sp. Karacaoðlu et al., (2004) reported that three parasitoids species were found in Ceroplastes populations and the most common predator species was Chilocorus bipustulatus (L.) (Col.: Coccinellidae). In the study, 7 predator species differ from the earlier survey were determined (Table 2). Four different families were identified in Zaðarlý, Erdemli and Kozan subregions (Table 2). Stethorus sp were abundant due to the excessive mite population in the orange orchard in Zaðarlý in May. The decreasing number of pesticide performance led to the intensive population of Stethorus, which kept the pest under economic threshold. Besides, only two Conwentzia sp. were found. Various predators observed in accordance with pest populations in Erdemli orchard surrounded by bushy plants. Rodolia cardinalis (Muls) identified when the population of Icerya purchasi (Mask.) increased. Scymnus rubromaculatus (Goeze) was found in low intensity in June- Natural Enemies of Ceroplastes Species (Homoptera: Coccidae) 39 August period. This predator is mentioned among Ceroplastes sp. predators (Anonymous, 1997). Coccinella spp. were found in various numbers. Chrysoperla carnea (Steph) is a common predator noticed in all the three orchards at different times and amounts. Paraseiulus soleiger (Ribaga,) was recorded at periods when mature females and active larvae of Ceroplastes sp. were intensive in all three orchards. This beneficial acarus is found in leaf dropping trees (willow, oak, acacia etc.) (Kabirec, 2003). These trees are thought to be the host to pass on to citrus orchards. The same species was found but in varying amounts in all the three orchards (Table 2).

Table 2. The Numbers of Predator Determined in Adana (Zaðarlý), Mersin (Erdemli) and Adana (Kozan) in Citrus Plantations

Zaðarlý Erdemli Kozan Predators Order Family 2003 2004 2005 2003 2004 2005 2004 2005

Chyrsoperla carnea (Steph.) Neuroptera Chrysopidae 9 16 22 44 48 40 32 28

Stethorus sp. Coleoptera Coccinellidae - 142 132 6 - - 2 6

Paraseiulus soleiger (Ribaga,) Acarina Phytoseiidae - 19 15 23 33 28 95 69

Conwentzia sp. Neuroptera Coniopterygidae - 2 - 7 10 12 2 3

Scymnus rubromaculatus (Goeze) Coleoptera Coccinellidae - - - 11 18 23 25 23

Coccinella spp. Coleoptera Coccinellidae - - - 3 11 - -

Rodolia cardinalis (Muls) Coleoptera Coccinellidae - - - 12 21 15 - -

9 179 169 106 130 129 156 129 Total 357 365 285

Four different families were identified in Zaðarlý, Erdemli and Kozan subregions (Table 2). Stethorus sp. were abundant due to the excessive mite population in the orange orchard in Zaðarlý in May. The decreasing number of pesticide performance led to the intensive population of Stethorus, which kept the pest under economic threshold. Besides, only two Conwentzia sp. were found. Various predators observed in accordance with pest populations in Erdemli orchard surrounded by bushy plants. Rodolia cardinalis (Muls) identified when the population of Icerya purchasi (Mask.) increased. Scymnus rubromaculatus (Goeze) was found in low intensity in June- August period. This predator is mentioned among Ceroplastes sp. predators (Anonymous, 1997). Coccinella spp. were found in various numbers. Chrysoperla carnea (Steph) is a common predator noticed in all the three orchards at different times and amounts. Paraseiulus soleiger (Ribaga,) was recorded at periods when 40 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F. mature females and active larvae of Ceroplastes sp. were intensive in all three orchards. This beneficial acarus is found in leaf dropping trees (willow, oak, acacia etc.) (Kabirec, 2003). These trees are thought to be the host to pass on to citrus orchards. The same species was found but in varying amounts in all the three orchards (Table 2).

Population Movement of Natural Enemies of Ceroplastes Species Population movement of alive and individuals emerged parasitoid of C. floridensis in orange orchards in Adana (Zaðarlý) during the years of 2003-2005 is given in (Fig.1a, b). In the first year, only 25 parasitized individuals were identified till the end of September. In the second year, the parasitized individuals were seen only in October-January period and during the summer no parasitized individual was found. In the second generation; the numbers of parasitized individual was low in September due to not being found the third stage larvae of wax scale which parasitoids prefer. Most of the larvae were in the first stage. The emerged parasitoid observed in December and January thought to be the individuals left over from the previous months. In the third year, the numbers of parasitized individual was low (15-20 individuals) in May and June. The highest parasitation rate was found in the third stage larvae followed by the second stage larvae and mature female individuals, respectively (Fig. 1a, b). Wakgari (2001) pointed out the pest prefers third stage larvae and the preoviposition period of females. Population movement of alive and emerged parasitoid of C. floridensis and C. rusci in lemon orchards in Mersin (Erdemli) during the years of 2004-2005 is given in (Fig. 2 and 3). The parasitation rate of C. floridensis was similar to the C. rusci in lemon orchard. The individuals of second and third stage larvae with mature female were found parasitized from the beginning of August although there was no any parasitation from March to July. The highest rate of parasitation was seen in September in the second stage larvae followed by third stage and mature female individuals, respectively. No parasitation was noticed in the first stage larvae. In the individuals of the second generation, the parasitation has been noticed to rise in October (Fig. 2 and 3.) Population movement of alive and emerged parasitoid of C. rusci in lemon orchards in Adana (Kozan) during the years of 2004-2005 is given in (Fig. 4). The numbers of parasitized individual was found low with10-15 individuals in the first Natural Enemies of Ceroplastes Species (Homoptera: Coccidae) 41 year and 25-30 individuals in the second year only in August and September due to using a broad spectrum insecticide against pests in previous year. In the second year, there was a rise in parasitation even if a very low one (Fig. 4). The highest parasitation rate was observed in the second and third stage larvae. Parasitation was started to be noticed in July. Similarly, Soylu (1976) pointed out parasitation was highly seen in the third stage larvae followed in the second stage larvae and mature females, respectively. The parasitation rate was 1-10 % in citrus orchards, 20-30 % on hosts (laurel) around the orchards. Huang & Huang (1988) pointed out that the parasitation rate of C. floridensis was 26.3%.

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0 11 .0 3.2 00 3 27.03.2003 11.04.2003 24.04.2003 20.05.2003 10.06.2003 25.06.2003 08.07.2003 23.07.2003 05.08.2003 19.08.2003 02.09.2003 16.09.2003 30.09.2003 22.10.2003 12.11.2003 16 .1 2.2 00 3

L1 alive L1 em erge d par asito ids L2 alive L2 emerged parasitoids L3 alive L3 emerged pa rasitoids female alive female emerged parasitoids

Fig. 1a. Population movement of alive and emerged parasitoid of Ceroplastes floridensis in orange orchards in Adana (Zaðarlý) during the year of 2003.

42 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F.

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L1 alive L1 emerged pa rasitoids L2 alive L2 emerged parasitoids L3 alive L3 emerged parasitoids female alive female emerged parasitoids

Fig. 1b. Population movement of alive and emerged parasitoid of Ceroplastes floridensis in orange orchards in Adana (Zaðarlý) during the years of 2004-2005. Natural Enemies of Ceroplastes Species (Homoptera: Coccidae) 43

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L1 alive L1 emerged parasitoids L2 alive L2 eme rged para sitoids L3 alive L3 emer ge d p arasito ids female alive female emerged parasitoids

Fig. 2. Population movement of alive and emerged parasitoid of Ceroplastes floridensis in lemon orchards in Mersin (Erdemli) during the years of 2004-2005. 44 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F.

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L1 alive L1 emerged parasitoids L 2 alive L2 emerged parasitoids L3 alive L 3 emerg ed parasitoids female alive fe male em erged parasitoid s

Fig. 3. Population movement of alive and emerged parasitoid of Ceroplastes rusci in lemon orchards in Mersin (Erdemli) during the years of 2004-2005. Natural Enemies of Ceroplastes Species (Homoptera: Coccidae) 45

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L1 alive L1 emerged parasitoids L2 alive L2 emerged parasitoids L3 alive L3 emer ge d p arasito ids female alive female emerged parasitoids

Fig. 4. Population movement of alive and emerged parasitoid of Ceroplastes rusci in lemon orchards in Adana (Kozan) during the years of 2004-2005. 46 ÖZTEMÝZ, S., KARACAOÐLU, M., YARPUZLU, F. REFERENCES

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Received: December 12, 2007 Accepted: August 19, 2008