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LIFE HISTORY AND BIOLOGY OF ROSE SAWFLY, ARGE ROSAE LINNAEUS (HYMENOPTERA: ARGIDAE)

Halil Bolu*, M. Murat Aslan** and Hasan Maral***

* Associate Professor, Dicle University Faculty of Agriculture, Plant Protection Department, 21280, Diyarbakır, TURKEY. E-mail: [email protected], ORCID ID: 0000-0001-5488- 0056 ** Professor, Kahramanmaraş Sütçü İmam University Faculty of Agriculture, Plant Protection Department, Kahramanmaraş, TURKEY. E-mail: [email protected], ORCID ID: 0000-0002-4586-1301 *** Karacadağ Development Agency, 21080, Bağlar, Diyarbakır, TURKEY. E-mail: [email protected], ORCID ID: 0000-0001-9201-8758

[Bolu, H., Aslan, M. M. & Maral, H. 2021. Life history and biology of rose sawfly, Arge rosae Linnaeus (Hymenoptera: Argidae). Munis Entomology & Zoology, 16 (1): 484-493]

ABSTRACT: Arge rosae Linnaeus (Hymenoptera: Argidae) is one of the most important pests of roses. This study has been carried out in Diyarbakır, which has an important place in rose cultivation, between March and July in 2016-2018 to determine the life parameters and damage type of A. rosae. The study has been carried out in the rose garden based on local (white, yellow, pink and red color) and Isparta variety. It has been investigated on A. rosae's eggs, larvae, pupae and adult periods, egg laying behaviour, colour preference for adults to lay eggs and loss rate. It has been determined that the female of the pest causes significant damage to the branches during egg laying and the larvae to the leaves during feeding as a result of the study. In the study, the average body length of the pest has been measured as 6.7 mm. The pest lays a maximum of 5 eggs package in one branch, and each egg pack has been found to have between 8 and 72 eggs. In the examination regarding the colour preference of A. rosae, it has been determined that the pest was contaminated with 100% in Isparta rose, 92% in pink roses, 88% in yellow roses, 24% in red roses, and 16% in white roses. As a result, it is recommended to investigate the damage status of the pest, which is determined to cause significant damages in roses, especially in cut flowers and oil roses and additional work on the activities of natural enemies in the future.

KEY WORDS: Arge rosae, roses, damages, life parameters, biology

The ornamental plants market in the world has a foreign trade volume of approximately 40 billion dollars. Rose (Rosa spp.) has significant economic value both in terms of being an ornamental plant and raw material of valuable products such as rose oil in this market. Turkey is a key actor in ornamental plants market. Cut roses are grown in the area of about 2 thousand decares in Turkey. Production quantity of roses called oil roses or Isparta roses which are rich in essential oil is around 15,000 tons per year in the world that 8,500 tonnes of it are produced in Turkey (Anonymous, 2018). Rose cultivation has a history of 4600 years in Diyarbakır, which stands out with its agricultural potential in every period of history (Yalçın Mendi, 2011). It is understood that Diyarbakır was an important “Rose Center” during the Ottoman Empire, 25 rose species were grown in the province and important rose cultivation researches were conducted in Diyarbakır at that time (Maral, 2010). Important awareness studies has carried out and trial production has carried out in order to reactivate the potential of Diyarbakır in terms of rose. It is of great

Munis Entomology & Zoology Mun. Ent. Zool. https://www.munisentzool.org/ (January, 2021) 485 ISSN 1306-3022 © MRG ______importance to know the pests and diseases that cause economic damage to rose in order to spread the production and obtain quality products. Numerous harmful insect species that damage to rose have been identified both in the world and in our country (Strom et al., 1997; Horst & Cloyd, 2007; Hazar & Baktır, 2014). Arge rosae L. (Hymenoptera: Argidae), one of these insect species, causes significant damage to roses (Sharifia et al., 2012). The larvae of the pest feed on fresh leaves and cause leaf loss in the plant; the females of the pest, leaving their eggs on young shoots, cause the stems to dry and consequently to shed leaves (Khosravi et al., 2015). As a result of all these losses, there are significant losses in rose yield and quality. It is of great importance to know the life parameters and damage type of the pest in order to reduce the economic losses caused by A. rosae and to determine the appropriate pest management method. The life parameters and damage type of A. rosae has been investigated in this study.

MATERIALS AND METHODS

The study has carried out between 2016-2018 in Dicle University Faculty of Agriculture (Diyarbakır) and established rose garden based on local (white, yellow, pink and red color) and Isparta variety (Fig. 1). Egg, larvae, pupae and adult periods, egg laying behavior, color preference of adults for laying eggs and the damage rate of A. rosae has investigated in the rose garden from March to July. It has brought to the laboratory with the its nutrients gathering larvae of the harmful insect in different periods from the garden. In addition, investigations on various biological phases, measurements and weighing have made about the pest collected from the garden on different dates brought to the laboratory. Measurement (digital caliper) and weighing (digital precision scales) has been made on the adult individuals. To determine the color preference of the pest, 25 plants from each color has been selected and the contamination rate of the pest in these plants has been determined. The data has been analyzed in Statistics Software SPSS 21 Windows Software package by applying Duncan 5% test.

Figure 1. The garden in which the study is carried out. A- local roses, B- Isparta Rose.

RESULTS

The examinations and observations on the biology of A.rosae in the rose garden and laboratory are given below. Adult Average length of male 6.7 mm (6-7.5 mm, excluding wings, n: 50), female have measured as 8.5 mm (6.5-9.5 mm, excluding wings, n: 50) (Figs. 2-3). The head of both sexes is black, from the top (dorsal) prothorax black and there is a

Munis Entomology & Zoology Mun. Ent. Zool. 486 https://www.munisentzool.org/ (January, 2021) ISSN 1306-3022 © MRG ______transverse black section between 1st and 2nd leg in. Abdomen is golden in both sexes. The wings and legs are yellowish.

Figure 2. The ventral view of the male (Left) and female (Right) of Arge rosae.

Figure 3. The lateral, ventral and dorsal view of the male and female of Arge rosae.

There are 3 ocelli eyes at head of male and female. Compound eyes are light black, dot eyes are reddish. There are obvious differences between the antennas of male and female (Fig. 4). The antennas has 3 segments. Flagellum are much longer than pedicel and scape. The predominant color of females' antennas is black and less hairy, while the upper part of males' antennas are covered with longer hairs and the underside is yellowish. Mandibules developed in both sexes.

Figure 4. Antennas of Arge rosae, male (A) and female (B).

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Egg As of the beginning of April, it was determined that adults started mating and laying eggs (Figs. 5, 6). It was observed that females lay eggs with their heads facing the soil surface (Fig. 7). Females lay their eggs on the branches in a double row and at an angle at horizontal. Transparent eggs and embryo in the first days become blackens near the opening (Fig. 7). A maximum of 5 egg groups were counted in one branch. It was determined that there were between 8 and 72 eggs in each egg group (Fig. 8).

Figure 5. Mating adults of Arge rosae.

Figure 6. Arge rosae's females lay eggs on the branches.

Figure 7. The eggs of Arge rosae laid on branches.

Figure 8. Egg groups of Arge rosae on the branches.

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Larvae Arge rosae mostly has 5 larval stages. However, in the study, 6th period larvae has been also found. It has not been determined under what conditions or sex group the larvae reached the 6th period. The capsules of the newly hatched larvae has been found to be white or black and the legs were blackish (Fig. 9).

Figure 9. Arge rosae's larvae hatching.

Head capsules and legs of the second stage larvae are completely black, black spots on the body are seen intensely (Fig. 10). The head capsules of the third stage larvae turn dark brown, the fourth stage light brown, and head capsule of last period larvae turn light yellow (Fig. 11). From the third period of larvae, its leg colors turn white. Changes in the body color of the larvae has been also observed. In the third period, its body colors are greenish, dorsal side is orange in the last period, the lateral side turns light yellow (Fig. 12).

Figure 10. Second stage larvae of Arge rosae.

Figure 11. The third, fourth and fifth stage larvae of Arge rosae.

Figure 12. Sixth stage larvae of Arge rosae.

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Pupa The larvae entering under a few cm of the soil near root of the roses during the last larval period becomes pupa in a cocoon (Fig. 13). The prepupa is orange (Fig. 14). Measurements and weighings has been made on cocoons that collected from the garden during the larvae period and taken to the culture obtained in this way and cocoons (Fig. 15) collected from the garden (Table 1). While there was no statistically significant difference between the width and length of the cocoons cultured in the laboratory and the cocoons collected from nature, the difference was found to be statistically significant in terms of weights. It was observed that the average weight of the individuals obtained in laboratory environment was higher. This may be attributed to the poor nutritional competence among larvae fed in the laboratory.

Figure 13. The cocoons of Arge rosae.

Figure 14. Ventral and lateral view of the prepupa of Arge rosae.

Figure 15. The cocoons of Arge rosae obtained in the laboratory and collected from the garden.

Table 1. Measurements of cocoons obtained in the laboratory and collected from the garden.

Width (mm) Length (mm) Weight (gr)

N Min Max. Avarege Min. Max. Avarage Min. Max. Avarege

Laboratory 50 3,30 5,69 4,5±0,076 7,42 11,20 9,6±0,158 0,012 0,077 0,052±0,027a

Garden 50 3,61 5,63 4,4±0,064 5,42 12,18 9,3±0,174 0,022 0,080 0,042±0,002b

Sex Ratio Unopened cocoons were collected at different dates and brought to the laboratory and cultured in the rose garden where the study was carried out in order to determine the sex ratio of individuals who make up the natural population. The results are given in (Table 2).

Table 2. Sex ratio of individuals emerging from cocoons collected from rose garden.

Date Total Opened Coco Adult Emerging Male:Female Cocoons Female Male 25.10.2017 720 131 96 35 12.03.2018 498 390 261 129 23.03.2018 44 30 22 8 26.03.2018 705 494 216 278 16.04.2018 549 41 18 23 Total 2516 1086 613 473 0,43

Damage Status Arge rosae causes damage to rose plants in two ways. The first case occurs when the female lays eggs. The female lays her eggs into the tissue by piercing the epidermis of the branches with the ovipositor. In this way, the branches that lay eggs are dried (Fig. 16).

Figure 16. The damage caused by Arge rosae females to branches after laying eggs. The second type of damage of Arge rosae is caused by larvae. The larvae hatching immediately begin feeding on the leaves. This feeding continues until the last larval period so that the main vessel of the leaf remains (Fig. 17).

Figure 17. Damage caused by Arge rosae larvae on leaves.

In the examination of 25 plants related to the color preference of A. rosae, it has been determined that the pest has contaminated with 100% in Isparta roses, 92% in pink roses, 88% in yellow roses, 24% in red roses, and 16% in white roses.

113 of the local rose varieties has been randomly checked and all has been found to be contaminated at the time when A. rosae laid eggs most intensively, in 113 controlled plants, 1064 branches has been examined and 601 branches has been found to be contaminated and the damage rate has been calculated as 56.48%.

DISCUSSION

In this study, conducted in both nature and laboratory conditions, A. rosae has been found to cause significant damage to roses. Important data about the biological periods of the pest and the type of damage has been obtained. It has been determined that the average height (8.5 mm) of the females of A. rosae is longer than the males (6.7 mm) in this study. Smith (1989) has stated that the lengths of the species depending on the Arge genus can be up to 14 mm, and the body colours can be orange, orange black mixture and completely black. It has been determined that the average height of the females of Arge hasegawae Takeuchi, which caused damage in the raspberry [Rubus crataegifolius Bunge (Rosaceae)], is 7 mm and males 6 mm (Shinohara et al. 2011), the average height of females of Arge humeralis (Beauvois), which causes damage in poison ivy [Rhus radicans L. (Anacardiaceae)], is 10.6 mm and males 8.5 mm (Regas- Williams & Habeck, 1979), the average height of females of Arge pagana (Panzer), which causes damage in violet rose [Rosa chinensis (Jacq)], is 8.7 mm and males are 6.7 mm (Zhao & Hua, 2016). Body colours of the species differed. The first stage that the pest causes economic damage in roses is caused by adults when they lay eggs. Females prefer fresh shoots for laying eggs and with ovipositors they lay eggs in a plant with a maximum of 5 groups where double rows into branches and at a certain angle horizontally. Shoots laid on the eggs are damaged and dry. It has been determined that Arge xanthogaster (Cameron), (Firake et al. 2013) Arge pagana, Arge hasegawae, Arge humeralis females - belongs to the same genus- has left the eggs to the shoots one by one on both sides by tearing fresh shoots with powerful saw-shaped ovipositors. Unlike the species mentioned above, Arge naokoae n.sp., belongs to the same genus, lays its eggs on the leaf edges of Spiraea dasyantha Bunge (Shinohara & Hara, 2013). It has been determined that while Spinarge fulvicornis Hara&Shinohara females, an important pest of Azalea (Rhododendron sp.), generally lay their eggs on the edges of the leaves in a row similar to A. naokoae, Spinarge affinis Hara & Shinohara females mostly choose places near the stem in the lower part of the leaves to lay eggs and, unlike the findings obtained in our study, they lay one egg on each leaf instead of laying eggs in groups (Shinohara & Hara, 2006). It is evaluated that the differenti plant tissues and species affect the egg laying preferences. Another period of A. rosae causing damage is the larval period. It has generally 5 larval periods. However, in this study, 6th period larvae were also found. It couldn’t been determined under what conditions or sex group the larvae reached the 6th period. All larval periods feed on leaves and cause serious damage. Sahragard & Heydari (2001) stated that especially, the first period larvae of A. rosae are fed in groups on the leaves and buds of the roses and cause significant damage. Although it has been stated in other researches that the species related to Arge genus do similar damage (Smith, 1989), it has been determined that the number of larvae periods may differ by species. Firake et al.

(2013) found that the larvae of A. xanthogaster cause significant damage to the roses, and in some cases the process results in the loss of a large part of the leaves. The same researchers found that A. xanthogaster usually had 5 larvae periods, stated that the 6th period larvae were also encountered, but did not give information about under which gender or conditions this occurred. Zhao & Hua (2016) determined that the males of A. pagana had 5 larvae and the females had 6 larvae period. Regas-Williams & Habeck (1979) found that A. humeralis has been found that males had 5, and females had 6 larvae periods similarly A. pagana. Adachi (1981) determined that Arge nigrinodosa (Motschulsky) and Arge nipponensis (Rohwer) cause significant damage to roses, and the larvae of both species had an average of 5 periods in males and 6 in females; When the larval density increased, A. nigrinodosa males tend to have 6, females tend to have 7 larval periods; A. nipponensis females tend to have 7 larval periods in laboratory conditions. It has been determined that the larvae of A. nigrinodosa feed on rose leaves in groups and cause significant yield losses (Kawasaki et al., 2012). we found that A. rosae became a pupa in a cocoon in the soil and the colour of prepupa was orange. The width, height and weight values of cocoons obtained in the laboratory were measured higher than the cocoons collected from garden. The average weight of cocoons obtained in the laboratory and collected from the garden was determined respectively 0,052 g and 0,042 g. Adachi (1981) measured that the average cocoon weight of males and females of A. nigrinodosa and A. nipponensis was respectively 0.026, 0.048, 0.021, 0.035 g in laboratory conditions. It is seen that there is a significant difference between the weight values obtained in our study and the weight values measured by Adachi (1981). It is considered that the measurements made in different conditions and development periods of cocoons may cause this difference in addition to the different species. We measured the average length of cocoons as 9.6 mm in the laboratory and 9.3 mm in nature. Shinohara et al. (2011) was determined that the average length of cocoons of A. hasegawae collected from the nature was 9 mm in females and 8 mm in males. Zhao & Hua (2016) measured the average pupa length of A. pagana as 9.14 mm. These values were similar to our results. It was observed that these rates may vary according to gender although sex ratios of Argidae family species are found close to each other. The male: female ratio of A. rosae was measured as 0.43 in our study. This ratio is similar to the results obtained by Sahragard & Heydari (2001) regarding A. rosae in laboratory conditions (0.35 ± 0.06). Borachi et al. (2005) has found that the sexual ratio of Digelasinus diversipes (Kirby, 1882) (Argidae) is 0.35 in favor of females (2.83 female to 1 male); Ciesla (2002) has found that sex ratio of Sericoceros mexicanus (Kirby) is almost the same as D. diversipes but on the contrary, it is 0,36 (2.76 male to 1 female) in favor of males. Zhao & Hua (2016) stated that A. pagana had large differences in gender ratios depending on environmental conditions. The damage rate of A. rosae in roses was calculated as 56.48% in our study. Firake et al. (2013) determined that the damage rate of A. xanthogaster in roses is 80% in India. Blank et al. (2010) found that Aproceros leucopoda Takeuchi (Argidae) causes an average of 74-98% leaf loss in elms (Ulmus spp.) in Romania. In our study, findings related to the color preference of A. rosae were also obtained. It was determined that the pest was contaminated with 100% in Isparta rose, 92% in pink roses, 88% in yellow roses, 24% in red roses, and 16% in white roses. In the literature review, no findings regarding color preference were found.

It has been concluded that A. rosae caused significant damages in roses and that the damage of this pest should be taken into consideration in order to minimize yield and quality losses in roses as a result. In particular it is recommended to investigate the damage status of the pest in cut flowers and oil roses in detail, and to conduct additional studies on the effectiveness of natural enemies in the future.

LITERATURE CITED

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