Volume 21(3), 96- 103, 2017 JOURNAL of Horticulture, Forestry and Biotechnology www.journal-hfb.usab-tm.ro

Dynamics of the attack by robiniella and Phyllonorycter robiniella of black locust from Valea lui Mihai and Covasna

Hulujan I.B.1*, Oltean I.1, Florian Teodora1

University of Agricultural Sciences and Veterinary Medicine from Cluj-Napoca, Calea Mănăștur, No. 3-5, 400372, Cluj-Napoca,

*Corresponding author. Email: [email protected]

Abstract In Romania, since 1989 acacia trees are attacked by Parectopa Key words robiniella Clemens and since 2002 by Phyllonorycter robiniella Clemens. There are two species of mining microlepidoptera that originate in the American continent. The area of spreading has increased annually, so Clemens, Phyllonorycter species are reported in all counties. In 2017, the frequency of the attack and robiniella Clemens, attack the number of mines the species develops on a leaf was monitored. The studies were conducted in two locations: Valea lui Mihai (Satu Mare County) and Covasna (Covasna County). At the end of the biological cycle of the two species, the frequency of the attack reached 29% in Covasna, and at 89% in Valea lui Mihai. The average number of mines/leaves developed by Phyllonorycter robiniella (in case of single attack) was 6.3 mines at Covasna and 4.3 mines at Mihai Valley. The average number of mines/leaves developed by Parectopa robiniella (in case of single attack) was 1.1 mines at Covasna and 15.3 mines at Mihai Valley. Leaves attacked simultaneously by both species showed an average number of 5.9 mines in Covasna (4.7 mines of Phyllonorycter robiniella and 1.2 mines of Parectopa robiniella), respectively 19.8 mines at Valea lui Mihai (6.7 mines of Phyllonorycter robiniella and 13.1 mines of Parectopa robiniella). Given the average surface area of a mine, they can often cover the surface of a foil. On a leaf, the maximum number of mines developed by Parectopa robiniella was 7 mines and for Phyllonorycter robiniella was 3 mines. The maximum number of mines on a foil attacked simultaneously by the two species was 6 mines (5 mines of Parectopa robiniella and one of Phyllonorycter robiniella).

In the last period, acacia trees are attacked by 2007, the species also attacks Russia (13), Lithuania two species of mining : Parectopa (17) and Belgium (3). robiniella Clemens-1893 and Phyllonorycter robiniella In Romania, Parectopa robiniella was Clemens-1859. The natural habitat of these species is reported in 1989, in Mehedinti County, in the Crivina North America, a region where pseudoacaccia Forest, located at approx. 30 km southwest of Drobeta also originates. After their penetration into the Tr. Severin, from where it spread rapidly, reaching European continent, the two species have expanded 1994 to the Buzau area. Currently the species is found their spreading area by approx. 100 km/year in acacia forests all over the country, sometimes In Europe, Parectopa robiniella was first causing significant injuries (27). According to Camelia reported in 1970 in on the acacias around Milan Ureche (38), the frequency of the attacked foliales at airport (39). The following year the attack of this Cosmeşti, Galati County, was 17,47% in 1999, and in species was also reported in Switzerland (31, 40, 41). Bacau County, the frequency of the attack in 2002 was In 1983 the species was reported in the southern part of between 9,05% (Bacau city) and 28.52% at Hemeius. (2, 35) and Yugoslavia (20). In 1984 the The adult species of Parectopa robiniella has species attacked the acacia in and increased its a wingspan of 7-8 mm and on repose is 4-5 mm. The area in Yugoslavia (21), and in 1986 in on the front wing is dark-brown, ornate on the marginal edge border with Switzerland (23). In 1987, in , the with four white bands. The back rim of the wings is first mines with larvae inside were found, the species trimmed with three white bands, interleaved between probably penetrating from Hungary (18). It has been the first three bands on the anterior edge (23). The egg reported in the Czech Republic since 1992, and in is elliptical, colorless, and slightly shiny. The Serbia since 1994 (3). Since 2000 it has been attacking dimensions of the egg, after Neţoiu and Tomescu (27), in . In Spain this pest reported in 2001(29). In are 0.35 x 0.25 mm. It is deposited isolated on the

96 underside of the foil, usually near a secondary vein and yellow, with a darker wings cover and head. It near the intersection with the main vein. The mature develops into a white, densely cocoon (27). larva of Parectopa robiniella is yellowish-green, with a Phyllonorycter robiniella in Romania usually brown head and reaches in the last age, a length of 4.0- has two generations, after Neţoiu (26), it could develop 4.5 mm. Pupa is 3.0-3.5 mm long, first greenish then a third generation in the long autumn years condition). brown. It develops inside a white cocoon, densely, The specie overwinters in the pupal stage. made by the larva on the attacked leaf. The female places the eggs on the underside In Romania the species develops 2-3 of the leaf, usually many eggs on a leaf. The hatched generations per year (25, 27). It winters as last age larvae develop a stigmatonomous type mine on the larva in a cocoon on the fallen leaves on the ground. In lower face of the acacia foil, the gallery having an oval spring, it take place a gradual transformation in pupae shape. This gallery never crosses the main vein. At the (14). mine level the lower epidermis remains whitish and the The female deposits the eggs on the underside upper one and the leading vessels become brown over of the leaf, usually at the main vein intersection with a time. The excrements remain inside the mine in the secondary vein. The damage caused by Parectopa central area. The mines developed by the larvae often robiniella is represented by the digit form mine. The merge (32). At this species, the average surface area of larva creates a crack in the lower epidermis, where it a mine is 1.4 cm², so 3-4 mines/foil can cover the entire removes the excrement, so that the upper part remains surface of the foliage (22). permanently clean. The surface of the mine is between As the larvae of Parectopa robiniella, the 0.14-1.24 cm² (10), so 5-6 fully developed mines can damage caused by Phyllonorycter robiniella larvae is cover the surface of a sheet (24). of a physiological-primary nature, causing damage by Phyllonorycter robiniella was first reported in both the mines resulting from feeding the larvae to the Europe in 1983 in Basel, Switzerland. Later, the foliage and by the premature fall of the attacked presence was reported in France (42); Northern Italy, foliage. The pest causes the greatest damage to young 1988, (1, 36); , 1989, (15); The Netherlands, trees, affecting their growth and flowering (22). 1989, (9, 16, 30); Germany, 1989, (4, 11, 12, 28); Slovakia, 1992, (19); , 1994, (34); Hungary, Material and Method 1998, (5, 14, 37); Bosnia Herzegovina, 2000, (6); Croatia, 2001, (22); Poland, 2002; Russia, 2005,(13); In August 3-10 and September 17-23, 2017, Lithuania, 2008, (17). was noted the frequency of the attack caused by the In our country, Phyllonorycter robiniella was two moths of the acacia, Phyllonorycter robiniella reported in 2002 at Păuşa, on the left bank of the Olt Clemens and Parectopa robiniella Clemens, as well as River near Călimăneşti locality, and the following year the number of mines they develop on a leaf of acacia. it poorly infested the acacia crops in the Calafat and The observations were made in two locations Poiana Mare areas. Ureche (38), reported it in Bacău with different pedoclimatic conditions: County (Hemeius Park) also in 2002, and in 2005 it  Valea lui Mihai, Satu Mare County, in an reports in the Letea Forest, in the Sulina area, the acacia forest of 24 ha; Danube Delta. In Covasna County, the presence of the  Covasna, Covasna County, to the acacia of the two species has been reported since 2006, and studies parks and green zones. of the population dynamics of these species, as well The observations on the proposed objectives studies on the frequency and severity of the attack have were made at each location approximately in the same been published since 2010 (7, 8). calendar interval, and the biological material samples The adult of the Phyllonorycter robiniella were collected at a one-month interval to compare and species has a 5-6 mm wingspan. The front wing is report as accurately as possible trends in the frequency brown-orange, with pale gray to the costal area. In the and the intensity of the attack. basal area there are white spots surrounded by light- For these determinations, 100 leaves of 10 gray scales. On the costal edge, there are four white trees (in total 1000 leaves) were harvested. Then, in the stripes, the first two are clearly contoured, and the last laboratory, the attacked leaves were inventoried. The two with a diffuse in a gray-outward contour. In the identification of the two species that attack the acacia apical area there is a black spot. The rear wing is pale- was done according to the characteristics of the mines gray, narrow, with brown hair (27). The egg is very developed by the two species (fig.1). Figure 2 shows small, 0.25-0.3 x 0.18-0.20 mm, and is deposited on the larvae of the two species. the underside of the foil far from a secondary vein. The From the collected material, were separated color is light green, similar to the color of the acacia the leaves attacked only by Phyllonorycter robiniella, leaves (26, 32, 33). The larva passes through 5 larval those attacked only by Parectopa robiniella, and those stages (32). At maturity, the larva usually has a body attacked simultaneously by both species. length of 3.5-4.0 mm and is white to yellowish, with a brown head. Pupa is 3.0-3.5 mm in size, it is brownish-

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A B C

Fig. 1 A) Damaged Acacia; B) Mine of Parectopa robiniella; C) Mine of Phyllonorycter robiniella (original, foto Hulujan)

A B

Fig. 2 A) Larvae of Phyllonorycter robiniella; B) Larvae of Parectopa robiniella (original, foto Hulujan)

Obtained results of the leaves, a doubling of the frequency of the attack against the previous monitoring term. Phyllonorycter Table 1 shows the results of the monitoring of robiniella was reported on 28% of the leaves analyzed the frequency of the attack caused by the acacia mining (26% of the leaves alone and 2% together with in 2017 in Covasna city. Parectopa robiniella). The frequency of attack of the At the observation of the first decade of species Parectopa robiniella was 3% (1% of solitary August, it was found that the two species of mining attacked leaves and 2% of the leaves attacked with attacked 14% of the acacia leaves. Phyllonorycter robiniella). In this interval, Phyllonorycter robiniella was reported on 13% of the Phyllonorycter robiniella was the species that had the analyzed leaves (12% of the leaves were attacked highest rate of attack rate increase 2,2 (two points solitary and 1% of the leaves attacked with Parectopa twice) over the previous observation. robiniella). Parectopa robiniella was reported on 2% In acacia mining moths, besides monitoring of the analyzed leaves (1% of the leaves alone and 1% the frequency of the attack, we also proceeded to of the leaves together with Phyllonorycter robiniella). determine the number of mines that species are We find that from the attacked leaves, 13% of them spreading on a leaf. This parameter was followed both were attacked by only one species, and 1% of the on the leaves attacked by one species, but on the leaves leaves were reported to me developed by both species. showing the attack produced by Phyllonorycter Monitoring in September reported an increase robiniella and Parectopa robiniella.. in the frequency of the attack, this time attacking 29%

98 At the first observation, the average number were 2.8 mines/leaf at Phyllonorycter robiniella and a of mines on a leaf attacked by one species was 3.4 mine/leaf at Parectopa robiniella. The average number mine/leaf at Phyllonorycter robiniella and 1.1 of mines reported on the attacked leaves of the mine/leaf at Parectopa robiniella. When mining moths analyzed sample was 3.3 mine/leaf. simultaneously attacked a leaf, the developed galleries Table 1 Dynamics of the attacked leaves by leaf mining moths and the number of mine/leaf, Covasna, 2017 3.08 - 10.08 17.09 - 23.09 SPECIES attacked average no. of attacked average no. of leaves  mines/leaf leaves  mines/leaf Phyllonorycter robiniella 12 3,4 26 6,3 Parectopa robiniella 1 1,1 1 1,1 Phyllonorycter robiniella+ 1 2,8 + 1,0 2 4,7 + 1,2 Parectopa robiniella TOTAL ATTACKED LEAVES 14 3,3 29 5,9

At the September observation, on the leaves attacked Parectopa robiniella. The average number of mines by only one species, the number of mines reached 6.3 reported on the attacked leaves in the analyzed sample mines/leaf at Phyllonorycter robiniella and 1.1 was 5.9 min/leaf. mins/leaf at Parectopa robiniella. When mining moth The results of monitoring the frequency of the attacked concurrently, it was 4.7 mines/leaf to attack caused by the mining moths in the acacia tree at Phyllonorycter robiniella and 1.2 mines/leaf to Valea lui Mihai are presented in Table 2.

Table 2 Dynamics of the attacked leaves by leaf mining moths and the number of mine/leaf, Valea lui Mihai, 2017 3.08 - 10.08 17.09 - 23.09 SPECIES attacked average no. of attacked average no. of leaves  mines/leaf leaves  mines/leaf Phyllonorycter robiniella 4 3,1 2 4,3 Parectopa robiniella 7 8,7 11 15,3 Phyllonorycter robiniella+ 53 4,9 + 9,2 76 6,7 + 13,1 Parectopa robiniella TOTAL ATTACKED LEAVES 64 12,8 89 18,9

From the data presented in the table, it is mines/leaf at Parectopa robiniella. When mining observed that in the area investigated the mining moths simultaneously attacked a leaf, the developed population populations have a very high numerical galleries were 4.9 mines/leaf at Phyllonorycter density. Due to this, the frequency of the attack in the robiniella and 9.2 mines/leaf at Parectopa robiniellas. first decade was 64%. Minerals of the species The average number of mines reported on the attacked Parectopa robiniella were reported on 60% of the leaves of the analyzed sample was 12.8 mines/leaf. analyzed leaf sample (7% of the leaves attacked alone At the September observation, on the leaves and 53% of the leaves attacked with Phyllonorycter attacked by only one species, the number of mines robiniella). Phyllonorycter robiniella had an attack reached 4.3 mines/leaf at Phyllonorycter robiniella and frequency of 57%, of which only 4% of the leaves were 15.3 mines/leaf at Parectopa robiniella. When mining reported alone. mites attacked concurrently, it was 6.7 mines/leaf to At September monitoring, the attack rate Phyllonorycter robiniella and 13.1 mines/leaf to reached 89%, an extremely strong attack that caused an Parectopa robiniella. The average number of mines early fall of the leaves. Parectopa robiniella attacked reported on the attacked leaves in the analyzed sample 87% of the acacia leaves (11% of the leaves attacked was 18.9 min/leaf. The maximum number of meals alone and 76% of the leaves attacked with reported on a leaf was 118, the leaf being entirely Phyllonorycter robiniella). The attack of covered by me. Phyllonorycter robiniella frequency was 78%, of It is noted that when moths attack which only 2% of the leaves were reported alone. simultaneously, the total number of mines on a leaf is Regarding the average number of higher than when moths each solitary attack. In this mines/leaves, in the August observation on a leaf situation, the average number of mines/leaves was 14.1 attacked by one species, this parameter was 3.1 in August and 19.8 in September. mines/leaf at Phyllonorycter robiniella and 8.7

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Given that the moth mines, as shown in the the biological material harvested at Valea lui Mihai, we literature, reach a size of more than 1 cm² (10, 22), it is analyzed the mines on the foliage of the attacked leaves possible to affect almost entirely the surface of a foil at (fig.3).

Fig. 2 Leaves attacked by Parectopa robiniella (original, foto Hulujan)

From the collected biological material, we Conclusions randomly chose three samples of attacked leaves, 50 leaves per sample. The total number of foliage on each 1.Mine species, Parectopa robiniella and leaf in the sample was counted, then the attacked ones Phyllonorycter robiniella, constitute a real danger to were separated, with the number of mines and the acacia stands and strongly affect the aesthetic value of species that produced the mine. acacia in landscaping. The average number of foils on the 50 leaves 2.The numerical density of the acacia moth populations in the sample was 922 foils. Of these, 164 were is correlated with the pedoclimatic conditions; In Valea unattached, and 758 foils presented mines, so the lui Mihai, the dominant species is Parectopa proportion of the infected foils was 82.2%. On the robiniella, and in the town of Covasna is attacked foliage the distribution of the attack on the Phyllonorycter robiniella. two species was as follows: 3.At the end of the biological cycle of the two species, Foils that were only attacked by Parectopa the frequency of the attack reached 29% in Covasna robiniella were 459, representing 60.6% of the total of and 89% in Valea lui Mihai. the attacked foils. On these foils we counted 781 4.The average number of mines/leaves developed by mines, averaging 1.7 mines/foil. The maximum Phyllonorycter robiniella (in case of single attack) was number of mines of this species on a foil was 7 mines. 6.3 mines at Covasna and 4.3 mines at Mihai Valley. The Phyllonorycter robiniella species was 5.The average number of mines/leaves developed by singly signaled on 86 foil, representing 11.3% of the Parectopa robiniella (in case of single attack) was 1.1 attacked foliage. The number of mines on these foils mines at Covasna and 15.3 mines at Mihai Valley. was 102, returning an average of 1.2 mines/foil. The 6.Leaves attacked simultaneously by both species maximum number of mines of this species on a foil showed an average number of 5.9 mines in Covasna was 3 mines. (4.7 mines of Phyllonorycter robiniella and 1.2 mines The two species simultaneously attacked 213 of Parectopa robiniella), respectively 19.8 mines at foils (28.1% of the total of the attacked foliage). A Valea lui Mihai (6.7 mines of Phyllonorycter robiniella number of 461 mines produced by Parectopa and 13.1 mines of Parectopa robiniella). robiniella (an average of 2.6 mines/foil) and 279 mines developed by Phyllonorycter robiniella (an average of Bibliography 1.3 mines/foil) were reported on these foliage. It is found that when the two species simultaneously attack 1.Arzone A., Vidano C., 1990, Insetti esotici di nuova the total number of mines/foil is higher, in this introduzione in Italia e in Piemonte, Informatore situation there is an average number of 3.9 mines/foil. Fitopatologico, 40(7-8): 47-54. The maximum number of mines on a folate attacked 2.Bakó Z., Seprős I., 1987, Új kártevő Magyarországon simultaneously by the two species was 6 mines (5 az akác aknázómoly Parectopa robiniella (Lep., mines of Parectopa robiniella and one of Gracillariidae), Növényvédelem, 23: 236–239. Phyllonorycter robiniella mine). 3.Baugnée J.Y., 2014, Parectopa robiniella (Lepidoptera: Gracillariidae), a leafminer of black locust , new to the Belgian fauna. Phegea, 42(3): 55-57.

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