Journal of Pest Science

, Volume 78, Issue 2, pp 109–114

Parasitoid complex of Phyllonorycter robiniella (Clemens, 1859) (Lepidoptera, Gracillariidae) in Serbia

Authors

  • Aleksandar Stojanović
    • Natural History Museum
    • Faculty of ForestryBelgrade University
Original Article

DOI: 10.1007/s10340-004-0077-y

Cite this article as:
Stojanović, A. & Marković, Č. J Pest Sci (2005) 78: 109. doi:10.1007/s10340-004-0077-y

Abstract

In a study of the parasitoid complex of the locust leaf miner Phyllonorycter robiniella (Clemens, 1859), 23 species of its parasitoids were recorded at 18 localities in Serbia. The parasitoid species included 2 species of the family Braconidae, 1 of the family Eupelmidae, and 20 of the family Eulophidae. The recorded species of parasitoids are polyphagous; in addition to Ph. robiniella, they also develop on other species of leaf miners as primary; primary and secondary; or primary, secondary, and tertiary parasitoids. Among the recorded species of parasitoids, the most significant were the species Pholetesor bicolor, Pholetesor nanus, Sympiesis sericeicornis, Sympiesis acalle, Minotetrastichus frontalis, Pediobius saulius, and Baryscapus nigroviolaceus. The parasitoids were found to have a strong effect on the abundance of Ph. robiniella because they reduced more than 50% of its larvae and pupae in the majority of study samples.

Keywords

ParasitismParasitoidsPhyllonorycter robiniellaRobinia pseudoacaciaSerbia

Introduction

The black locust or false acacia Robinia pseudoacacia Linnaeus is a North American species of tree that was introduced to Europe (France) at the beginning of the 17th century (in 1601). Today it is widely cultivated in much of Europe on account of its fast growth, modest soil requirements, good wood, and ability to bind loose soils well. Unfortunately, in central Europe and the greater part of southern Europe, it is highly infested by the leaf miner Phyllonorycter robiniella, a North American species of moth introduced to Europe. In Europe, this moth was first reported in Switzerland (near Basel) in 1983. From there its range has spread extensively across Europe (Šefrová 2003). Due to the high abundance of its populations, premature defoliation of R. pseudoacacia occurs frequently.

In addition to Ph. robiniella, the miner Parectopa robiniella Clemens (Lepidoptera, Gracilariidae) also develops on leaves of black locust in Europe. It, too, is a North American species introduced to Europe (1970, Italy) (Mihajlović et al. 1994). However, in comparison with Ph. robiniella, it occurs in Serbia considerably more rarely and is only massively present on sandy terrains (the Delibato, Ram-Golubac, and Kladovo Sands), where it causes premature defoliation.

Ph. robiniella develops three overlapping generations per year. It hibernates in the imago stage. Moths of the first generation are present from mid-June to the beginning of August, those of the second generation from the beginning of August to mid-September, and those of the third (hibernating) generation from mid-August to mid-May. In May (when leaves of black locust appear), females that have completed hibernation oviposit abaxially on the leaf, usually laying several eggs per leaf. After 6–10 days the larvae hatch and bore directly into the leaf, creating mines in the shape of an elongated oval under the epidermis on the leaf’s abaxial surface. Initially visible only on the abaxial surface of the leaf, the mines later become visible on its adaxial surface as well. Because the female lays a number of eggs per leaf, several mines sometimes merge into a single common mine in which a number of larvae are present. Larval development is highly irregular and lasts 20–50 days, depending on weather conditions. Toward the end of their development, the larvae spin a white cocoon in which they pass over into the pupal stage. In this stage, Ph. robiniella spends 7–10 days in summer and 10–20 days in winter. Prior to eclosion, the pupa breaks through the cocoon and leaf epidermis abaxially and more than half its length emerges from the mine, after which eclosion occurs (Gibogini et al. 1994; Dimić et al. 2000; Csóka 2001; Šefrová 2001).

A fairly large number of parasitoids have so far been recorded on Ph. robiniella in Europe (Serini 1990; Whitebread 1990; Deschka 1995; Gibogini et al. 1996; Hellrigl 2001; Csóka et al. 2003):
  • Ichneumonoidea
    • Braconidae
      • Colastes braconius Haliday

      • Pholetesor bicolor (Nees)

      • Pholetesor circumscriptus (Nees)

      • Pholetesor nanus (Reinhard)

  • Chalcidoidea
    • Eulophidae
      • Baryscapus nigroviolaceus (Nees)

      • Chrysocharis nephereus (Walker)

      • Chrysocharis laomedon (Walker)

      • Minotetrastichus frontalis (Nees) (=ecus Walker)

      • Minotetrastichus platanellus (Mercet)

      • Sympiesis sericeicornis (Nees)

      • Sympiesis xanthostoma (Nees)

      • Sympiesis acalle (Walker)

      • Cirrospilus elegantissimus Westwood

      • Cirrospilus viticola (Rondani) (=subviolaceus Thomson)

      • Cirrospilus variegatus (Masi)

      • Closterocerus trifasciatus (Westwood)

      • Pediobius saulius (Walker)

The significance of parasitoids of Ph. robiniella in Europe has been studied so far by several authors (Angeli et al. 1996; Gibogini et al. 1996; Dimić et al. 2000; Šefrová 2001; Wojciechowicz and Jankowska 2004). According to the results of their investigations, the level of parasitism of this species is quite variable and ranges from 10 to more than 60%.

In Serbia, Ph. robiniella was first recorded in 1998 (Šefrová 2003). As black locust is a common species in Serbia and is widely cultivated in certain parts of the country, the appearance of this new pest here is of great significance. We therefore conducted a detailed study of its parasitoids.

Materials and methods

The parasitoid complex of Ph. robiniella was studied at the following 18 localities in central and southern Serbia: Aleksinac-Bobovište, Aleksinac-Deligrad, Ćićevac, Jagodina, Jagodina-Bagrdan, Kruševac-Djunis, Kruševac-Kapidzija, Lapovo-Brzan, Mala Krsna, Niš-Toponica, Obrenovac, Paraćin, Ražanj, Topola, Topola-Donja Trešnjevica, Trstenik, Ub, and Velika Plana. At each locality, five R. pseudoacacia trees attacked by Ph. robiniella were selected at random. During the years 2002 and 2003, 70 infested leaves were collected from the selected trees several times from mid-July to mid-October. Due to generational overlapping, leaves in each of the samples had mines with different larval stages (mainly IV and V), pupae, and mines from which adults had emerged. Upon being brought into the laboratory, the leaves were placed in emergence boxes, which were kept in the insectarium under field conditions. During the flight of Ph. robiniella and its parasitoids, the emergence boxes were examined daily. The emerged adults were collected, killed by ether, prepared, identified (by A. Stojanović), and counted. The parasitoid adults are stored in the collection of the Faculty of Forestry in Belgrade.

A total of 44 samples were collected. The significance of Ph. robiniella parasitoids was assessed based on the following:
  1. 1.

    Number of samples in which a parasitoid species was identified

     
  2. 2.

    Dominance (relation between the number of parasitoid adults of a particular species and the total number of parasitoids, in percent)

     

The level of parasitism of Ph. robiniella (the percentage of parasitized hosts in a sample) was established by dissection. In 2003 at the localities mentioned and at Aleksinac-Tešica, Kruševac, Mrčajevci, Sokobanja, and Zaječar, 15 attacked leaves were collected at the time when mines for the most part housed larvae in stages IV and V and pupae. On being brought into the laboratory, the mines on leaves were counted and then opened. Dead larvae and pupae were recorded. Living larvae and pupae were dissected.

Results

Twenty-six species of parasitoids were recorded in our investigations. Table 1 presents the recorded species of parasitoids, their taxonomic affiliation, and their status. The total number of obtained imagoes of each parasitoid species and their frequency of occurrence in the examined samples are shown in Table 2.
Table 1

Recorded species of parasitoids and their status

Species

Statusa

Primary

Secondary

Tertiary

Endoparasite

Ectoparasite

Solitary

Gregarious

Ichneumonoidea

 Ichneumonidae

  Stictopisthus formosus (Bridgeman)

 

+

 

+

 

+

 

 Braconidae

  Pholetesor bicolor (Nees)

+

  

+

 

+

 

  Pholetesor nanus (Reinhard)

+

  

+

 

+

 

Chalcidoidea

 Eurytomidae

  Eurytoma goidanichi (Bouček)

 

+

  

+

  

 Eupelmidae

  Eupelmus urozonus (Dalman)

+

+

  

+

+

 

 Pteromalidae

  Catolaccus ater (Ratzeburg)

 

+

  

+

+

 

 Eulophidae

  Achrysocharoides cilla (Walker)

+

  

+

 

+

 

  Baryscapus nigroviolaceus (Nees)

+

+

+?

+

 

+

 

  Chrysocharis nephereus (Walker)

+

  

+

 

+

 

  Cirrospilus elegantissimus (Westwood)

+

   

+

+

 

  Cirrospilus lyncus (Walker)

+

r+

  

+

+

 

  Cirrospilus pictus (Nees)

+

r+

  

+

+

 

  Cirrospilus talitzkii (Bouček)

+

   

+

+

 

  Cirrospilus variegatus (Masi)

+

   

+

+

 

  Cirrospilus viticola (Rondani)

+

r+

  

+

+

 

  Closterocerus trifasciatus (Westwood)

+

r+

 

+

 

+

 

  Minotetrastichus frontalis (Nees) (=ecus Walker)

+

+

+

 

+

 

+

  Neochrysocharis cf. Chlorogaster (Erdös)

+

  

+

 

+

 

  Neochrysocharis formosa (Westwood)

+

  

+

 

+

 

  Pediobius saulius (Walker)

+

+

r+

+

 

+

 

  Pnigalio agraules (Walker)

+

r+

  

+

+

 

  Pnigalio pectinicornis (Linnaeus)

+

+

  

+

+

 

  Sympiesis acalle (Walker)

+

+

  

+

+

 

  Sympiesis gordius (Walker)

+

+

  

+

+

 

  Sympiesis gregori (Bouček)

+

   

+

+

 

  Sympiesis sericeicornis (Nees)

+

+

  

+

+

 

aThe status of the obtained parasitoid species is given according to Bouček and Askew (1968), Graham (1969, 1987, 1991), Papp (1988), Schwenke (1999), and Zverova (1992)

r Rare

Table 2

Total number of imagoes obtained in the insectarium and their frequency of occurrence in the collected samples

Species

Obtained imagoes (n)

Frequency in the study samples

Samples (n)

%

Achrysocharoides cilla

1

1

2.3

Baryscapus nigroviolaceus

89

23

52.3

Catolaccus ater

2

1

2.3

Chrysocharis nephereus

5

2

4.5

Cirrospilus elegantissimus

2

1

2.3

Cirrospilus lyncus

3

2

4.5

Cirrospilus pictus

17

9

20.5

Cirrospilus talitzkii

7

2

4.5

Cirrospilus variegatus

1

1

2.3

Cirrospilus viticola

40

14

31.8

Closterocerustrifasciatus

3

3

6.8

Eupelmus urozonus

1

1

2.3

Eurytoma goidanichi

1

1

2.3

Minotetrastichus frontalis

251

35

79.5

Neochrysocharis cf. chlorogaster

2

2

4.5

Neochrysocharis formosa

11

8

18.2

Pediobius saulius

141

35

79.5

Pholetesor bicolor

48

21

47.7

Pholetesor nanus

40

8

18.2

Pnigalio agraules

24

11

25.0

Pnigalio pectinicornis

10

7

15.9

Stictopisthus formosus

36

11

25.0

Sympiesis acalle

132

25

56.8

Sympiesis gordius

2

2

4.5

Sympiesis gregori

1

1

2.3

Sympiesis sericeicornis

640

38

86.4

As can be seen in Table 1, 23 species of parasitoids of Ph. robiniella and three species that are exclusively hyperparasitoids (Stictopisthus formosus, Eurytoma goidanichi, and Catolaccus ater) were recorded at the investigated localities in Serbia. Among the recorded parasitoids of Ph. robiniella, the species Achrysocharoides cilla, Chrysocharis nephereus, Cirrospilus elegantissimus, Cirrospilus lyncus, Cirrospilus talitzkii, Cirrospilus variegatus, Closterocerus trifasciatus, Eupelmus urozonus, Neochrysocharis cf. chlorogaster, Sympiesis gordius, and Sympiesis gregori were found rarely and in small numbers. It can therefore be stated that they were of little significance as parasitoids of Ph. robiniella during the present investigations.

Dissection of larvae and pupae of Ph. robiniella revealed that species of the genus Pholetesor have the greatest effect on the abundance of Ph. robiniella. Two species of Pholetesor, Pholetesor bicolor and Pholetesor nanus, were obtained from samples of attacked leaves in the insectarium (Table 1). The species Ph. bicolor was obtained from nearly twice as many samples (47.7%), so it can be said to have greater significance as a parasitoid of Ph. robiniella. In the samples dissected, the level of parasitism of Ph. robiniella by Ph. bicolor and Ph. nanus ranged from 22.8–63.8%. Moreover, their participation in the total level of parasitism ranged from 43.6–96.0%. The level of their hyperparasitism ranged from 6.6–53.8%, most often comprising about 10.0%. As the most frequent hyperparasitoids, we recorded species of the genus Sympiesis and Stictopisthus formosus.

Four species of the genus Sympiesis were obtained from the collected leaf samples in the insectarium (Table 1). Among them, only the species Sympiesis sericeicornis and Sympiesis acalle manifested any great abundance and frequency of occurrence (Table 2). The species S. sericeicornis was recorded in 86.4% of the samples and there was no locality at which it was not found. In the majority of samples (54.5%), it was the most abundant parasitoid, comprising as much as 92.3% of the sample collected on 17 October 2002 at the Velika Plana locality and 78.7% of the sample collected that same day at the Topola locality. Values of its dominance most often ranged between 20.0 and 50.0%. However, because S. sericeicornis is a primary and secondary parasitoid, it is difficult to estimate the extent to which the obtained values of its dominance are a consequence of its primariness.

The species S. acalle also occurred frequently. It was recorded in 56.8% of the samples and was absent at only two localities. However, in relation to S. sericeicornis, its abundance was significantly lower. Values of its dominance most often ranged between 5.0 and 15.0%. However, because it (like S. sericeicornis) is a primary and secondary parasitoid, the intensity of its primariness is likewise open to question.

In addition to the species of the genera Pholetesor and Sympiesis described above, the species Minotetrastichus frontalis, Pediobius saulius, and Baryscapus nigroviolaceus also manifested fairly great abundance and frequency of occurrence among parasitoids of Ph. robiniella in the investigated samples.

M. frontalis was a frequent parasitoid of Ph. robiniella. It was recorded in 79.5% of the samples and there was no locality at which it was not found. M. frontalis was the dominant species in 11 (25%) of the samples, comprising as much as 79.6% of the sample collected on 20 September 2003 at the Jagodina-Bagrdan locality and 77.8% of the sample collected the same day at the Jagodina locality. In the majority of samples in which it was recorded, its dominance ranged between 5.0 and 25.0%. However, because it is a gregarious parasitoid, the obtained values of its dominance are probably somewhat overstated in relation to the real ones. The overstatement, however, is certainly not very great because we established by means of dissection that gregariousness of parasitoids of Ph. robiniella is weakly expressed. Moreover, since it is a primary, secondary, and tertiary parasitoid, the question of its primariness arises here too.

P. saulius and B. nigroviolaceus were also frequent parasitoids of Ph. robiniella. Pediobius saulius was recorded in 79.5% of the samples. It was not recorded at only one locality. Values of its dominance in samples where it was recorded most often ranged between 5.0 and 15.0%. B. nigroviolaceus was recorded in 52.3% of the samples. It was absent at only two localities. In the majority of samples in which it was recorded, values of its dominance were less than 10.0%.

Generally, it can be asserted that parasitoids had a great effect on the abundance of Ph. robiniella (Table 3). The percentage of its parasitized hosts in the examined samples ranged from 30.0–67.5% and exceeded 50.0% in the majority of samples. The level of hyperparasitism ranged between 5.4 and 46.7%; in the majority (71.4%) of samples it was between 5.4 and 15.0%.
Table 3

Results of dissection: role of disease, predators, and parasitoids in reduction of larvae and pupae of Ph. robiniella, and established level of hyperparasitisma

Locality and date of sampling

Mines (n)

Larvae and pupae

Living

Disease-killed

Predator-reduced

Parasitized

With hyperparasites

Larvae

Pupae

n

%

n

%

n

%

n

%*

Aleksinac-Bobovište, 13.6.2003

86

62

23

0

0.0

14

14.1

56

56.6

3

5.4

Aleksinac-Deligrad, 13.6.2003

25

20

18

2

3.4

19

32.2

18

30.5

2

11.1

Ćićevac, 4.8.2003

74

60

9

0

0.0

22

24.2

35

38.5

3

8.6

Jagodina, 4.8.2003

54

36

8

1

1.8

12

21.1

33

57.9

2

6.1

Jagodina-Bagrdan, 4.8.2003

95

94

21

0

0.0

5

4.2

81

67.5

9

11.1

Kruševac, 13.6.2003

71

40

37

0

0.0

5

6.0

34

41.5

4

11.7

Kruševac-Djunis, 13.6.2003

88

44

62

0

0.0

13

10.9

43

36.1

5

11.6

Kruševac-Kapidžija, 13.6.2003

97

39

67

0

0.0

8

7.0

42

36.8

5

11.9

Lapovo-Brzan, 31.8.2003

84

81

8

1

0.9

14

13.5

58

55.8

6

10.3

Mala Krsna, 16.6.2003

47

25

22

0

0.0

5

9.6

26

50.0

4

15.4

Mrčajevci, 13.6.2003

38

31

7

0

0.0

4

9.5

26

61.9

2

7.7

Niš-Toponica, 15.6.2003

40

31

7

0

0.0

6

13.6

29

65.9

3

10.3

Obrenovac, 9.6.2003

45

48

2

1

1.9

1

1.9

32

61.5

6

18.8

Paraćin, 4.8.2003

42

36

1

0

0.0

23

38.3

18

30.0

3

16.7

Ražanj, 31.8.2003

61

33

10

0

0.0

27

38.5

21

30.0

2

9.5

Sokobanja, 16.6.2003

58

38

20

0

0.0

14

19.5

37

51.4

6

16.2

Topola, 26.6.2003

40

37

8

0

0.0

4

8.2

30

61.2

14

46.7

Trstenik, 13.6.2003

75

44

24

1

1.1

18

20.7

31

35.6

3

9.7

Zaječar, 13.6.2003

65

46

20

2

2.6

8

10.5

40

52.6

4

10.0

Ub, 9.6.2003

68

71

9

1

1.2

0

0.0

54

66.7

15

27.8

Velika Plana, 4.8.2003

40

23

6

0

0.0

13

31.0

15

35.7

1

6.7

aThe percentage of hyperparasitism is given as the ratio of hyperparasitized to parasitized larvae and pupae

In relation to parasitoids, predators were of less significance in reduction of Ph. robiniella. Predator-reduced larvae and pupae were regularly found in dissected samples, but their number in comparison with the number of parasitized larvae and pupae was usually discernibly smaller (Table 3). Diseased larvae and pupae were rarely found.

Discussion

Results of the present study and those of Csóka et al. (2003), Deschka (1995), Gibogini et al. (1996), Hellrigl (2001), Serini (1990), and Whitebread (1990) indicate that following its introduction to Europe, Ph. robiniella has become host to a large number of parasitoids. Its parasitoids are broadly polyphagous species; in addition to Ph. robiniella, they also develop on other species of leaf miners as solitary or gregarious; primary; primary and secondary; or primary, secondary, and tertiary parasitoids (Bouček and Askew 1968; Graham 1969, 1987, 1991; Pschorn-Walcher 1980; Mey 1991, 1993; Zverova 1992; Stojanović and Marković 2004). Certain species of the parasitoids of Ph. robiniella are also parasitoids of the locust leaf miner Parectopa robiniella (Serini 1990; Mihajlović et al. 1994).

We recorded 23 species of parasitoids of Ph. robiniella in Serbia. Many of them are already known parasitoids of Ph. robiniella in central Europe (see Introduction).

Taking into account the frequency of occurrence of the investigated species of parasitoids, their dominance, and results obtained by dissection, we established that the species Ph. bicolor, Ph. nanus, S. sericeicornis, S. acalle, M. frontalis, P. saulius, and B. nigroviolaceus were of the greatest significance as parasitoids of Ph. robiniella at the investigated localities in Serbia. According to Csóka et al. (2003), the most significant parasitoid of Ph. robiniella in Hungary is the species Ph. nanus, while Gibogini et al. (1996) reported that Ph. bicolor, B. nigroviolaceus, and M. frontalis are its most significant parasitoids in Italy. However, since among the mentioned species of parasitoids, Ph. bicolor and Ph. nanus are only primary parasitoids, data given on other species of parasitoids must always be taken provisionally.

As to the significance of parasitoids in reduction of Ph. robiniella, different data can be found in the literature. According to Šefrová (2001), parasitism of Ph. robiniella was not great and ranged between 10 and 30%. According to Wojciechowicz and Jankowska (2004), it did not exceed 40%, while Angeli et al. (1996) indicated that it varied between 35 and 50%. According to Gibogini et al. (1996) and Dimić et al. (2000), it was greater than 60%. The results that we obtained indicate that the level of parasitism of Ph. robiniella in Serbia is fairly high. It varied between 30 and 67.5% in the examined samples and was greater than 50% in the majority of them.

Apart from Ph. robiniella, a high level of parasitism has also been recorded in other species of leaf miners. For example, it is greater than 55% in Coleophora serratella Linnaeus (Lepidoptera, Coleophoridae) (Pschorn-Walcher 1980) and greater than 50% in the second generation of Leucoptera malifoliella (Costa) (Lepidoptera, Lyonetiidae) (Mey 1993).

At the time when Ph. robiniella was introduced to Europe, the miner Cameraria ohridella Deschka & Dimić (Lepidoptera, Gracillariidae) appeared on leaves of Aesculus hippocastanum Linnaeus on the Balkan Peninsula. Its spread across Europe (like that of Ph. robiniella) took place fairly rapidly, so that in a short time it occupied the region of central Europe and the greater part of eastern and southern Europe (Šefrová 2003). Like Ph. robiniella, it became host to a large number of parasitoids. However, they are much less significant than the parasitoids of Ph. robiniella. To be specific, the level of parasitism of C. ohridella usually does not exceed 10% (Stojanović and Marković 2004). This is probably because species of the genus Pholetesor do not parasitize C. ohridella.

Even though the role of predators in reducing Ph. robiniella was greater than that of parasitoids in several samples, it can be stated that predators are still less significant. However, it is important to point out that parasitoids and predators together significantly reduced the abundance of Ph. robiniella. The combined level of reduction was usually more than 60%. By way of contrast, diseases only insignificantly affected the abundance of Ph. robiniella. In samples where diseased larvae and pupae were found (and the number of such samples was small), the level of reduction attained 3.4% at most. A small effect of disease on the abundance of Ph. robiniella was also reported by Angeli et al. (1996).

In light of all the foregoing considerations, it can be stated that Ph. robiniella is a species that has acquired a large number of natural enemies among parasitoids in Europe. Alone or together with predators, the parasitoids significantly reduce the abundance of Ph. robiniella.

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© Springer-Verlag 2005