Electronic Journal of Polish Agricultural Universities (EJPAU) founded by all Polish Agriculture Universities presents original papers and review articles relevant to all aspects of agricultural sciences. It is target for persons working both in science and industry,regulatory agencies or teaching in agricultural sector. Covered by IFIS Publishing (Food Science and Technology Abstracts), ELSEVIER Science - Food Science and Technology Program, CAS USA (Chemical Abstracts), CABI Publishing UK and ALPSP (Association of Learned and Professional Society Publisher - full membership). Presented in the Master List of Thomson ISI.
2007
Volume 10
Issue 1
Topic:
Horticulture
ELECTRONIC
JOURNAL OF
POLISH
AGRICULTURAL
UNIVERSITIES
Kot I. 2007. PARASITIC ENTOMOFAUNA OF LEAF TORTRICIDS (Lepidoptera: Tortricidae) OCCURRING IN APPLE ORCHARDS, EJPAU 10(1), #27.
Available Online: http://www.ejpau.media.pl/volume10/issue1/art-27.html

PARASITIC ENTOMOFAUNA OF LEAF TORTRICIDS (LEPIDOPTERA: TORTRICIDAE) OCCURRING IN APPLE ORCHARDS

Izabela Kot
Department of Entomology, University of Life Sciences in Lublin, Poland

 

ABSTRACT

The studies were carried out in the years 1999-2001 in apple orchards in the vicinity of Lublin (Poland). The purpose of the present study was to establish the species composition of parasitoids belonging to the order Hymenoptera and Diptera, and the degree of parasitization of caterpillars and pupae of leaf tortricids (Lepidoptera: Tortricidae) in apple orchards characterized by varying intensity of plant protection. Parasitic entomofauna was the most numerous in apple orchard without any chemical control, where the degree of parasitization of larvae and pupae of leaf tortricids ranged from 7.2% to 26.4% depending on the year of studies. In this apple orchard 23 species of parasitic Hymenoptera belonging to 2 families (Ichneumonidae and Braconidae) as well as 6 species of Diptera from the family of Tachinidae were isolated. Parasitoids from the family of Ichneumonidae (Hymenoptera) turned out to be the most effective, and the dominating species was ectoparasitoid Phytodietus segmentator Grav. The most numerous among all the parasitic Diptera: Tachinidae was Eumea linearicornis Zett.

Key words: tortricids, Lepidoptera, Tortricidae, parasitoid, Ichneumonidae, Braconidae, Tachinidae, apple orchard.

INTRODUCTION

Tortricids (Tortricidae) belong to one of the most numerous families of Lepidoptera. They play an important role in plant protection due to a big number of harmful species and frequent occurrence on different cultivations. In recent years the observations conducted in apple orchards have shown that the population and the economic importance of these phytophagous species is increasing, which often makes the use of chemical control necessary. However, tortricids are attended by a big number of natural enemies and that is the reason why a lot of attention is given to the preparation of programs of controlling them by means of selective treatment.

Within the beneficial entomofauna accompanying the leaf tortricids in apple orchards a big role is played by parasitic insects, both from the order of Hymenoptera and Diptera. They attack the larvae and pupae of tortricids, limiting the density of their population. In this way they contribute to the stability in biocenosis. The data concerning the species composition and the role that parasitoids play in limiting the population of leaf tortricids are included both in Polish [11, 12, 13, 14, 15, 16, 18, 20] and foreign literature [1, 2, 3, 5, 8, 19].

The parasitoids to leaf tortricids in the order to Hymenoptera are representatives of the family Ichneumonidae and Braconidae and also superfamily Chalcidoidea. On the other hand, Diptera are represented by the family Tachinidae.

The parasitic ichneumons (Ichneumonidae) attacking leaf tortricids belong to nearly all biological categories of parasitoids: ecto- and endoparasites, mono-, olygo- and polyphagous, parasites to eggs, caterpillars, pupae; parasites of the first and second degrees as well as gregarious parasites [4]. Parasites of leaf tortricids from the family Braconidae are endoparasites showing adaptability usually to a taxonomically narrow group of hosts. Most Braconidae are olygo- and monophagpus species, with no polyphagous ones or superparasitoids [10]. On the other hand, parasitic insects belonging to the order Diptera: Tachinidae are primary endoparasites, most frequently olygo- and polyphagous ones [7].

The purpose of the present paper was to establish the species composition of parasitoids belonging to the order Hymenoptera and Diptera, and the degree of parasitization of caterpillars and pupae of leaf tortricids by those parasitoids in apple orchards of the vicinity of Lublin (Poland) characterized by varying intensity of plant protection.

MATERIAL AND METHODS

The studies were carried out in the years 1999-2001 in three apple orchards in the vicinity of Lublin (Poland). Particular objects differed between each other with the cultivation system, the type of agrotechnical treatments and the intensity of utilization.

Site 1 is an orchard without any chemical control situated at Leonów (UTM FB 19), where no protective treatments or fertilization have been applied for a few years.

Site 2 is an orchard with a limited control program in Motycz (UTM EB 98). The chemical protection of plants in this orchard was used when the population of the pest exceeded the threshold of danger.

Site 3 is an intensively protected production orchard in Jastków (UTM FB 08).

45 trees located in different parts of the orchards were randomly selected in each of the studied sites. Five branches were randomly selected on each tree and the flower-leaf rosettes and then the leaf rosettes were observed there, picking up the caterpillars and the pupae of leaf tortricids. These were taken to an insectarium and placed singularly in flasks. The observations were carried out within 7-days’ intervals, between the phase of leaf bud breaking and the falling of leaves. The caterpillars kept in the insectarium were fed with the leaves of the host plant every day, and the culture was maintained until a moths or parasitoid imago was obtained. Parasitoids were stuck to little pieces of cardboard and they were meant for identification.

The name of HymenopteraParasitica was accepted after the key by Medvedev [9, 10], while that of Diptera: Tachinidae – according to Tschorsnig and Herting [22] and Tschorsnig and Richter [23].

RESULTS

During the studies totally 2593 caterpillars and 64 pupae of leaf tortricids were collected (tab. 1). Both the larvae and the pupae were most numerous in the orchard without any chemical control (Site 1), where 2518 larvae and 62 pupae were picked up. In the other two orchards, where the plant protection treatments were applied, caterpillars and pupae occurred sparsely.

Table 1. The total number of larvae and pupae of leaf tortricids (Lepidoptera: Tortricidae) colleted in studied apple orchards in 1999–2001

 

An orchard without chemical control
(Site 1)

An orchard with a limited control
(Site 2)

An orchard intensively protected
(Site 3)

Total

larvae

2518

62

13

2593

pupae

62

2

0

64

When the raising of larvae and pupae of leaf tortricids was maintained, numerous specimens of parasitoids from the order of Hymenoptera and Diptera were obtained (Photo 1-9), which made it possible to establish their species composition and determine the degree of their parasitization. Most parasitoids were obtained from caterpillars and pupae picked up in the unprotected orchard in Leonów (Site 1). Individual specimens of parasitic insects were obtained from the larvae collected in the orchard with a limited program of plant protection in Motycz (Site 2). No flights of the parasitic entomofauna were observed during the raising of tortricid larvae from the intensively protected orchard in Jastków (Site 3).

Photo 1. Itiplectis alternans Grav. (Ichneumonidae)

Photo 2. Phytodietus segmentator Grav. (Ichneumonidae)

Photo 3. Apophua bipunctoria Thunb. (Ichneumonidae)

Photo 4. Campoplex mutabilis Holmgr. (Ichneumonidae)

Photo 5. Campoplex sp. (Ichneumonidae)

Photo 6. Macrocentrus linearis Nees (Ichneumonidae)

Photo 7. Cotesia ater Ratz. (Braconidae)

Photo 8. Meteorus ictericus Nees (Braconidae)

Photo 9. Eumea linearicornis Zett. (Diptera: Tachinidae)

23 species of parasitic Hymenoptera belonging to 2 families (Ichneumonidae and Braconidae) and 12 subfamilies as well as 6 species of Diptera from the family of Tachinidae were isolated from the orchard without chemical protection (Site 1).

The most numerously represented family among the parasitoids belonging to Hymenoptera was the family of Ichneumonidae, which included 16 species, while the family of Braconidae included 7 species (tab. 2). Most of the obtained parasitoids turned out to be internal parasites. Only Phytodieyus segmentator Grav. from Ichneumonidae family belongs to outer parasites. Gregarious parasitoids were also found in the obtained material: Lissonota segmentellator Aubert (Ichneumonidae), Macrocentrus linearis Nees (Braconidae) and Cotesia ater Ratz. (Braconidae), as well as egg-larval parasitoids belonging to the subfamily Cheloninae and Macrogasterinae. Their females attack Lepidoptera eggs, but the development of the larvae of the parasite takes place in the caterpillar.

Table 2. The hymenopterous parasites (Hymenoptera – Parasitica) reared from larvea and pupae of leaf tortricids in the apple orchard without any chemical control (Site 1) in 1999–2001

Parasitoids

Number of individuals
(in specimens)

Total

1999

2000

2001

Number of individuals
(in specimens)

%

Ichneumonidae
Pimplinae
Acropimpla pictipes Grav.
Apechtis rufata Gmel.
Itoplectis maculator F.
Itoplectis alternans
Grav.





3



1
1
3
1





4



1
1
10
1



0.3
0.3
3.0
0.3

Tryphoninae
Phytodietus segmentator Grav.


44


51


16


111


33.1

Banchinae
Apophua bipunctoria Thunb.
Teleutaea striata Grav.
Lissonota segmentellator Aubert


22
1


27

2


22
1
3


71
2
5


21.2
0.6
1.5

Campopleginae
Campoplex mutabilis Holmgr.
Campoplex sp.
Diadegma ? fenestralis Holmgr.


8
6
3


1
1





9
7
3


2.6
2.1
0.9

Anomaloninae
Camposcopus canaliculatus Ratz.
Camposcopus perspicuus Wesm.


1
1






1
1


0.3
0.3

Metopiinae
Triclistus pygmaeus Cresson
Exochus lentipes Grav.


1


4
1




5
1


1.5
0.3

Mesochorinae
Mesochorus sp.



1



1


0.3

Braconidae
Macrocentrinae
Macrocentrus linearis Nees



4



2



4



10



3.0

Agathidinae
Agathis dimidiator Nees




1


1


0.3

Cheloninae
Ascogaster quadridentata Wesm.



1



1


0.3

Microgasterinae
Lissogaster globata L.
Cotesia longicauda Wesm.
Cotesia ater Ratz.



5
28


4
4
32


1
1
2


5
10
62


1.5
3.0
18.5

Euphorinae
Meteorus ictericus Nees


10


3


3


16


4.8

Total

137
(14 species)

140
(18 species)

58
(11 species)

335

 

A considerable part of parasitic Hymenoptera from the family Ichneumonidae are polyphagous species which can colonize representatives of different families from the order Lepidoptera, and only P. segmentator is an olygophagous species connected to the family of Tortricidae. Hymenoptera from the family Braconidae are olygophagous species, and in the case of Ascogaster quadridentata Wesm. specialization towards the subfamily Olethreutinae (Tortricidae) was observed.

Parasitoids of caterpillars distinctly prevailed within the rare of parasitic Hymenoptera (83.0% of the total number of species). The following species: Itoplectis maculator F., Itoplectis alternans Grav., Camposcopus canaliculatus Ratz. and Camposcopus perspicuus Wesm. belonging to the family of Ichneumonidae turned out to be parasitoids of tortricid pupae.

The main role in limiting the population of leaf tortricids was played by Hymenoptera. In all the studied years P. segmentator, constituting 33.0% of all the obtained parasitoids from the order of Hymenoptera, was the most numerous (tab. 2). The studies observed big populations of ichneumon Apophua bipunctoria Thunb., as well as Cotesia ater Ratz. of Braconidae, whose proportion in the total population of Hymenoptera-Parasitica was 21.2% and 18.5%, respectively. The proportion of the other species, both from Ichneumonidae and Braconidae, was small and did not exceed 5.0%.

The most numerous among all the parasitic Diptera: Tachinidae was Eumea linearicornis Zett., whose population constituted 73.8% of all the obtained individuals of this family (tab. 3). Individuals of this species developed both in the larvae and pupae of leaf tortricids. Dipteron Nemorilla floralis Fall., constituting 13.7% of all the Diptera, was much less numerous and the majority of specimens of this species underwent development in pupae of leaf tortricids. The population of the other species was on a much lower level, not exceeding 5.0%. It was found out that the larvae of all the obtained species of parasitic Diptera: Tachinidae developed individually both in larvae and pupae of Tortricidae.

Table 3. Parasitoids from the order of Diptera: Tachinidae reared from larvae and pupae of leaf tortricids in the apple orchard without any chemical control (Site 1) in 1999–2001

Species

Reared from

Number
([in specimens)

Total

Term of flight

1999

2000

2001

Individuals
(in specimens)

%

Nemorilla floralis Fall.

larvae

 

2

 

11

13.7

7 VI-24 VI

pupae

 

7

2

Eumea linearicornis Zett.

larvae

20

17

 

59

73.8

2 VI-30 VI

pupae

8

11

3

Pales pavida

larvae

 

2

 

4

5.0

15 VI-17 VI

pupae

 

2

 

Bessa parallela Meig.

larvae

1

 

1

2

2.5

24 VI
and 17 VIII

pupae

 

 

 

Blondelia nigripes Fall.

larvae

2

 

 

3

3.7

17 VI-26 VI

pupae

 

 

1

Actia pilipenis Fall.

larvae

 

1

 

1

1.3

7 VI

pupae

 

 

 

Total

 

31

42

7

80

-

-

The degree of parasitization of larvae and pupae of leaf tortricids in particular years of studies in the orchard without chemical protection is presented in Table 4. The total parasitization of tortricids by Ichneumonidae, Braconidae and Tachinidae during the three years of studies was 16.0%. In particular vegetation seasons it ranged from 7.2% (in 2001) to 26.4% (in 2000).

Table 4. Parasitation of leaf tortricids larvae and pupae in the apple orchard without any chemical treatment in 1999–2001

Year

Number of collected larvae and pupae

Larvae and pupae parasitised by

Total parasitism

Ichneumonidae

Braconidae

Tachinidae

Number
(in specimens)

%

Number
(in specimens)

%

Number
(in specimens)

%

Number
(in specimens)

%

1999

1003

90

9.0

47

4.7

31

3.1

168

16.8

2000

689

94

13.6

46

6.7

42

6.1

182

26.4

2001

906

46

5.1

12

1.3

7

0.8

65

7.2

Total

2598

230

8.8

105

4.0

80

3.1

415

16.0

Parasitoids from the family Ichneumonidae, whose total proportion in parasitization during the three years of studies was 8.8%, limited the population of Tortricidae in the highest degree. Representatives of the family Braconidae and Tachinidae turned out to be less effective and limited the population of tortricids by 4.0% and 3.1%, respectively.

The role of particular groups of parasitoids in parasitization of tortricids changed depending on the year of studies, which is presented in figure 1. In 1999 the proportion of parasitoids from the family Ichneumonidae was twice as high as that from the family Braconidae and almost three times as high as from the family Tachinidae. The year 2000 was also characterized by a big population of ichneumons, while the proportions of representatives of Braconidae and Tachinidae were on similar levels and they were 6.7% and 6.1%, respectively. In 2001 Tachinidae parasitized only 0.8% caterpillars and pupae of the host, and the proportion of Braconidae was only slightly higher and it was 1.3%.

Fig. 1. Parasitation of Tortricidae larvae and pupae by particular parasitoids families in the apple orchard without chemical treatment in 1999–2001

The flights of parasitic Hymenoptera from the family Ichneumonidae were observed mainly in May and June (94.6%). The maximum of their flights took place most frequently during the second 10 days’ period of June (35.6%). In the case of Apophua bipunctoria species relatively numerous flights were also observed in August.

The flights of Hymenoptera from the family of Braconidae also took place mainly in June (97.2%), and their maximum was observed in the second 10-days’ period of that month (52.2%). Cotesia ater, whose individuals were also observed during the first 10 days of August, was characterized by a longer period of flights.

The flights of Diptera from the family Tachinidae were mostly observed in June (tab. 3).

Only single specimens of parasitic Hymenoptera and Diptera were found in the orchard with a limited program of plant protection in Motycz (Site 2). In 1999 only two specimens of Phytodietus segmentator (Hymenoptera: Ichneumonidae) and 1 specimen of Eumea linearicornis (Diptera: Tachinidae) were obtained. The year 2000 was on a similar level to 1999 as far as the populations of the obtained parasitoids are concerned. A rearing of larvae gave 2 species of hymenopterous parasites from the family Ichneumonidae: Phytodietus segmentator (1 specimens) oraz Apophua bipunctoria (1 specimens). Besides, one specimen of Eumea linearicornis (Diptera: Tachinidae) was obtained. In 2001 3 specimens of parasitoids belonging to the order Hymenoptera were obtained. 2 specimens of Apophua bipunctoria were obtained from the family of Ichneumonida, and Macrocentrus linearis Ness (6♀♀ from 1 larva) was obtained from the family of Braconidae.

DISCUSSION

During the rearing of caterpillars and pupae of leaf tortricids numerous parasitic insects belonging to the order Hymenoptera and Diptera were obtained. The majority of parasitoids were obtained in the orchards without any chemical protection, while in the orchards where man’s interference was visible the flights of parasitoids were scarce or they were not observed at all. The order Hymenoptera was represented by the species belonging to two families: Ichneumonidae and Braconidae, which is consistent with the results achieved by Miczulski and Anasiewicz [11] and Miczulski and Koslińska [12]. Zajančkauskas et al. [24] reports that 64 species of Hymenopterous parasitoids can colonize the larvae and pupae of tortricids, whereas Zierowa et al. [25] enumerate as many as 201 species. The authors’ own studies found out the occurrence of 23 species of parasitic Hymenoptera. The family Ichneumonidae, which was the most numerous, included 16 species, while the family Braconidae – 7 species. The order of Diptera was represented by the family of tachina flies (Tachinidae), which included 6 species.

The dominating species was ectoparasitoid Phytodietus segmentator (Hymenoptera: Ichneumonidae), which is a primary parasitoid mainly to caterpillars of Archips rosana (L.) [24]. This species also dominated in Miczulski and Koslińska’s studies [12]. It attacks hairless moths larvae in the final stages of development. This protects the parasitoid from being thrown off during the moulting [9].

Most of the obtained parasitic insects from Hymenoptera order were parasitoids to caterpillars, while the parasitoids attacking Tortricidae pupae included four species: Itoplectis maculator, Itoplectis alternans, Camposcopus canaliculatus and Camposcopus perspicuus belonging to the family of Ichneumonidae. Głowacki [6] and Medvedev [9] report that representatives of the subfamily Anomaloninae, which belongs for example the species of the genera Camposcopus, attack caterpillars, but the development of the parasitoid finishes already in the pupa of the host. An adult ichneumon flies out of the pupa cover biting off the lid in its head part. Hymenoptera from the species Itoplectis alternans and Itoplectis maculator attack the host at the stage of pupa and they develop there forming their own cocoon [1, 9]. On the other hand, Tian and Piekarska-Boniecka [20] found out that those two enumerated species of ichneumons are superparasitoids attacking Hymenoptera from the family of Braconidae or other ichneumons.

Eumea linericornis dominated among the parasitic Diptera: Tachinidae. This is a species attacking different leaf tortricids, especially from the genus Archips [21]. Nemorilla floralis, constituting only 13.7% of the total population of those Diptera, were on the second place in respect of the number. On the other hand, in Miczulski and Koslińska’s studies [12] this is a dominating species among Tachinidae.

Three years of the authors’ own studies showed that total parasitization of leaf tortricids was 16.0%. Piekarska-Boniecka and Wilkaniec [17] gives an almost twice as high degree of parasitization of tortricid larvae, whereas Miczulski and Koslińska [12] claims that it can range from 3.0% to 32.0%, depending on the season and the studied orchard. The highest effectiveness in parasitization was characteristic of parasitoids from the family Ichneumonidae, whose proportion in the course of the three years of studies was 8.8%. The population of parasitoids from the family Braconidae and Tachinidae was smaller, and their proportion in parasitization was 4.0% and 3.1%, respectively. Similar results were obtained by Miczulski and Anasiewicz [11] and Piekarska-Boniecka [14], who stated that the main role in limiting the population of tortricids was played by ichneumons (Ichneumonidae).

CONCLUSIONS

  1. Parasitic entomofauna, which limited the population of leaf tortricids, was found first of all in the orchard without any chemical protection.

  2. The application of chemical treatments of plant protection in apple orchards considerably limited the species composition and the population of parasitoids.

  3. Hymenoptera from the family of ichneumons (Ichneumonidae) limited the populations of caterpillars and pupae the most. Parasitoids from the families of Braconidae and Tachinidae turned out to be less effective.

  4. In all the studied years the dominating species was ectoparasitoid Phytodietus segmentator Grav. (Ichneumonidae).

  5. Most of the obtained parasitic insects from the order Hymenoptera were parasitoids towards caterpillars. Parasitoids attacking the pupae of Tortricidae included four species.

  6. The most numerous among the parasitic Diptera: Tachinidae was Eumea linearicornis Zett.

ACKNOWLEDGMENTS

I would like to express my deep gratitude Professor Bartłomiej Miczulski for help in identification to species, parasitoids belonging to the order of Hymenopter-Parasitica and Doctor Cezary Bystrowski for those belonging to Diptera: Tachinidae.

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Accepted for print: 16.01.2007


Izabela Kot
Department of Entomology,
University of Life Sciences in Lublin, Poland
7 Leszczynskiego Street
20-069 Lublin, Poland
Phone: +48 81 52 48 135, +48 81 52 48 165
email: izabela.kot@up.lublin.pl

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