THE OCCURRENCE OF APHIDS AND THEIR NATURAL ENEMIES ON JUNIPER SHRUBS IN THE AREA OF LUBLIN

Bożenna Jaśkiewicz

ABSTRACT

The subject of the studies conducted in the years 1999-2001 was the occurrence of aphids and their natural enemies on the shrubs of common and Pfitzer juniper. Observations were carried out in the green areas of the city in a street (A) and a park (B) sites. The studies established the presence of one aphid species of Cinara juniperi De Geer. Aphids occurred in the largest numbers on common juniper shrubs in 2001, and on Pfitzer juniper in 2000. It was also observed that on both species of juniper the population of aphids was bigger in site A than in site B.

Key words: Cinara juniperi De Geer, Juniperus communis L., Juniperus × pfitzeriana (L. Späth) P. A. Schmidt, city green areas, natural enemies.

INTRODUCTION

The increasing importance of city green areas in parks, squares and housing estates, which create suitable places for relaxation, is followed by a greater role and application of coniferous shrubs. Together with deciduous plants, lawns and flowerbeds, they form very effective compositions. The richness of their species, varieties and forms as well as their ever greenness make them desirable plants in cities. Coniferous plants have a positive effect on the microclimate, increasing the air humidity and giving off oxygen and medicinal ethereal oils. These plants include for example junipers: Juniperus communis L. and J. × pfitzeriana (L. Späth) P. A. Schmidt (a cross of J. chinensis L. and J. sabina L.).

Worse and worse ecological conditions in city agglomerations make the plants weaker, increasing their susceptibility to pests and disease. The city entomofauna is characterized by a dynamic development of arthropods with a stinging-sucking mouth apparatus [5, 21], among which the aphids make a group of most dangerous pests. The notion “pest” refers in urbanized settings to those species that lower the decorative value of ornamental shrubs, in this case of junipers. Despite the practical and aesthetic values of these plants, there is a lack of studies on the occurrence of aphids throughout the whole vegetation period.

The purpose of the present paper was to establish the species composition, the numbers and dynamics of the aphid population and their natural enemies on the shrubs of common and Pfitzer juniper in street and park sites.

MATERIALS AND METHODS

Observations were performed in the years 1999-2001 in the green areas close to the Rector’s Office of the Agricultural University (area A) and in the Housing estate “Czechów” (area B). Area A can be treated as a street site (heavy traffic), while area B is a park site in the centre of a housing estate (no traffic). Five shrubs of common juniper and five of Pfitzer juniper were chosen in both sites, A and B. Those plants were not submitted to any protective treatments. The presence of aphids and their natural enemies was observed on five shoots (of similar length) of each shrub. The plants were monitored from early spring till late autumn with about 10-days’ intervals. When the weather conditions were unfavourable (rainfalls), the observations were put off onto the following days.

Meteorological data were obtained from the Institute of Agrometeorology of the University of Agriculture in Lublin.

The studies made use of the ecological index – constancy of appearance (C), or – in other words – frequency index (F), which was calculated according to the following formula:

where:
q – number of samples where a given species was observed,
Q – number of all the samples.

Basing on the directions included in the paper by Górny and Grüm [6] and Trojan [18], 4 classes of constancy (frequency) were distinguished:

Class I (euconstants) – 0.76-1 (76-100%),
Class II (constants) – 0.51-0.75 (51-75%),
Class II (accessory species) – 0.26-0.50 (26-50%),
Class IV (accidents) – Ł 0.25 (Ł 25%).

RESULTS

The studies conducted on the shrubs of Juniperus communis L. as well as on J. × pfitzeriana found out the presence of one aphid species – Cinara juniperi (De Geer) from the family Lachnidae, the subfamily of Lachninae. The course of the weather is presented in figure 1. The information concerning the numbers, dates of occurrence of early aphids, the maximum of the population and the disappearance of the colonies as well as the constancy of occurrence on common and Pfitzer juniper is included in tables 1 and 2. The aphid population dynamics on common juniper is shown in figure 2, while in Pfitzer juniper in figure 3. The numbers and periods of occurrence of pests are included in table 3, while the data on the occurrence of primary and secondary parasitoids are in tables 4 and 5.

Due to the delayed period of vegetation in 1999, the first small colonies (of green brown and dark brown, strongly waxed aphids) were found on young juniper shoots in the sites where observations were performed in the third decade of April. The maximum numbers were observed already in the next observation – in the first decade of May (A – 51 aphids/shrubs and B – 39 aphids/shrub). Beginning with the second decade of May the numbers stared to decrease. The reason could have been frequent stormy rains, and after the heat waves between the second decade of June and the middle of July, only singular individuals were found on the shrubs. After the repeated heat in August, subsequent observations did not find any increase of the numbers. The dynamics of the population of this species was analogous in both sites. This aphid is a one-home species; its disappearance in site A took place in the second decade, while in site B in the third decade of October.

After a mild winter of 2000, the first aphids were observed in site A in the first decade of May, while in site B – in the third decade of April. Warm spring and summer with the rains within the norm favoured the development of aphids. Despite that, beginning with September, they occurred with changing intensity. Exceptionally in that period, the maximum of their numbers was found out in October, in site A (5.4 aphids/shrub) in the second decade, and in site B (39.2 aphids/shrub) in the first decade. The number of aphids in site B that year was four times as high as in site A. In 2000 the vegetation was exceptionally long (warm October and November). In site A aphids disappeared in the first 10 days of December, and in site B already in the second decade of November.

After a mild winter and early spring of 2001, the first single individuals appeared already in April, in site A – in the first decade, and in site B – in the second decade. That year the number of aphids in site A was the highest as compared with the former years of studies. Beginning with the third decade of April, the studies observed a rapid increase of the number of aphids, which reached the maximum in the first 10 days of May (A – 60 aphids/shrub, B – 29 aphids/shrub). The subsequent observations found out a slow decrease of their population. Only single individuals were observed till September. In area A the aphids disappeared in the first decade, while in area B – in the second decade of November.

Totally, during the three years of studies, 404.6 wingless individuals/shrub and 4.2 winged ones/shrub were observed in site A, while 336.2 wingless individuals/shrub and 4.8 winged ones/shrub were found in site B.

Constancy (frequency) of aphid appearance. Considering the constancy of occurrence, in 1999 and 2000 this species belonged to I frequency class – euconstant, while in 2001 it was included in II frequency class – constant (tab. 2).

Symptoms of injuries. Cinara juniperi is a one-home species, hence, it was present throughout all period of vegetation, always in small colonies consisting of no more than several individuals. As a result of those insects feeding on the shrubs, the needles got discoloured and brown, and even the branches started to wither. Worse decorative character of those plants could have resulted from the numerous occurrences of scale insects from the species of Carulaspis juniperi (Bouché), which also fed on the twigs. This fact made it more difficult to determine the real damage done by Cinara juniperi.

In 1999 no such aphid was found in either of the examined sites.

In 2000 this species occurred in site A only scarcely (8.8 aphids/shrub) and only between the second decade of October and the third decade of November. In that period the aphids laying eggs were observed. Only 3 individuals were found in area B (in the first decade – 1 aphid, and in the second decade – 2 aphids).

In 2001 that aphid was found only in site A during two observations in the second and third decades of April. Further observations in both areas did not reveal any aphids. During the three years of studies 12 wingless individuals/shrub were noted in site A, and 0.6 wingless individual/shrub in site B.

Constancy of occurrence (frequency) of aphids. A short period of that aphid’s occurrence on J. × pfitzeriana was the factor that decided that on that plant it belonged to IV frequency class – accident (tab. 2).

Symptoms of injuries. Aphids stayed on the studied shrubs for a very short time and in small numbers; hence, probably they had no effect on lowering the decorative character of the plants.

The aphid colonies on Juniperus communis shrubs included the following predators: young and adult individuals of Araneida; larvae and adults of Dermaptera; larvae and adults of Coccinellidae; eggs and larvae of Chrysopidae and Syrphidae. Among them, the most important were probably Chrysopidae, whose numerous eggs were observed on the examined plants, and ladybirds from the subfamily of Coccinellinae from the genus of Chilocorus (Leach) – Chilocorus bipostulatus (L.) (Photo 5). Characteristic larvae of this ladybird were frequently observed on juniper twigs. In 2000 the total number of all the predators was the highest in comparison with the years 1999 and 2001 (tab. 3).

Cinara juniperi occurred on the shrubs Juniperus × pfitzeriana very scarcely and no aphidophagous species were observed in its colonies.

The three-year-long observations on Juniperus communis found out the presence of parasitized aphids. Totally, 173 mummies were found: 35 individuals in 1999, 80 individuals in 2000, and 58 individuals in 2001 (tab. 4). Some of them were empty mummies, from which parasitic Hymanoptera had flown away, while the others were taken for culture. Their occurrence was observed between April and November, most frequently in May and June. There were more aphid mummies and parasitoids obtained from the culture in site A (103 individuals) as compared to site B (70 individuals). It was found out that aphid parasitisation on the shrubs of J. communis ranged in the years of studies from 3.35% (site B) to 4.35% (site A). The culture of parasitised aphids gave adult individuals of Hymenoptera (34 individuals), which were included in primary and secondary parasitoids (tab. 5). Primary parasitoids belonged exclusively to the family of Aphidiidae from the subfamily of Aphidiinae. The following were defined as hyperparasoids: Hymenoptera from the family Cynipidae from the subfamily Charpinae – Charpis victix Westwood (Photo 7), from the family Pteromalidae of the subfamily Pteromalinae – Coruna clavata Walker (Photo 8) and subfamily Asaphinae – Asaphes vulgaris Walker from the family Encyrtidae from the subfamily Encyrtinae – Leptomastidae bifasciata Mayr (Photo 9) as well as from the family Megaspilidae of the subfamily Megaspilinae – Dendroceus carpentieri Curtis (Photos 10, 11). The culture gave 11 individuals of primary parasitic Hymenoptera from the species Aphidius ervi Haliday, which constituted about 32% of all the obtained parasitoids (Photo 6). Hyperparasitoids, which limited the numbers of A. ervi, constituted 68% of all the obtained Hymenoptera. The highest numbers were characteristic of the species A. vulgaris (11 individuals) and Coruna clavata (6 individuals). The number of the other three species ranged from 1 to 4 individuals.

DISCUSSION

Analyzing the three years of studies it was found out that the shrubs of common juniper and Pfitzer juniper are the host plants for one species of aphids – C. juniperi. This is a one-home aphid, found on those plants by other authors [12, 13, 15, 16, 17]. The population dynamics (the whole season of vegetation) of this aphid on common juniper was earlier studied by Jaśkiewicz [7, 8, 9]. Szelęgiewicz [17] states the presence of Cinara mordvilkoi on common juniper. This aphid rarely occurs in Poland and but only in the Carpathian area. Many years of studies in the area of Lublin did not confirm its presence.

C. juniperi occurred on the twigs of common juniper from early spring till the end of November, with changing intensity. The values of its maximum occurrence, which inform about the date of the greatest threat for the plants, were within the range of 5.4 and 60.0 aphids/shrub. Annually, but with an exception of 2000, this aphid occurred in greater numbers in area A (street site). Cichocka and Goszczyński in Warsaw [5] and Wilkaniec in Poznań [21] compare the populations of aphids in parks and street sites, finding out more numerous populations in the latter.

Single individuals of C. juniperi were observed on Pfitzer juniper in areas A and B in 2000, while in 2001 only in area A. The numbers ranged from 0.6 to 8.8 aphids/shrub. The occurrence of C. juniperi on those shrubs could have been related to the neighbourhood of common juniper in the studied sites.

Weather conditions in a given year had an effect on the population, dates of occurrence, the maximum and disappearance of aphids and laying eggs. One of the important factors is the date of vegetation and temperatures in the spring period. With an early spring, the first aphids were observed on the examined plants as early as in April (especially in 2001). During the studies, high temperatures of 30°C to 35°C occurred frequently, and they caused decrease of the aphid population. The population of aphids also decreased due to the rainfalls, especially in 1999. Warm and long autumn favoured the laying of eggs. Ground frosts destroyed the oviparous females and freshly laid eggs. The effect of the weather on the development of aphids is confirmed in the studies by other authors [3, 4, 5, 10, 11, 22].

The aphid population in the vegetation season is also influenced by natural enemies [1, 2, 3, 14]. The greatest influence in limiting the aphid population on the shrubs of common juniper could have been exerted by Chrysopidae, whose numerous eggs were already observed in May, as well as ladybirds from the genus Chilocorus (Ch. bipostulas L.). Larvae of this ladybird were observed on juniper twigs in spring (single individuals), and in greater numbers in July and August. Individual larvae of Syrphidae occurring in June and October did not have any significant effect on the reduction of aphid population. The appearance and activity of aphid-eaters were related to the weather; they occurred in greater numbers in warm spring with little rain [23]. When the temperature drops to 12°C, ladybirds do not feed [10], and these data were partly confirmed by results of the present studies. In 2000 the total number of predators was higher as compared to the years 1999 and 200 1. It was also established that parasitoids had an effect on the reduction of aphid population. Aphid parasitisation in the years of studies on J. communis ranged between 3.35% (site B) and 4.35% (site A). The culture gave 11 individuals of primary parasitoids from the species of Aphidus ervi Haliday, which constituted 32% of all the obtained parasitoids. The effect of parasitoids on the population of C. juniperi was shown in the studies by Werstak and Wiąckowski [19] as well as Wiąckowski et al. [20].

C. juniperi aphids occurred on the shrubs of J. × pfitzeriana only for a short time and in small numbers. No aphidophagous species were observed.

C. juniperi most frequently fed on one-year-old, more rarely two-year-old, juniper shoots between the needles. They occurred individually or in small colonies. The following were the results of the juices sucked out of the plants: inhibition of the shoot growth, little growth, discoloration, twisting, browning and even drying of the needles. The injuries caused by those aphids clearly lowered the ornamental value of juniper shrubs. The data from the present studies confirmed earlier observations by Jaśkiewicz [7, 8, 9] in the areas of parks and housing estates in Lublin. On the other hand, the results from the years 1999-2001 showed a longer period of this aphid’s occurrence and they were different as to the numbers. Aphids were observed from April, sometimes till November, and the population was higher depending on the year.

CONCLUSIONS

1. The shrubs of Juniperus communis L. and Juniperus × pfitzeriana (L. Späth) P. A. Schmidt were inhabited only by one aphid species, namely Cinara juniperi (De Geer).

2. The studies found out a greater population of aphids (on both juniper species) in the street site (A) as compared to the park site (B).

3. After a mild winter and a warm spring with the rainfalls within the norm the aphids occurred in greater numbers (in 2000 and 2001), while a negative effect on the dynamics of their population was exerted by a delayed period of vegetation, high temperatures (over 30°C) and heavy rainfalls (in 1999).

4. The population of aphids on J. communis was not much affected by the presence of predators and parasitoids. No aphidophagous species were found on the shrubs of J. × pfitzeriana.

5. The injuries caused by C. juniperi clearly lowered the ornamental value of common juniper shrubs.

1. Barczak T., 1988. Owady – naturalni wrogowie mszycy trzmielinowo-burakowej A. fabae Scop. (Homoptera, Aphididae). [Insects – natural enemies of A. fabae Scop. Homeoptera Aphididae]. Wiad. Entomol. 8, 1, 13-26 [in Polish].

2. Barczak T., 1994. Naturalni wrogowie mszyc i ich znaczenie w ochronie roślin [Natural enemies of aphids and their importance in plant protection]. Wiad. Entomol. 13, 3, 141-152 [in Polish].

3. Cichocka E., 1980. Mszyce roślin sadowniczych Polski [Aphids of Polish orchards]. PWN, Warszawa, 119 pp. [in Polish].

4. Cichocka E., 1995. Przyczyny masowego wystąpienia mszyc w sadach w 1994 r. [Causes of massive occurrence of aphids in orchards in 1994]. Sad Nowoczesny 3, 4-6 [in Polish].

5. Cichocka E., Goszczyński W., 1991. Mszyce zasiedlające drzewa przyuliczne w Warszawie. W: Mszyce ich bionomia, szkodliwość i wrogowie naturalni [Aphids inhabiting street trees in Warsaw. In: Aphids and their bionomy, harmfulness and natural enemies]. (red. Cichocka E., Goszczyński W.), PAN, Warszawa, 9-18 [in Polish].

6. Górny M., Grüm L., 1981. Metody stosowane w zoologii gleby [Methods used in soil zoology]. PWN, Warszawa, 483 pp. [in Polish].

7. Jaśkiewicz B., 2000a. Cinara juniperi De Geer occurring on common juniperi. Aphids and Other Homopterous Insects 7, PAS, Olsztyn, 75-82.

8. Jaśkiewicz B., 2000b. Aphids colonising the shrubs of Juniperus communis L. and Rosa canina L. in urban conditions. Electronic Journal of Polish Agricultural Universities, Series Horticulture, Volume 3, Issue 2 http://www.ejpau.media.pl/series/volume3/issue2/horticulture/art-02.html

9. Jaśkiewicz B., Bartoszek A., 2001. Obserwacje nad występowaniem Cinara juniperi De Geer na krzewach Juniperus communis L. w Lublinie [Observations on the occurrence of Cinara juniperi De Geer on the shrubs of Juniperus communis L. in Lublin]. Progress in Plant Protection 41, 2, 665-670 [in Polish].

10. Jurek M., 1980. Wpływ czynników siedliska na liczebność mszyc na jabłoniach [The effect of habitat factors on the aphid population on apple treest]. Ochrona Roślin 12, 13-16 [in Polish].

11. Leszczyński B., 1990. Wpływ czynników klimatycznych na populację mszyc zbożowych [The effect of climatic conditions on the population of cereal aphids]. Zesz. Probl. Post. Nauk Roln. 392, 121-131 [in Polish].

12. Łabanowski G., Orlikowski L., 1997. Ochrona roślin iglastych i wrzosowatych [Protection of coniferous and heather plants]. Plantpress Sp. z. o. o., Kraków, 256 pp. [in Polish].

13. Müller F. P., 1976. Mszyce – szkodniki roślin. Terenowy klucz do oznaczania [Aphids – plant pests. A field key for marking]. PWN, 118 pp. [in Polish].

14. Olszak R. W., 1991. Ocena skuteczności zespołu afidofagów występujących w sadach jabłoniowych. W: Mszyce – ich bionomia, szkodliwość i wrogowie naturalni [Estimation of the effect of a community of aphidophagous species occurring in apple tress orchards. In: Aphids – their bionomy, harmfulness and natural enemies]. (red. Cichocka, Goszczyński), PAN, Warszawa, 107-113 [in Polish].

15. Soika G., Łabanowski G., 2001. Aphids belonging to Cinara Curtis (Aphidodea, Lachnidae) – the pest of ornamental conifers in Poland. Aphids and Other Homopterous Insects 8, PAS, Siedlce, 175-184.

16. Szelęgiewicz H., 1968. Mszyce – Aphidoidea. Katalog fauny Polski [Aphids – Aphidoidea. A catalogue of the Polish fauna]. XXI, 4, 316, PWN, Warszawa [in Polish].

17. Szelęgiewicz H., 1978. Klucze do oznaczania owadów Polski, cz. XVII Pluskwiaki równoskrzydłe – Homoptera, zeszyt 5a Mszyce – Aphidodea [Keys for marking insects in Poland, p. XVII. Homoptera, no. 5a Aphids – Aphidodea]. PWN, Warszawa, 107 pp. [in Polish].

18. Trojan P., 1977. Ekologia ogólna [General ecology]. PWN, Warszawa, 418 pp. [in Polish].

19. Werstak K., Wiąckowski S., 1998. Mszycarzowate (Hymenoptera, Aphidiidae] w aglomeracjach miejskich województwa kieleckiego. W: Fauna miast [Hymenoptera, Aphididae in urban agglomerations of the Kielce district. In: Urban fauna], (red. T. Barczak., P. Indykiewicz), Wyd. ATR, Bydgoszcz, 73-82 [in Polish].

20. Wiąckowski S. K., Wiąckowska J., Werstak K., Ślusarczyk J., 2001. Parazytoidy mszyc (Hymenoptera, Aphidiidae) Polski centralnej i południowej [Aphid parasitoides (Hymenoptera, Aphididae) of central and southern Poland]. Wiad. Entomol. 20 (1/2), 57-65 [in Polish].

21. Wilkaniec B., 1994. Afidofauna of selected tree species in the urban area of Poznań. Aphids and Other Homopterous Insects 4, PAS, Skierniewice, 71-79.

22. Wójtowska M., 1990. Wpływ różnych czynników na liczebność mszycy grochowianki na różnych roślinach motylkowych [The effectof various factors on the population of pea aphid on different papilionaceous plants]. Zesz. Probl. Post. Nauk Rol. 392, 161-169 [in Polish].

23. Ziarkiewicz T., Kozłowska A., 1973. Materiały do poznania składu gatunkowego drapieżnych bzygowatych (Syrphidae, Diptera) występujących w koloniach mszyc na krzewach ozdobnych [Materials for the species composition of Syrphidae, Diptera occurring in aphid colonies on decorative shrubs]. Pol. Pismo Entomol. 43, 3, 621-626 [in Polish].

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