Startseite Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
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Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey

  • Şükran Oğuzoğlu ORCID logo , Mustafa Avcı ORCID logo und Kahraman İpekdal ORCID logo EMAIL logo
Veröffentlicht/Copyright: 1. Juli 2021
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 16 Heft 1

Abstract

Marchalina hellenica is a sap sucking scale insect endemic to the Aegean basin and it has been introduced to several regions in Greece and Turkey to increase pine honey production. It is also considered as a pest since heavy infestation may leave the host trees vulnerable to secondary pests. An understanding of its natural predators would facilitate planning biocontrol programs. Although there are several studies reporting the predators of M. hellenica in its native range, there is no study identifying those in its introduced range. We aimed to determine predators of M. hellenica in Burdur, one of its introduced sites in Turkey. We carried out sampling through regular visits in an M. hellenica-infested locality nearby Burdur Lake. Through field and laboratory observations, we identified 19 species predating upon M. hellenica. Comparing predators reported in previous studies in its native range and those we found in the present study showed that 12 of the species that we found are new reports for the species predating upon M. hellenica. The highest number of predator individuals belonged to the monophagous Neoleucopis kartliana. Myrrha octodecimguttata, Chilocorus bipustulatus and Harmonia quadripunctata were also the most frequently observed predators.

Keywords: honeydew producer; Brutian pine; biological control; natural enemy; prey shift

1 Introduction

The giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), is an economically important species for two contrasting reasons. First, it is the most significant of several honeydew-producing insects in Greece and Turkey; pine honey production relies mainly on M. hellenica honeydew in both the countries [1,2]. For this reason, it has been intentionally introduced at many natural pine forests in these countries and its population has increased locally [3,4,5]. Second, it is a pine pest as it feeds on pine sap and can cause increment loss, desiccation, branch dieback, increasing crown transparency and tree decline [5,6,7,8,9]. Furthermore, Petrakis et al. [9] showed that the giant pine scale can cause decrease in diversity of pine-forest-related insects. Therefore, its population size must be in a balance to provide the highest possible honey yield and the lowest possible damage to the pine ecosystem. However, this is not always possible due to climate warming and human-mediated introduction of the species, and it can turn to be a pest which may necessitate control measures to be taken. Being endemic to Greece and Western Turkey, M. hellenica has been introduced to the Italian island of Ischia and Australia, where it is accepted as a dangerous exotic species [10,11]. It has also been reported in Armenia, Georgia and Krasnodar and Sochi in Russia [12,13], although taxonomic status of the Caucasian population is controversial [14].

Predators and parasitoids play a significant role in suppressing the population size of forest pest insects [15]. Exotic species usually benefit from the enemy-free advantage of the new ecosystems during the early stages of the invasion [16]. This advantage can subside as the host-specific parasitoids and predators follow the invader or the generalist parasitoids and predators start to feed on the invader. Generalist parasitoids and predators can use “host/prey switching” strategy; thus, they can forage on the most abundant prey, the invader in the case of an invasion, in a habitat (e.g., ref. [17]).

The giant pine scale occurs almost in the entire western coasts of Turkey [4,18,19]. It has also been introduced into several regions in the country by beekeepers (Figure A1). Burdur basin, where the present study was undertaken, is one of those regions. Although the first report of M. hellenica in the region was in 2004 [20], the local beekeepers introduced the giant pine scale-infested branches into the region in the early 1990s from Muğla province ca. 200 km west of the study site (M. Bilgiç/Burdur Association of Beekeepers, personal communication). The species has been well established in this isolated basin during the last 30 years. However, it has not been investigated which predatory species prey upon M. hellenica during this period in its recent range. This information may be important for biological control against M. hellenica. Studies on the predators of the giant pine scale revealed 28 predaceous species (two of which being ectoparasitic) so far in Georgia, Greece and Turkey ([13,14,19] Süreyya and Hovasse 1931 cited in ref. [21,22,23,24]) with 3, 7 and 22 species, respectively (Table A1). Although the striking difference in the number of described predatory species among the three countries could be related to the number of studies conducted in each country, the natural history of M. hellenica or a combination of these factors, it is not in our scope to resolve this issue. However, our preliminary observations suggested that the list of predacious species from Turkey seems to be even longer. Accordingly, we asked the following questions in the present study: (1) What are the arthropod predator species in Burdur basin where M. hellenica has been an introduced species? (2) How different is the predator composition in the introduced range of M. hellenica from those in its natural range?

2 Materials and methods

The study area, Burdur Urban Forest (Southwestern Turkey), is located at an average altitude of 910 m (a.s.l., ±30 m; 37°41′30″N, 30°11′54″E) and at the northwestern aspect facing the lake (Figure 1). It is an isolated area of ca. 100 ha, consisting of mainly Pinus brutia, but also of P. nigra and P. pinea. Approximately 300 beehives have been placed in the area for pine honey production. Giant pine scale introductions were carried out intensely in the early 1990s in the region. The Brutian pine in the area was heavily infested not only by M. hellenica but also by bark beetles (mainly Mediterranean pine beetle, Orthotomicus erosus and pine shoot beetle, Tomicus destruens).

Figure 1 Study site. Dashed circle depicts the approximate natural distribution of Marchalina hellenica (a), Burdur Lake (b) and the study site near the lake (c), beehives in Pinus brutia stand in the study site (d) and M. hellenica adults on the stem bark (e).
Figure 1

Study site. Dashed circle depicts the approximate natural distribution of Marchalina hellenica (a), Burdur Lake (b) and the study site near the lake (c), beehives in Pinus brutia stand in the study site (d) and M. hellenica adults on the stem bark (e).

We identified one site of heavy infestation around Burdur Lake in Burdur basin through visual inspection and visited this site (ca. 5 ha, 37°42′0.81″N–30°12′52.32″E; 37°41′49.78″N–30°12′27.65″E; 37°41′36.83″N–30°11′52.99″E; 37°41′26.94″N–30°11′44.08″E; 37°41′26.22″N–30°11′29.60″E) once in October 2017, 13 times between April and October 2018 and 5 times between March and May 2019 (a total of 19 visits). We always conducted the field visits between 11:00 am and 02:00 pm and during this period, we visited 30 trees which we randomly selected in each visit. We collected adult insects from the infested branches by using an entomological beating sheet and a mouth aspirator. We took advantage of the trap-logs placed in the stand in 2019 by the local department of forestry as a part of the management practices applied against O. erosus. We recorded and collected the insects preying on M. hellenica on the trap-logs. During the field observations, we also found pupae on the cottony secretions of M. hellenica. In order to identify them, we reared these pupae in plastic cages (680 mm × 465 mm × 360 mm, 80 lt) with a ventilated lid in the laboratory and recorded the adult emergences. Then we offered M. hellenica nymphs and adults to the adults emerging from the pupae collected from the field to observe predation in the laboratory. Although this was not a setting designed for a choice experiment, it provided us a chance to evaluate possible predation by the species whose immature stages were found in M. hellenica-related structures. Finally, we evaluated the collected species according to the relevant literature, and we discarded those which have not been shown to feed on Coccoidea. Thus, we provided evidence for predation through direct observation in the field and the laboratory, and literature records.

The criteria we used to determine predation on M. hellenica were as follows: (1) If the potential predator was seen feeding directly on M. hellenica (but not on its honeydew) in the field, then we identified the species as a predator. If not, we did not collect it. (2) If it was seen feeding directly on M. hellenica in the laboratory, then we identified it as a predator. If not, we discarded it. (3) If the predation could not be detected through field and laboratory observations but was previously reported in the literature, then we identified the considered species as a predator.

Taxonomical identification of the specimens confirmed by specialists is acknowledged at the end of the article. Specimens were stored at the Entomological Museum of Isparta University of Applied Sciences, Faculty of Forestry.

3 Results

We found 29 insect species during the study, but we eliminated ten species that do not normally prey on scale insects including the giant pine scale. As a result of field and laboratory observations, we identified 19 species (295 individuals) as predators of M. hellenica. Among them, one belonged to Acari, ten to Coleoptera, one to Diptera, five to Hemiptera and two to Neuroptera (Table 1, Figure 2). Detailed descriptions of the identified species are given below. Among all the predator species, the one with the highest number of individuals, both in the field and laboratory observations, was Neoleucopis kartliana (116 individuals), which was followed by Myrrha octodecimguttata (29), Chilocorus bipustulatus (26), Anthocoris nemorum (24) and Temnostethus reduvinus (21) (Table 1). The most frequently detected species was M. octodecimguttata which was recorded as 68.4% of all field visits. Other frequently detected species were C. bipustulatus (57.9%), Harmonia quadripunctata (47.4%), A. nemorum (42.1%) and T. reduvinus (42.1%) (Table 1). The highest number of predator species (7) was recorded on 22 April 2018 and 9 September 2018; whereas the highest number of predator individuals (55) was recorded on 18 March 2019, which was followed by the record on 12 April 2019 (36) and 12 May 2019 (32) (Figure 3). The lowest number of predator species (1) was recorded on 6 April 2018, 27 April 2019 and 19 May 2019; whereas the lowest number of predator individuals (1) was recorded on 6 April 2018 and 19 May 2019 (Figure 3).

Table 1

Predators of Marchalina hellenica found in Burdur, Turkey

No Order Family Species Number of individuals Individual detection rate (%)* Species detection rate (%)**
1 Acari Anystidae Anystis baccarum ‡ 5 1.7 5.3
2 Diptera Chamaemyiidae Neoleucopis kartliana 116 39.3 21.1
3 Coleoptera Coccinellidae Chilocorus bipustulatus ‡ 26 8.8 57.9
4 Harmonia quadripunctata 16 5.4 47.4
5 Myrrha octodecimguttata ‡ 29 9.8 68.4
6 Nephus quadrimaculatus +‡ 5 1.7 21.1
7 Novius cruentatus +‡ 16 5.4 36.8
8 Rodolia cardinalis ‡ 1 0.3 5.3
9 Scymnus pallipediformis +‡ 1 0.3 5.3
10 Scymnus subvillosus 2 0.7 5.3
11 Scymnus syriacus +‡ 1 0.3 5.3
12 Stethorus gilvifrons +‡ 9 3.1 15.8
13 Hemiptera Anthocoridae Anthocoris nemoralis +‡ 1 0.3 5.3
14 Anthocoris nemorum +‡ 24 8.1 42.1
15 Orius majusculus +‡ 1 0.3 5.3
16 Temnostethus reduvinus +‡ 21 7.1 42.1
17 Reduviidae Nagusta goedelii +‡ 1 0.3 5.3
18 Neuroptera Chrysopidae Chrysoperla carnea +‡ 1 0.3 5.3
19 Raphidioptera Raphidiidae Raphidia ambigua + 19 6.4 5.3

*Percentage of detection of the individuals among all other species.

**Percentage of detection of the species in all field visits.

+New record as a predator of M. hellenica.

‡New record for Burdur region.

Figure 2 Predators of Marchalina hellenica identified in Burdur, Turkey: (a) Anystis baccarum, (b) Neoleucopis kartliana, (c) Chilocorus bipustulatus [88], (d) Harmonia quadripunctata, (e) Myrrha octodecimguttata, (f) Nephus quadrimaculatus, (g) Novius cruentatus, (h) Rodolia cardinalis, (i) Scymnus pallipediformis, (j) S. subvillosus, (k) S. syriacus, (l) Stethorus gilvifrons, (m) Anthocoris nemoralis, (n) A. nemorum, (o) Temnostethus reduvinus, (p) Orius majusculus, (q) Nagusta goedelii, (r) Chrysoperla carnea and (s) Raphidia ambigua.
Figure 2

Predators of Marchalina hellenica identified in Burdur, Turkey: (a) Anystis baccarum, (b) Neoleucopis kartliana, (c) Chilocorus bipustulatus [88], (d) Harmonia quadripunctata, (e) Myrrha octodecimguttata, (f) Nephus quadrimaculatus, (g) Novius cruentatus, (h) Rodolia cardinalis, (i) Scymnus pallipediformis, (j) S. subvillosus, (k) S. syriacus, (l) Stethorus gilvifrons, (m) Anthocoris nemoralis, (n) A. nemorum, (o) Temnostethus reduvinus, (p) Orius majusculus, (q) Nagusta goedelii, (r) Chrysoperla carnea and (s) Raphidia ambigua.

Figure 3 (a) Number of predator individuals per species per field visit. (b) Seasonal development of M. hellenica in the region (A: Adult, E: Egg and N: Nymph).
Figure 3

(a) Number of predator individuals per species per field visit. (b) Seasonal development of M. hellenica in the region (A: Adult, E: Egg and N: Nymph).

ACARI: ANYSTIDAE

Anystis baccarum (Linnaeus 1758)

Material examined: 12.05.2019 (5 individuals)

Polyphagous predator is known to feed on M. hellenica [19]. In Turkey, it occurs in Denizli and Manisa [25], İzmir [26] and Muğla [19]. This is the first report from Burdur.

COLOPTERA: COCCINELLIDAE

Chilocorus bipustulatus (Linnaeus 1758)

Material examined: 15.10.2017 (1), 01.05.2018 (3), 24.06.2018 (1), 28.07.2018 (1), 19.08.2018 (7), 09.09.2018 (4), 27.09.2018 (2), 20.10.2018 (3), 18.03,2019 (2) and 12.05.2019 (2) (26 individuals)

It is known to feed on Coccoidea species [27,28]. In Turkey, it occurs in Aydın, Artvin Denizli, İzmir, Muğla [28], Kahramanmaraş [29], Ankara [30], Antalya [31,32] and Çanakkale [33]. This is the first report from Burdur.

Harmonia quadripunctata (Pontoppidan 1763)

Material examined: 22.04.2018 (2), 01.05.2018 (3), 02.06.2018 (1), 24.06.2018 (1), 29.06.2018 (2), 14.07.2018 (1), 09.09.2018 (1), 27.09.2018 (1) and 20.10.2018 (4) (16 individuals)

It is known to feed on Torosaspis cedricola (Balachowsky & Alkan) [34] and M. hellenica [24]. In Turkey, it occurs in Adana, Ankara, Afyonkarahisar, Bursa, Denizli, Isparta, [28], Kahramanmaraş [29], Artvin [35], Antalya [31,32], Çanakkale [33], Bartın [36] and Burdur [37].

Myrrha ( Myrrha ) octodecimguttata (Linnaeus 1758)

Material examined: 15.10.2017 (1), 06.04.2018 (1), 22.04.2018 (2), 01.05.2018 (2), 02.06.2018 (2), 14.06.2018 (2), 24.06.2018 (4), 29.06.2018 (8), 28.07.2018 (1), 19.08.2018 (2), 09.09.2018 (1), 27.09.2018 (1) and 20.10.2018 (2) (29 individuals)

It is known to feed on M. hellenica [19], Matsucoccus pini (Green) (Hemiptera: Matsucoccidae) [38], Carulaspis juniperi (Bouché 1851) and Leucaspis lowi Colvée 1882 (Hemiptera: Diaspididae) [39]. In Turkey, it occurs in Adana, Ankara, Afyonkarahisar, Bursa, Denizli, Isparta, Rize, [28], Kahramanmaraş [29], Balıkesir, Çanakkale, İzmir and Muğla [19]. This is the first report from Burdur.

Nephus (Nephus) quadrimaculatus (Herbst 1783)

Material examined: 22.04.2018 (1), 01.05.2018 (1), 20.10.2018 (2) and 12.05.2019 (1) (5 individuals)

It is known to feed on Palaeococcus fuscipennis (Hemiptera: Monophlebidae) (Burmeister 1835) [40] and Coccus pseudomagnoliarum (Kuwana 1914) [41,47,84]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Antalya [32] and Diyarbakır [42]. This is the first report from Burdur.

Novius cruentatus (Mulsant 1850)

Material examined: 15.10.2017 (3), 22.04.2018 (2), 02.06.2018 (1), 29.06.2018 (7), 27.09.2018 (1), 18.03.2019 (1) and 12.04.2019 (1) (16 individuals)

It is known to feed on Palaeococcus fuscipennis [43]. This is the first report showing that it predates upon M. hellenica. Löbl and Smetana [83] reported the species in Turkey without any locality detail. This is the first report from Burdur.

Rodolia cardinalis (Mulsant 1850)

Material examined: 24.06.2018 (1 individual)

It is known to feed on M. hellenica [19,78] and P. fuscipennis [40,43]. In Turkey, it occurs in Mediterranean region [28], Aydın, İzmir, Muğla [19] and Antalya [32]. This is the first report from Burdur.

Scymnus pallipediformis Günther 1958

Material examined: 01.05.2018 (1 individual)

It is a polyphagous species feeding on aphids and scale insects [29,42,51]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Mediterranean region [28], Adıyaman, Diyarbakır, Şanlıurfa [42], Ağrı [44], Antalya [31,32], Çanakkale [33], Kahramanmaraş [29], İzmir [45] and Yalova [46]. This is the first report from Burdur.

Scymnus ( Pullus ) subvillosus (Goeze 1777)

Material examined: 15.10.2018 (1) and 22.04.2018 (1) (2 individuals)

It is a polyphagous species feeding on aphids and scale insects [29,42,51]. It is known to feed on M. hellenica [19], Coccus pseudomagnoliarum [47] and Planococcus citri (Risso) (Hemiptera: Pseudococcidae) [48]. In Turkey, it occurs in Adıyaman, Diyarbakır [42], Antalya [32], Aydın, Balıkesir, İzmir, Muğla [19], Burdur [49], Çanakkale [33], Kahramanmaraş [29] and Yalova [46].

Scymnus syriacus (Marsuel 1868)

Material examined: 29.06.2018 (1 individual)

It is known to feed on Aphididae [42,50], Cicadellidae, Coccidae, Diaspididae and Psyllidae [51,52]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Adana, Hatay, Mersin [28], Adıyaman, Şanlıurfa [51], Antalya [32], Diyarbakır [42] and Kahramanmaraş [29]. This is the first report from Burdur.

Stethorus gilvifrons (Mulsant 1850)

Material examined: 15.10.2017 (2), 09.09.2018 (1) and 20.10.2018 (6) (9 individuals)

It is known to feed on aphids and scale insects [29,31,51] and Tetranychidae [28]. Anapulvinaria pistaciae (Bodenheimer 1926), Eulecanium rugulosum (Arch. 1937; Coccidae), Pistaciaspis pistaciae Arch. and Suturaspis pistaciae (Lindinger 1906) (Diaspididae) are reported to be its prey species [51]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Mediterranean region and Adıyaman, Diyarbakır, Şanlıurfa [42], Antalya [31,32], Çanakkale [33], Isparta [53], İzmir [28] and Kahramanmaraş [29]. This is the first report from Burdur.

DIPTERA: CHAMAEMYIIDAE

Neoleucopis kartliana (Tanasijtshuk 1986)

Material examined: 18.03.2019 (52), 12.04.2019 (28), 27.04.2019 (23) and 12.05.2019 (13) (116 individuals). It feeds only on Marchalina [19,54]. In Turkey, it occurs in Antalya, Aydın, Balıkesir, Burdur, Bursa, Çanakkale, Denizli, Edirne, İstanbul, İzmir, Manisa and Muğla [19].

HEMIPTERA: ANTHOCORIDAE

Anthocoris nemoralis (Fabricius 1794)

Material examined: 12.04.2019 (1 individual)

It is a polyphagous species feeding on aphids, mites, psyllids and lepidopteran eggs and young larva [55,56,57]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Antalya, Erzincan, Erzurum, İzmir, Manisa and Mersin [58,59]. This is the first report from Burdur.

Anthocoris nemorum (Linnaeus 1761)

Material examined: 22.04.2017 (1), 14.06.2018 (1), 24.06.2018 (2), 14.07.2018 (2), 09.09.2018 (1), 12.04.2019 (6), 12.05.2019 (10) and 19.05.2019 (1) (24 individuals)

It is a polyphagous species reported to feed on Cacopsylla pyri (L.) (Hemiptera: Psyllidae) and Brevicoryne brassicae (L.) (Hemiptera: Aphididae) [56,85,86]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Antalya and Erzurum [59], Artvin, Bolu and Trabzon [60]. This is the first report from Burdur.

Orius ( Heterorius ) majusculus (Reuter 1879)

Material examined: 09.09.2018 (1 individual)

It is a polyphagous species [61] reported to feed on aphids, thrips and whiteflies [62,63,64]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Eastern Black Sea and Eastern and Central Anatolia regions [60]. This is the first report from Burdur.

Temnostethus ( Ectemnus ) reduvinus (Herrich-Schäffer 1850)

Material examined: 24.06.2018 (3), 29.06.2018 (2), 14.07.2018 (6), 28.07.2018 (1), 19.08.2018 (1), 09.09.2018 (5), 27.09.2018 (2) and 20.10.2018 (1) (21 individuals)

It is known to feed on Lepidosaphes ulmi (L.) (Diaspididae) and Agonoscena pistaciae Burck. & Laut. (Psyllidae) [65,66,67]. This is the first report showing that it predates upon M. hellenica. In Turkey, it occurs in Adıyaman, Siirt [67], Antalya, Artvin, Erzincan, Erzurum and Kars [59]. This is the first report from Burdur.

HEMIPTERA: REDUVIIDAE

Nagusta goedelii (Kolenati 1857)

Material examined: 27.09.2018 (1 individual)

It is a polyphagous species reported to feed on aphids, psyllids and pseudococcids [32,68,69,70]. This is the first report showing that it predates upon M. hellenica. In Turkey, it has a wide distribution [71,72,73]. This is the first report from Burdur.

NEUROPTERA: CHRYSOPIDAE

Chrysoperla carnea (Stephens 1836)

Material examined: 28.07.2018 (1 individual)

It is a polyphagous species reported to feed on aphids, scale insects, lepidopter eggs and larvae, psyllids, chrysomelid larvae, thrips and acars [74]. This is the first report showing that it predates upon M. hellenica. Ülgentürk et al. [19] reported another species of the genus (C. lucasina) as a predator of M. hellenica in Turkey. It occurs widely in Turkey [75,76]. This is the first report from Burdur.

RAPHIDIOPTERA: RAPHIDIIDAE

Raphidia ambigua Aspöck&Aspöck 1964

Material examined: 22.04.2018 (13), 01.05.2018 (5) and 12.05.2019 (1) (19 individuals)

It feeds on Coccoidea and Raphidiidae [77]. This is the first report showing that it predates upon M. hellenica. Argyriou et al. [78] reported another species of the genus (R. notata F.) as a predator of M. hellenica in Greece. In Turkey, it occurs in Afyonkarahisar, Ankara, Antalya, Balıkesir, Bilecik, Bitlis, Burdur, Çorum, Denizli, Diyarbakır, Elazığ, Isparta, İzmir, Kırşehir, Konya, Mersin, Muğla and Muş [79].

4 Discussion

In the present study, we identified 19 species foraging on M. hellenica in an isolated P. brutia stand, where M. hellenica is an introduced species. We report 12 of these species as the predators of M. hellenica for the first time (A. nemoralis, A. nemorum, C. carnea, N. quadrimaculatus, N. cruentatus, N. goedelii, O. majusculus, R. ambigua, S. pallipediformis, S. syriacus, S. gilvifrons and T. reduvinus), whereas 12 of the identified species were the first records for the Burdur region (A. nemoralis, A. nemorum, A. baccarum, C. bipustulatus, M. octodecimguttata, N. quadrimaculatus, N. cruentatus, R. cardinalis, S. syriacus, S. pallipediformis, S. gilvifrons and T. reduvinus). Among the 19 species we found, 7 species were also reported from the native range of M. hellenica (Table A1 in Appendix). The number of M. hellenica predator species in all its distribution reached 40 after the present study. The updated predator list is provided in Table A1 (Appendix). On the other hand, our low sample size along with suboptimal assumption approach we adopted to identify predation on M. hellenica necessitate further studies focusing directly on the predatory behavior of the species found in this study in order to confirm their predatory status. We additionally provided eight new occurrence records for M. hellenica out of its native range in Turkey (Figure A1).

The western end of the Taurus Mountain chain is a significant geographical barrier separating the coastal Aegean and Mediterranean regions from the Burdur basin. Furthermore, the forest cover is not continuous into the inner regions which must be a major barrier for the spread of a weak disperser such as the giant pine scale (40 m/year) (Nicolopoulos 1965 cited in ref. [80]). Thus, human-aided introduction seems to be the only way for M. hellenica to spread the appropriate spots in the inner regions. The local beekeepers have been introducing M. hellenica to several areas in Burdur since 1990s but some of these efforts failed probably due to inappropriate ecological conditions for M. hellenica. However, the humid climate of the study site owing to the nearby lake seems to have facilitated its establishment. We found 12 new species predating upon M. hellenica in its introduced range and we could not find in the study site the other 12 species that had been reported as M. hellenica predators from its native range. The two ranges (native and introduced) had seven species in common (Table A1). Although some of the predators (particularly N. kartliana) might be accidentally introduced into the region during the introduction of M. hellenica, most of them were cosmopolitan species occurring also in M. hellenica-free ecosystems. Therefore, we believe that most of the predator species we identified have started foraging on M. hellenica in the past 30 years in the study site, although they most probably occur in the natural range of M. hellenica. These results also suggest that native predator community can rather quickly include the giant pine scale into the menu in scale’s introduced range. This is not surprising as prey switching is a strategy that predators use in the process of accepting a new prey species [17]. Although identifying the predation strategy of M. hellenica predators was out of the scope of the present study and its sampling design, we hypothesize that prey switching strategy might be used by most of the predators we identified. As a supporting observation for this hypothesis, the abundance of the Aphididae and Coccoidae species, which are the main preys of the predatory species we identified in the present study, was significantly low in the study region during all the field visits. Therefore, the most abundant prey species in the region which was always available to the predators was M. hellenica. This hypothesis should be tested by further studies.

The highest number of individuals we found belonged to N. kartliana. This result was in accordance with that of Ülgentürk et al. [19] who demonstrated that N. kartliana was the most common predator of M. hellenica in the entire range of the giant pine scale in Turkey. This is not surprising as N. kartliana is a monophagous predator [43]. On the other hand, it was found only in March, April and May 2019, but not in 2018 probably due to the sampling bias. Its pupae were available only in the cottony secretions of M. hellenica which were more abundant in 2019 because of trap-logs established for O. erosus management program. We found N. kartliana pupae in March and larvae by April. If the species were in the adult stage in late May (e.g., Gaimari et al. [54] found adults in June in Greece), it might escape from the sampling. Although revealing the biology of N. kartliana was out of our scope in this study, the abundance of it and its monophagous nature suggests that it is the best candidate for biological control against the giant pine scale as suggested by Avtzis et al. [14]. Considering observed high frequencies of M. octodecimguttata (68.4% of all field visits), C. bipustulatus (57.9%) and H. quadripunctata (47.4%), and absence or scarcity of other possible prey species in the study site, the hypothesis of these Coccinellids being significant suppressors of the giant pine scale populations seems reliable. However, this hypothesis remains for testing through future studies.

5 Conclusion

The giant pine scale is an important component of the biodiversity in its native range as it supports several insect species by its honeydew secretion. On the other hand, it can be a pest in habitats where the host trees are weak due to several reasons such as poor soil quality and climatic change. In such habitats, the presence of M. hellenica can favor outbreaks of secondary pests such as bark beetles which can eventually lead to death of the host trees [3,80]. Indeed, during the present study, we noted several P. brutia deaths due to the Mediterranean pine beetle particularly on the hosts heavily infested with the giant pine scale. Therefore, introducing M. hellenica out of its native range in favor of apiculture can lead to serious pest problems which may ultimately threaten not only the biodiversity but also the sustainability of pine honey production. Considering the serious impact of the climate change predicted for the eastern Mediterranean [81], control of M. hellenica can be expected to be one of the major issues in the near future in the pine forests of the region and in other introduction spots such as Australia. This makes research on M. hellenica predators and parasitoids, particularly those from Anatolia where the giant pine scale most probably originated from ref. [80,82], a priority. In the future studies related to biological control of populations of the giant pine scale, a special importance should be given to N. kartliana as it seems to be a host specific predator of the pest [14]. Additionally, since all the predatory species feeding upon M. hellenica described so far have been diurnal species, research on the nocturnal predatory species may also contribute to a list of giant pine scale predators.

Acknowledgements

The authors thank Asst. Prof. Dr Derya Şenal for Coccinellidae, Prof. Dr Ahmet Dursun and Prof. Dr Meral Fent for Hemiptera, Prof. Dr Savaş Canbulat for Neuroptera and Raphidioptera identifications. The authors thank anonymous reviewers for their comments and suggestions on the earlier version of the article.

  1. Funding information: The study was financially supported by theTurkish Beekeeping Association.

  2. Conflict of interest: The authors state no conflict of interest.

  3. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Appendix

Table A1

Predators of Marchalina hellenica identified so far in Georgia, Greece and Turkey (○: in the natural range of M. hellenica in TR, ●: in the introduced range of M. hellenica in TR)

Order: family Species Country Reference
Acarina: Trombidiidae Allothrombium pulvinum ○ Turkey Ülgentürk et al. 2013 [19]
Allothrombium triticium ○ Turkey Ülgentürk et al. 2013 [19]
Acarina: Anystidae Anystis baccarum ○● Turkey Ülgentürk et al. 2013 [19]; Present study
Neuroptera: Chrysopidae Chrysopa pallens (Rambur) Greece Argyriou et al. 1976 [78]
Chrysopa (=Dichochrysa) flavifrons Greece Argyriou et al. 1976 [78]; Nicolopoulos 1965 [80]
Chrysoperla carnea ● Turkey Present study
Chrysoperla lucasina ○ Turkey Ülgentürk et al. 2013 [19]
Dichochrysa genei ○ Turkey Ülgentürk et al. 2013 [19]
Dichochrysa prasina ○ Turkey Ülgentürk et al. 2013 [19]
Pseudomallada flavifrons Greece Nicolopoulos 1965 [80]
Neuroptera: Hemerobiidae Wesmaelius subnebulosus ○ Turkey Ülgentürk et al. 2013 [19]
Raphidioptera: Raphidiidae Raphidia ambigua ● Turkey Present study
Raphidia (=Phaeostigma) notata Armenia, Georgia Hadzibejli 1969 [89]
Greece Nicolopoulos 1965 [80]; Gaimari et al. 2007 [54]
Diptera: Chameamyiidae Leucopis sp. ○ Turkey Bodenheimer 1953; Selmi 1983 [24]
Leucopis obscura Greece Nicolopoulos 1965 [80]
Neoleucopis kartliana ○● Turkey Ülgentürk et al. 2013 [19]; Present study
Georgia, Greece Gaimari et al. 2007 [54]
Hemiptera: Anthocoridae Anthocoris nemoralis ● Turkey Present study
Anthocoris nemorum ● Turkey Present study
Brachysteles parvicornis ○ Turkey Selmi 1983 [24]
Cardiastethus nazarenus ○ Turkey Ülgentürk et al. 2013 [19]
Ectemnus sp. ○ Turkey Selmi 1983 [24]
Elatophilus pachycnemis ○ Turkey Ülgentürk et al. 2013 [19]
Orius majusculus ● Turkey Present study
Temnostethus reduvinus ● Turkey Present study
Hemiptera: Reduviidae Nagusta goedelii ● Turkey Present study
Coleoptera: Coccinellidae Chilocorus bipustulatus ○● Turkey Giray 1970 [23]; Selmi 1983 [24]; Present study
Coccinella septempunctata ○ Turkey Selmi 1983 [24]
Exochomus sp. Georgia Hadzibejli 1969
Exochomus quadripustulatus ○ Turkey Selmi 1983 [24]
Harmonia quadripunctata ○● Turkey Selmi 1983 [24]; Present study
Hippodamia variegata Greece Nicolopoulos 1965 [80]
Myrrha octodecimguttata ○● Turkey Ülgentürk et al. 2013 [19]; Present study
Nephus quadrimaculatus ● Turkey Present study
Novius cruentatus ● Turkey Present study
Rodolia cardinalis ○● Turkey Ülgentürk et al. 2013 [19]; Present study
Scymnus pallipediformis ● Turkey Present study
Scymnus subvillosus ○● Turkey Ülgentürk et al. 2013 [19]; Present study
Scymnus syriacus ● Turkey Present study
Stethorus gilvifrons ● Turkey Present study
Coleoptera: Cantharidae Dasytes flavipes Turkey Bodenheimer 1953 [22]
Figure A1 Natural (circles) and introduced (triangles) distribution of Marchalina hellenica in Turkey (data from ref. [ 4,18,19,24] and personal observations) along with the first records made in the present study (asterisks) (counter map from ref. [87]).
Figure A1

Natural (circles) and introduced (triangles) distribution of Marchalina hellenica in Turkey (data from ref. [ 4,18,19,24] and personal observations) along with the first records made in the present study (asterisks) (counter map from ref. [87]).

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Received: 2021-01-14
Revised: 2021-04-24
Accepted: 2021-05-01
Published Online: 2021-07-01

© 2021 Şükran Oğuzoğlu et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
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  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
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  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
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  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
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  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
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  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
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  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
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  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
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  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
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https://doi.org/10.1515/biol-2021-0066
Schlagwörter für diesen Artikel
honeydew producer; Brutian pine; biological control; natural enemy; prey shift
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
  53. Primary localized cutaneous nodular amyloidosis presenting as lymphatic malformation: A case report
  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
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Heruntergeladen am 22.10.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2021-0066/html?srsltid=AfmBOoqaEJZsr5R32CYx_MDm-ex04c6V4T-UW2_qlITyqpWVq4P706oM
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