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3Russian Journal of Nematology, 2023, 31 (2), 125 - 137
Nematode biodiversity in pomegranate (Punica granatum L.) and mulberry (Morus spp.) growing
areas in Western Turkey
** 1 2 Lerzan Ozturk and Tohid Behmand
'Tekirdag Viticulture Research Institute, 59100, Tekirdag, Turkey 2Bayer, 16535, Bursa, Turkey e-mail: lerzanozturk@gmail.com
Accepted for publication 01 August 2023
Summary. The diversity and community structure of nematodes in pomegranate (Punica granatum L.) and mulberry (Morus spp.) growing areas in Western and Northwestern Turkey were determined in a two-year study. During surveys, 82 soil samples were collected from seven districts in izmir and Tekirdag provinces. A total of 37 nematode genera (mulberry 25 genera; pomegranate 27 genera) were identified. Nematodes were classified into six feeding groups: plant feeders (35%), bacterivores (16.7%), root-fungal feeders (15%), fungivores (11.7%), omnivores (5%) and predators (3.3%). The recovered species belonged to Dorylaimida, Chromadorida, Rhabditida, Aphelenchida, Mononchida, Triplonhida and Tylenchida orders. The most frequent species were Helicotylenchus digonicus, Pratylenchoides alkani, Boleodorus thylactus in pomegranate, and H. dihystera, Xiphinema pachtaicum, B. thylactus and Ditylenchus myceliophagus in mulberry. Criconemoides informis, Aphelenchoides clarus, A. sacchari, D. valveus, D. dipsaci, H. canadensis, H. varicaudatus and Longidorus elongatus were found for the first time in these host plants in Turkey. Key words: Aegean region, izmir, nematode fauna, orchards, Tekirdag, Thrace region.
Pomegranate (Punica granatum) and Mulberry (Morus spp.) are deciduous trees of the families Lythraceae and Moraceae. Originating from Asia, pomegranate (500 species) and mulberry trees (150 species) are grown in Europe, the Americas, and many other areas (Chandra et al., 2010; Kahramanoglu & Usanmaz, 2016). The biggest producers of pomegranate are Iran and India. Turkey, Egypt, Morocco, Tunisia and Spain are Mediterranean countries with large growing areas, and China is the leading mulberry grower (Zarfeshany et al., 2014). In Turkey, 69,317 tonnes of mulberry and 559,171 tonnes of pomegranate are produced annually in areas of 19,916 ha and 285.82 ha, respectively (TUiK, 2023).
Studies on plant-parasitic nematodes in mulberry and pomegranate orchards are limited in Turkey. There is some research on pomegranate in Southeastern Anatolia, but nematodes were identified to genus level only (Yildiz & Mamay, 2014). There are species-based diagnoses in mulberry areas, and two species were identified (Yuksel, 1977). Therefore, our research aimed to determine nematode diversity in mulberry and pomegranate growing areas in the western Turkey. In the survey area, both plants are often grown
separately or in polyculture with plants like grapevine and walnut.
MATERIAL AND METHODS
Survey and soil sample collection. A survey was carried out in 2019-2021 on pomegranate and mulberry in orchards in izmir and Tekirdag provinces, Turkey (Fig. 1). In the provinces, pomegranate is grown as monoculture or in polyculture with other plants such as grapevine and walnut. Hicaz pomegranate variety and black and white mulberry varieties were common in orchards. A total of 107 soil samples (48 mulberries, 59 samples of pomegranate) were collected from randomly selected different orchards from 0-40 cm (0-10, 10-20, 20-30 and 30-40 cm) soil depth using a soil auger. In a previous study to determine the prevalence of Xiphinema and Longidorus in the region, these species were found to be common at a depth of 30 cm and above. Plant-parasitic species were abundant between 10-30 cm (Ozturk et al., 2023). Therefore, soil samples were taken from four different depths in this study. The sampled locations were recorded, and soils were put into polyethylene bags, labelled, and transferred to the laboratory.
© Russian Society of Nematologists, 2023; doi: 10.24412/0869-6918-2023-2-125-137
Extraction of nematodes from soil samples.
Plant-parasitic nematodes were extracted by the centrifuge flotation method described by Jenkins (1964). In the process, approximately 100 g of soil samples were suspended in water. This mixture was sieved through 100 and 400 mesh sieves, and the supernatant was collected into a 50 ml centrifugation tube, which was centrifuged for 5 min at 370 g. Then, the existing water in the tube was discarded and 475 g l1 sugar solution was added and centrifuged again for 1 min at 370 g. After centrifugation, the suspension was sieved through 400 mesh sieves, and the supernatant containing the nematodes was collected.
Nematode identifications. Species
identifications were carried out by observation of females under a microscope from prepared nematode slides. Slides were prepared from extracted females killed at 60°C and fixed in TAF solution (Seinhorst, 1959). The morphometric parameter ratios and indices (Table 1) developed by De Man (1876) were used for characterisation. Measurements were done with Leica application suite software, and images were taken with a Celestron microscope (Celestron LCC, USA). The original descriptions and published dichotomous keys of Geraert and Raski (1987), Loof and Luc (1990), Loof and Chen (1999), Castillo and Volvas (2005) and Handoo et al. (2007) were used for species identification. Nematodes were subjected to diversity analysis, trophic groups were assigned based on feeding habitat, and coloniser-persister values were determined (c-p value 1-5) (Bongers, 1990; Yeates et al., 1993).
RESULTS
Fifty-three species of nematodes belonging to six orders, 37 genera, and 12 families were found in the
soils of mulberry and pomegranate orchards. The majority of all identified specimens belonged to Tylenchida (32 species), and the rest were from Rhabditida (7), Dorylaimida (6 species), Aphelenchida (5 species), Mononchida (1 species), Chromadorida (1 species), Triplonchida (1 species) orders. In the surveys, 40 nematode species were detected in the mulberry fields, while 46 were determined in the pomegranate fields. Forty species were determined in the soil samples taken from the province of Izmir, and 47 were determined in the samples from Tekirdag. Most nematodes in mulberry areas were plant-parasitic species, followed by root-fungal feeders, bacteriovores, fungal feeders, predators, and omnivores. Plant-parasitic species took first place in pomegranate areas, followed by root-fungal feeders, bacteriovores, fungal feeders, predators, and omnivores. The recovered nematode species were from values 1 to 5 according to coloniser-persister values (c-p) (Bongers, 1990; Yeates et al., 1993). Nearly half of the species detected in mulberry samples were in c-p 2; the rest were c-p 1, c-p 3, c-p 4, and c-p 5 class, while in pomegranate, they belonged to c-p 2, c-p 3, c-p 4, c-p 5, c-p 1 class. Plant-parasitic species belonging to the c-p were predominant in Izmir and Tekirdag provinces (Fig. 2). The species recovered from pomegranate and mulberry soil samples are listed in Table 1.
Among plant-parasitic nematodes, 25 were migratory ectoparasites, five were migratory endoparasites, and one was semi-endoparasite (Figs 2, 3). Five endoparasitic species were found in pomegranate and four in mulberry. The number of ectoparasite species identified was 20 in mulberry and 23 in pomegranate. The semi-endoparasite, Rotylenchulus macrosoma, was only present in soil samples collected from Izmir province. Among all these species, Ditylenchus dipsaci, Mesocriconema
Fig. 1. Survey area map of mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Nematodes associated with pomegranate and mulberry in Western Turkey
Table 1. Nematodes identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Nematode genus/species Feeding habitat c-p Mulberry Mulberry Pomegranate Pomegranate
izmir Tekirdag Tekirdag izmir
Alaimus spp. Bacteriovores 2 + - - -
Achromadora Bacteriovores 3 - - + -
Acrobeloides Bacteriovores 2 + + + +
Acrobeles Bacteriovores 2 + + + +
Aporcelaimellus Bacteriovores 5 - + + +
Aphelenchus avenae Fungal feeder 2 + + + +
Aphelenchoides sacchari Fungal feeder 2 + + + +
Aphelenchoides clarus Fungal feeder 2 - - + -
Aphelenchoides obtusus Fungal feeder 2 - + - -
Basiria graminophila Root-fungal feeder 2 - - + -
Boleodorus thylactus Root-fungal feeder 2 + + + +
Cephalobus Bacteriovores 2 + + + +
Clarkus Predator 4 + + + -
Criconemoides infromis Plant feeder 3 - - + +
Coslenchus turkeyensis Root-fungal feeder 2 - + + +
Ditylenchus longicauda Fungal feeder 2 - + - -
Ditylenchus myceliophagus Fungal feeder 2 - + - +
Ditylenchus dipsaci Plant feeder 2 + - + +
Ditylenchus valveus Fungal feeder 2 - - + -
Dorylaimus Omnivore 4 + - + +
Eucephalobus Bacteriovores 2 + - - -
Filenchus filiformis Root-fungal feeder 2 - - + -
Filenchus cylindricauda Root-fungal feeder 2 + + + +
Filenchus sheri Root-fungal feeder 2 - + + +
Filenchus thornei Root-fungal feeder 2 + + + -
Geocenamus microdorus Plant feeder 3 - + + -
Geocenamus brevidens Plant feeder 3 + + + +
Helicotylenchus dihystera Plant feeder 3 + + + -
Helicotylenchus digonicus Plant feeder 3 + + + +
Helicotylenchus tunisiensis Plant feeder 3 - + - -
Helicotylenchus canadesis Plant feeder 3 - + + -
Helicotylenchus varicaudatus Plant feeder 3 - - + -
Longidorus elongatus Plant feeder 5 - - - +
Mesocriconema xenoplax Plant feeder 3 + + + +
Mesorhabditis Bacteriovores 1 + + + +
Mesodorylaimus Omnivore 4 + + + +
Panagrolaimus Bacterovores 1 - - + -
Paratrophurus loofi Plant feeder 3 - - + -
Paratylenchus nainianus Plant feeder 2 - + - -
Paratylenchus nawadus Plant feeder 2 - - + -
Pratylenchoides alkani Plant feeder 3 + + + +
Pratylenchus thornei Plant feeder 3 + + + +
Pratylenchus neglectus Plant feeder 3 + + - +
Table 1 (continued). Nematodes identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Nematode genus/species Feeding habitat Mulberry Mulberry Pomegranate Pomegranate
c-P izmir Tekirdag Tekirdag izmir
Psilenchus hilarulus Root-fungal feeder 2 - + + -
Rhabditis Bacteriovores 1 + + + +
Seinura Predator 4 - - - +
Rotylenchulus macrosoma Plant feeder 3 + - - +
Tripyla Bacteriovores 3 + + + +
Tylenchus davainei Root-fungal feeder 2 + + + -
Tylenchorhynchus cylindricus Plant feeder 3 + - - +
Tylenchorhynchus robustus Plant feeder 3 - - + -
Xiphinema pachtaicum Plant feeder 5 - + + -
Zygotylenchus guevarai Plant feeder 3 - + - -
xenoplax, Pratylenchus thornei and P. neglectus were considered the most harmful in the world by causing greater damage and yield loss (Singh et al., 2013). On the other hand, Longidorus elongatus can transmit several nepoviruses.
The highest number of individuals of Geocenamus brevidens (110 specimens (100 cm3 soil)-1) Helicotylenchus digonicus (50 specimens (100 cm3 soil)-1), Pratylenchoides alkani (50 specimens (100 cm3 soil)-1), Filenchus filiformis (62 specimens (100 cm3 soil)-1), Criconemoides informis (137 specimens (100 cm3 soil)1), Boleodorus thylactus (50 specimens (100 cm3 soil)-1) and Ditylenchus dipsaci (37 specimens (100 cm3 soil)-1) were collected from pomegranate fields. The most frequent species in soil samples were H. digonicus, P. alkani and B. thylactus. Longidorus elongatus, detected in only one orchard in izmir, was the least common species. Most of the specimens were collected from 10-30 cm soil depth. In addition, the population density of some species, including C. informis, B. thylactus and Aphelenchus avenae decreases significantly as soil depth increases. In mulberry areas, the highest number of individuals collected were R. macrosoma (70 specimens (100 cm3 soil)-1), H. tunisiensis (62 specimens (100 cm3 soil)-1), Xiphinema pachtaicum (55 specimens (100 cm3 soil)-1), B. thylactus (47 specimens (100 cm3 soil)-1) and D. dipsaci (54 specimens (100 cm3 soil)-1).
Bacterivore nematodes were the second most distributed group after plant-parasitic nematodes. Cephalobus was the prevalent genus with 82% occurrence, followed by Acrobeloides, Acrobeles and Rhabditis. The other widespread species belonged to the omnivore Mesodorylaimus and
predator Clarkus genera. No species belonging to the genera Achromadora, Seinura and Panagrolaimus were found in the mulberry orchards, Alaimus and Eucephalobus were not found in the pomegranate fields. The morphometrics of nematode species are given in Tables 2-7, and the parameters fit with the original descriptions.
DISCUSSION
In the studies, carried out in pomegranate and mulberry orchards in izmir and Tekirdag provinces in the Aegean region and the Marmara regions of Turkey, a total of 53 nematode species were identified. Nematodes in this survey area belonged to Aphelenchida, Tylenchida, Mononchida, Enoplida, Chromadorida and Rhabditida orders, with Tylenchida as the dominant order. All nematodes from Aphelenchida and Tylenchida and some species from Dorylaimida were identified to the species level. Most of the detected species were the first records in pomegranate and mulberry fields in our country. In terms of the number of species, Helicotylenchus (5), Filenchus (4), and Ditylenchus (4) from Tylenchida took the first place. The majority of specimens in izmir and Tekirdag were plant-parasitic nematodes.
To date, several studies have been carried out in pomegranate orchards worldwide. Melodogyne incognita, M. javanica, M. acrita, Xiphinema basiri, X. index, Longidorus iranicus, Pratylenchus coffeae, Helicotylenchus indicus, H. multicinctus, Ditylenchus spp., Rotylenculus reniformis, Aglenchus spp., Basiria graminophila, Basiroides obliquus, Ditylenchus sp., Merlinius communicus, M. pistaciei, Criconema punici, Psilenchus
Nematodes associated with pomegranate and mulberry in Western Turkey
hilarulus, Tylenchulus semipenetrans and Tylenchorhynchus brassicae have been found in pomegranate (Edward et al., 1971; Sturhan & Barooti, 1983; Fatema & Farooq, 1992; Khan et al., 2005; Nasira et al., 2011; Ilangovan & Poornima, 2017; Bajestani & Dolatabadi, 2018). By contrast, the presence of Pratylenchus, Meloidogyne, Xiphinema, Filenchus, Helicotylenchus and Geocenamus genera in pomegranate in Turkey was reported in the literature (Yildiz & Mamay, 2014). Many nematodes also attack mulberry; to date, 42 nematode species belonging to 24 genera have been recorded from different parts of the world. Pratylenchoides erzurumensis has also been found in mulberry-growing areas in Turkey (Yuksel, 1977). In the current study in izmir and Tekirdag, similar genera were detected in mulberry and pomegranate, but different species were identified. The morphometric parameters and descriptions of the specimens in this study correspond with the original descriptions. Only minor differences, like tail shape, number of annuli (16-19), and tail tip (rounded or slightly truncate) in Pratylenchus neglectus were observed.
Plant-parasitic species can feed on roots all year, and constantly damaged roots lose their ability to take up water and nutrients from the soil. These pests seriously affect young rootstocks planted in newly established orchards or nurseries. In addition to direct plant damage, the nematode wounds at feeding sites
provide access to many soil-born pathogens, which may cause secondary infections and significant yield loss (Back et al., 2002). Not all, but some species are considered significant pests of agricultural production. Mesocriconema xenoplax that we detected in both pomegranate and mulberry fields are able to cause stunting in plants. Species from Pratylenchinae and Pratylenchoidinae subfamilies that we found also cause significant damage. The Pratylenchus genus in Pratylenchinae is the main threat to agricultural production, with more than 70 polyphagous species feeding as endoparasites. Migratory endoparasites P. thornei and P. neglectus are among the most harmful nematode species in the world, causing up to 90% yield loss in some plants (Riga et al., 2008). Additionally, the virus vector Longidorus elongatus, which we detected in the pomegranate orchard in izmir, is an important ectoparasitic nematode of many cultivated plants. Transmission of tobacco black ringspot virus (TRBV) and raspberry ringspot virus (RRSV) by the vector nematode occurs during a short feeding period, and disease control is difficult in infected plants (Halbrendt & Brown, 1993).
In contrast to plant-parasitic nematodes, free-living bacterivore species play an essential role in the mineral cycle of soil. As a result of consuming bacterial food sources, they release nitrogen and promote phosphorus and sulfur mineralisation (Kennedy & de Luna, 2005). Other roles of nematodes
Fig. 2. Percentage of nematodes in mulberry and pomegranate orchards: A) Feeding habitat; B) Coloniser-persister class; C-D) % proportions in izmir and Tekirdag.
Fig. 3. Light microscope images of Mesocriconema xenoplax (A-B), Longidorus elongatus (C-E); Xiphinema pachtaicum (F-H) and Helicotylenchus digonicus (I-J). All scale bars are 20 ^m.
Table 2. Morphometries of Aphelenchus avenae, Aphelenchoides sacchari, A. obtusus.A. darns, Boleodorus thylactus, Basiria graminophila and Coslenchus turkevensis identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Measurements except for L in |im: mean ± SD (range).
Characters Aphehencliits avenae Aphelenchoides sacchari Aphelenchoides obtusus Aphelenchoides clarus Boleodorus thylactus Basiria graminophila Coslenchus turkeyensis
n 10 8 2 5 10 2 6
L (mm) 0.75 ±0.01 (0.75-0.78) 0.76 (0.73-0.8) 0.54-0.58 0.46 (0.45-0.47) 0.55 ±0.02 (0.51-0.59) 0.78-0.80 0.57 ±0.02 (0.54-0.59)
a 34.1 ±4.72 34.8 ±2.69 28.4-31 33.5 ±0.35 27.8 ±3.61 37.2 28.1 ±0.6
(28.7-38.3) (31.2-38.8) (33.2-34.1) (22.5-32.5) (27.2-29)
5.43 ±0.07 6.5 ±0.23 5.34-5.54 5.43 ±0.07 4.88 ±0.2 6-6.2 5.3 ±0.12
1) (5.3-5.5) 6.2-6.8) (5.3-5.5) (4.61-5.14) (5.2-5.4)
30.6 ±3.16 16.1 ± 1.68 14.5-19 14.4 ±0.27 10.8 ±0.8 6.5-6.6 6.7 ±0.55
c (25.8-33.7) (14.4-18.8) (14-14.7) (9.8-12.2) (6.2-7.5)
* 1.76 ±0.36 4 ±0.75 8.67-8.9 3 ± 0.04 4.3 ±0.22 9.22-9.43 10.8 ±0.94
c (1.34-2.3) (2.9-4.8) (2.9-3.1) (3.95-4.36) (9.5-11.7)
Stylet 25.35 ± 1 (24-26.9) 16 ± 1 (14.7-17.4) 10-10.21 10.15 ±0.33 (9.8-10.79) 11.2 ±0.92 (10.5-13) 10.4-10.7 9.9 ±0.21 (9.8-10.3)
Tail 25.3 ±3.23 50.4 ±3.72 31-37.9 34.2 ±0.67 51.9 ±4.39 119.6-121.3 87.3 ±3.72
(22.4-30.4) (45.9-55) (33.2-35) (47.1-56.6) (82-90)
Vulva % 76.7 ±0.82 68.3 ± 1.23 72-75 66 54.2 ±4.1 68-70 63.6 ±2
(76-78) (67-70) (51.9-58.4) (61-64)
T/V-A
Table 3. Morphometries of Filenchus sheri, F. cvlindricauda, F. thorn ei, F. filiform is, Geocenamus microdorus, G. brevidens, Ditvlenchus valve us and /1 dipsaci identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Measurements except for L in |im: mean ± SD (range).
Characters Filenchus Filenchus Filenchus Filenchus Geocenamus Geocenamus Ditylenchus Ditylenchus
sheri cylindricauda thorn ei Jiliformis microdorus brevidens valveus dipsaci
n 6 6 8 10 5 6 1 6
L (mm) 0.54 ±0.01 0.86 0.73 ± 0.02 0.57 ±0.02 0.71 ±0.01 0.54 ±0.01 0.82 0.96 ±0.02
(0.52-0.67) (0.85-0.87) (0.71-0.76) (0.54-0.61) (0.71-0.74) (0.52-0.56) (0.79-0.86) (0.93-1)
a 30.8 ±3.3 38.5 ±2.48 33.2 ± 1.64 34.8 ±0.88 28.2 ±2.47 26.6 ±0.69 44 ± 2.2 32.8 ±0.9
(26.7-34.5) (35-40) (31.6-35.3) 33-35.8) (26.3-31.7) (25.4-27.4) (41-48) (32-34.3)
5.4 ±0.36 6.16 ±0.3 6.43 ±0.23 5.6 ±0.26 5.2 ±0.08 4.58 ±0.42 6.3 ±0.39 6.6 ±0.22
D (5-6) (5.9-6.6) (6.1-6.8) (5.2-5.7) (5.1-5.3) (4-5) (6.1-7) (6.3-6.9)
5 ± 0.1 6.5 ±0.3 4.3 ±0.11 62.6 ±0.93 15.8 ±0.66 12.3 ± 1.39 11.3 ± 1 20 ± 1.71
C (4.86-5.33) (6-6.8) (4.2-4.5) (61.6-64) (14.9-16.4) (10.7-14.1) (10.2-12.3) (18.6-23.3)
* 10.5 ± 1.23 6.5 ±0.49 13.4 ± 1.64 135.7 ± 1.24 2.6 ±0.08 2.6 ±0.07 6.2 ±0.42 2.29 ±0.08
C (8.8-12) (6.5-6.6) (11.3-15.3) (134-137.5) (2.5-2.7) (2.5-2.7) (5.8-6.4) (2.17-2.41)
Stylet 9.84 ±0.6 10.3 ±0.3 10.25 ±0.45 12.4 ±0.3 14.2 ±0.14 14.4 ± 1.24 7.9 ±0.62 10.7 ±0.64
(8.8-10.4) (9.9-10.7) (9.5-10.7) (12-12.6) (14-14.3) (12.7-15.5) (7-8.7) (9.9-11.7)
Tail 108.2 ±2.16 121 ±6.4 170.5 ±8.8 30.2 ±0.71 46.5 ±0.9 48.2 ±3.9 73 ±4.13 30.2 ±0.71
(105-111) (112-124) (157-181) (29.2-31) (45.2-47.7) (46-50.7) (68-77) (29.2-31)
Vulva % 61 ±2.54 66.6 ± 4 61 ±0.89 56.7 ±0.45 53.4 ±0.87 56.2 ± 1.28 79 ±3.39 86 ± 4.24
(58-65) (61-70) (60-62) (56-57) (52.2-54.1) (55-58.7) (74-83) (80-89)
T/V-A 1.24 ±0.09 (1.17-1.41) - 1.6 - - - - -
Table 4. Morphometries of Ditylenchus longicauda, D. mvceliophagus, Helicotvlenchus varicaudatus, H. digonicus, H. dihvstera, H. canadensis and H. tunisiensis identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Measurements except for L in |im: mean ± SD (range).
Characters Ditylenchus longicauda Ditylenchus mycelioph agus Helicotylenchus varicaudatus Helicotylenchus digonicus Helicotylenchus dihystera Helicotylen ch us canadensis Helicotylenchus tunisiensis
n 2 6 5 8 6 2 5
L (mm) 1.17-1.23 0.77 ±0.01 (0.74-0.77) 0.76 (0.75-0.77) 0.76 ±0.02 (0.72-0.78) 0.67 (0.65-0.67) 0.98-0.99 0.97 ±0.01 (0.97-1)
a 45-47 37.16 ± 1.59 27.3 ± 2.06 29.3 ±2.21 25.7 ±0.5 28.6-29.7 40.1 ±4.7
(35.3-39.1) (24.5-29.3) (26.5-32.2) (24.9-26.3) (33.7-45)
8-8.2 6.23 ±0.2 5.9 ±0.3 4.7 ±0.15 5.35 ±0.14 7.3-7.7 7.26 ± 0.04
D (6-6.5) (5.5-6.2) (4.5-4.9) (5.2-5.5) (7.2-7.3)
8.71-9 12.3 ±0.9 48.9 ± 1.47 24.1 ±0.69 18.1 ±0.77 25.7-26.1 48.1 ±3.56
C (11.3-13.9) (47.7-51) (23.3-24.6) (17.1-19.1) (43.4-52)
* ft ^ ft S 4.47 ±0.3 0.94 ±0.04 1.7 ±0.08 1.2 ±0.05 0.89-0.91 1.1 ±0.08
C (4-4.85) (0.89-1) (1.59-1.72) (0.97-1.11) (1-1.2)
Stylet 10.5-11.2 10.2 ±0.28 (9.9-10.6) 26 ± 1 (25-27.5) 26.1 ± 1 (25-27.8) 26.2 ±0.87 (25-27.3) 26.9-27.3 26.4 ±0.50 (25.7-27.1)
Tail 134.2-136.1 58.3 ±4.9 15.3 ±0.49 32 ±0.08 35.5 ±4.2 37.5-38.4 21 ± 1.63
(57-65) (14.8-16) (31.1-33.6) (35-38) (19-23)
Vulva % 79-80 82.5 ± 1.80 (80-85) 60 ± 1 (60-62) 60 62 57-59 59.2 ± 1.92 (56-61)
T/V-A
Table 5. Morphometries of Longidorus elongatus, Paratylenchus nawadus, P. nainianus, Paratrophurus loofi, Pratylenchoides alkani, Pratylenchus neglectus, P. thornei and Psilenchus hilarulus identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Measurements except for L in |im: mean ± SD (range).
Characters Longidorus elongatus Paratylenchus nawadus Paratylenchus nainianus Paratroph urus loofi Pratylenchoides alkani Pratylenchus neglectus Pratylenchus thornei Psilenchus hilarulus
n 2 8 5 6 10 11 8 2
L (mm) 5.8-6.2 0.35 ±0.05 (0.27-0.4) 0.28 ±0.01 (0.27-0.3) 1±0.01 (0.99-1.02) 0.74 ±0.02 (0.72-0.78) 0.46 ± 0.02 (0.43-0.5) 0.55 (0.51-0.59) 9.1-9.4
a 94.8-99.6 21.2 ±2.96 28 ± 1 34.2 ±0.85 29.1 ±0.14 24 ±3.68 28.4 ±0.96 33.5-33.7
(17.7-24.2) (27-30) (33.3-35.1) (29-29.4) (20.4-29.4) (27-29.7)
u 18-20.3 5.23 ± 0.26 4.08 ±0.07 5.4 4.71 ±0.18 5 ± 013 6 ±0.09 6.57-6.59
1) (5-5.6) (4-4.2) (5.3-5.5) (4.48-5) (4.86-5.18) (5.97-6.22)
136-148.3 12.4 ± 1.64 23 ± 0.08 22.4 ±0.11 16.15 ± 1.42 20.35 ±3.16 22.2 ±0.43 6.4-6.52
c (10.2-14.1) (23-23.2) (22.3-22.5) (14.5-17.9) (16.3-25) (22-23)
1.01-1.07 2.66 ±0.23 2.66 ±0.23 2 ± 0.06 2.66 ±0.03 1.69 ±0.27 1.88 ±0.03 8.34-8.47
c (2.46-3) (2.46-3) (1.9-2.2) (2.6-2.7) (1.2-1.9) (1.85-2.01)
Stylet 136-140 28.9 ± 1.67 (27.6-31.3) 26.8 ±0.35 (26.3-27.2 16.5 ±0.13 (16.4-17) 17.3 ±0.81 (16-18.5) 15.4 ± 1.58 (13-17.9) 15.3 ±0.66 (15.3-17) 11.4-12
Tail 41.8-42.4 25.7 ±2.51 12.27 ±0.46 45.5 ±0.84 46.2 ±2.56 23.5 ±2.58 24.3 ±0.6 142.4-144.3
(22.2-27.9) (11.7-12.9) (44.9-46) (43.9-49.8) (20-27) (23.5-25)
Vulva % 49 84 ± 0.82 82.2 ±0.56 82 ± 1.58 56 57.2 ± 1 54.2 ±4.1 49-50
(83-85) (81-83) (80-84) (57-59.2) (51.9-58.4)
T/V-A
Table 6. Morphometries of Rotvlenchulus macrosoma, Tylenchorhynchus cvlindricus, T. robustus, Tylenchus davainei.Xiphinema pachtaicum and Zygotylenchus quevarai identified in mulberry and pomegranate orchards in the izmir and Tekirdag regions of Turkey.
Measurements except for L in |im: mean ± SD (range).
Characters Rotylenchulus macrosoma Tylenchorhynchus cylindricus Tylenchorhynchus robustus Tylenchus davainei Xiphinema pachtaicum Zygotylenchus quevarai
n 6 5 2 1 10 6
L (mm) 0.47 ±0.3 (0.43-0.49) 0.80 ±0.01 (0.79-0.83) 0.95-0.97 0.67 1.86 ±0.02 (1.82-1.89) 0.58 ±0.05 (0.49-0.65)
a 30 ±2.58 34.8 ± 1.43 34.9-35.1 34.7 62.6 ±0.82 22.8 ±4.1
(27.5-33.2) (33-36.5) (61.8-64) (19.2-29)
4.28 ±0.45 6.13 ±0.12 5.33-5.41 6.6 5.6 ±0.26 5.45 ±0.4
D (3.5-4.7) (6-6.3) (5.2-5.7) (5-5.9)
12.47 ±0.21 12.8 ±0.41 16.1-16.2 4 ± 0.19 22.4 ±0.78
C (12.1-12.6) (12.4-13.4) 0 (3.7-4.2) (21.6-23.4)
26.2 ±0.87 3.65 ±0.08 2.87-2.93 7.62 10.5 ±0.96 1.84 ±0.08
C (25-27.3) (3.5-3.7) (10.1-10.9) (1.7-2)
Stylet 35.5 ±4.2 (35-38) 12.46 ±0.41 (11.9-12.9) 19.5-19.7 10.21 12.4 ±0.30 (12-12.6) 16 ±2.43 (12.8-18.8)
Tail 37.4 ± 1.6 63 ±0.77 58.7-59.8 111.1 142 ±5.5 26.1 ±2.13
(35.6-39) (62.1-64) (137-148) (22.4-28.1)
Vulva % 66.4 ±4.8 53.2 ±0.72 64-66 61 57.2 ± 1.33 59.6 ± 1.81
(66-67) (52-54) (55-60) (57-62)
T/V-A - - - - - -
Table 7. Morphometries of Mesocriconema xenoplax and Criconemoides informis identified in mulberry and
pomegranate orchards in the izmir and Tekirdag regions of Turkey. Measurements except for L in ^m; mean ± SD (range).
Characters Mesocriconema xenoplax Criconemoides informis
n 10 5
0.57 ± 0.01 0.49 ± 0.03
L (mm) (0.55-0.61) (0.46-0.54)
13.4 ± 1.24 16.15 ± 1.38
a (11.2-15.1) (14.5-19.1)
3.4 ± 0.31 4.94 ± 0.14
b (2.9-3.7) (4.7-5.1)
14.8 ± 1.96 34.1 ± 1.88
c (11.2-16.7) (31.7-37)
80.8 ± 4.33 44.4 ± 2.16
Stylet (76-88) (41-47)
90.1 ± 2 90.2 ± 1.47
% Vulva (88-94) (88-94)
105.8 ± 3.82 71.4 ± 2.65
R (100-112) (68-76)
92 ± 4 69.3 ± 3.29
RV (86-98) (65-73)
RAN 6 ± 0.92 2.8 ± 0.74
(5-7) (2-4)
are to regulate the rate at which organic compounds break down into inorganic ions, feed on plant pathogens and reduce their populations, and serve as prey and food source for nematode-trapping fungi. Fungivore nematodes like Aphelenchus avenae, which we found in orchards, can feed on fungal hyphae of more than 54 species, including plant-pathogenic Botrytis cinerea, Fusarium graminearum, F. oxysporum and Verticillium dahliae (Taher et al., 2017). Predator nematodes can feed on other nematodes or insects; for example, Clarkus species can feed on the world's most damaging plant-parasitic nematodes, Meloidogyne spp. (Steiner & Heinley, 1922).
Studies on identifying nematode species in mulberry and pomegranate orchards in Turkey and the world are limited, and the number of identified species is low. In previous studies, only plant-parasitic nematode species were determined (Khan et al., 2005; Yildiz & Mamay, 2014). In the present work the presence of all nematode species, such as predators, bacterivores, omnivores, fungal feeders and plant parasites, in pomegranate and mulberry fields in two different provinces in our country were examined and identified. Migratory ectoparasite, migratory endoparasite, and semi-endoparasite plant-parasitic species were found in survey areas.
Within these, P. neglectus, P. thornei, Mesocriconema xenoplax, and virus vector L. elongatus can directly or indirectly cause severe plant damage and economic yield loss.
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L. Ozturk and T. Behmand. Биоразнообразие нематод в районах выращивания граната (Punica granatum L.) и шелковицы (Morus spp.) в Западной Турции.
Резюме. В ходе двухлетнего исследования были определены разнообразие и структура сообществ нематод в районах выращивания граната (Punica granatum L.) и шелковицы (Morus spp.) на западе и северо-западе Турции. Было собрано 82 образца почвы в семи районах провинций Измир и Текирдаг. Всего выявлено 37 родов нематод (25 родов у тутовника и 27 родов у граната). Нематоды были разделены на шесть пищевых групп: фитотрофы (35%), бактериотрофы (16,7%), корневые микотрофы (15%), микотрофы (11,7%), политрофы (5%) и хищники (3,3%). Обнаруженные виды принадлежали к отрядам Dorylaimida, Chromadorida, Rhabditida, Aphelenchida, Mononchida, Triplonhida и Tylenchida. Наиболее часто встречающимися видами были Helicotylenchus digonicus, Pratylenchoides alkani, Boleodorus thylactus на гранате и H. dihystera, Xiphinema pachtaicum, B. thylactus и Ditylenchus myceliophagus на шелковице. Criconemoides informis, Aphelenchoides clarus, A. sacchari, D. valveus, D. dipsaci, H. canadensis, H. varicaudatus и Longidorus elongatus были впервые обнаружены у этих растений-хозяев в Турции.
