1✉ Plant Protection Department, Faculty of Agriculture, Ordu University, Ordu, Turkey.
2Plant Protection Department, Faculty of Agriculture, Ordu University, Ordu, Turkey.
2022 - Volume: 62 Issue: 4 pages: 941-955https://doi.org/10.24349/vt6l-svza
Pome fruits are members of the family Rosaceae and subfamily Pomoideae (Özçağıran et al. 2005). In the world, the total production of pome fruits is approximately 113,750,265 tons per year on 7,485,379 hectares of land (FAO 2019). In Turkey, pome fruits are grown on 211.961 hectares of the 23.199.945 hectares of agricultural land. Pome fruits with an annual production of 5,056,672 tons constitute the second group in order of importance in Turkish fruit cultivation (TUIK 2021).
Pome fruits contribute significantly to the Turkish economy. This fruit group's revenue derived from exports has been approximately 200 million US Dollars (YMS Reports 2021). Besides the significant economic importance, these fruits are intended for fresh consumption but also in processed forms. They also supply the raw material for industry (Milic et al. 2016). However, even today, world pome fruit production suffers significant losses due to plant pests, diseases and weeds, despite all scientific advances (Özsayın 2012). Phytophagous mites are potentially one of the major pest groups of pome fruits (Hoy 2011).
Many studies on mite species associated with pome fruits were conducted in various countries. For example, mite species on apple trees in England (Collyer 1956), Michigan (USA) (Strickler et al. 1987), Finland (Tuovinen and Rokx 1991), Israel (Palevsky et al. 1996), Slovakia (Praslicka and Bartekova 2008), Iran (Rahmani et al. 2010), Syria (Dahiah et al. 2011), Serbia (Stojnic et al. 2014) and Egypt (Hussian et al. 2018); pear mite fauna in Britain (Bergh and Weiss 1993), Egypt (Ismailia) (Osman and Mahmoud 2008); mite species on both apple and pear trees in Slovakia (Praslicka et al. 2009) and India (Singh et al. 2016) were determined.
Other studies detected the mite species on pome fruits in different regions of Turkey (Çobanoğlu 1993 a, b, c, d; İncekulak and Ecevit 2002; Yanar and Ecevit 2005; Kasap and Çobanoğlu 2007; Kumral and Kovancı 2007; Yanar and Ecevit 2008; Kasap et al. 2013; Kasap et al. 2015; Akyazı et al. 2017). However, as far as we know, no previous research has investigated mite species on apple, pear, quince and loquat in Ordu province. Although there are conventional pome fruit orchards in Ordu, fruit production is generally carried out in small gardens without using pesticides, in contrast to conventional orchards. So, our initial hypothesis is that a high diversity of mite species is expected to be found in the non-treated orchards.
The study also presents the result of a faunistic analysis of the phytophagous and predatory mite communities found in this area. Kumral and Kovancı (2007) studied the similarity indexes of mite species on apple, pear, and quince trees in conventional and agrochemical-free orchards in Bursa province of Turkey. In Serbia, the species assemblages of tetranychid and phytoseiid mites on cultivated and wild apple trees were researched by Stojnic et al. (2014).
Thus, the purpose of the current study is to present the comparative faunistic analysis of mite species on conventional and neglected apple, pear, quince, and loquat trees in 12 municipalities of Ordu province in Turkey as well as their diversity and distributions.
The survey was conducted in selected neglected (naturally growing trees without using agrochemicals) and conventional pome fruit orchards (trees grown using synthetic chemical fertilizer, pesticides, herbicides, and other continuous inputs). Leaf samples were collected from 12 different sampling areas (Altınordu, Fatsa, Kabadüz, Perşembe, Ulubey, Ünye, Akkuş, Çatalpınar, Çaybaşı, Çamaş, Gürgentepe and Gülyalı) in Ordu, Black Sea region (Turkey) (Figure 1). Geographical coordinates were recorded using a GPS mobile device (Garmin Etrex 30).
The surveys were carried out on four different pome fruit species; apple (Malus domestica Borkhausen), pear (Pyrus communis L.), quince (Cydonia oblonga Miller), and loquat [Eriobotrya japonica (Thunberg) Lindley] (Rosaceae). The samples were collected from 271 different coordinate points located at 176 villages. A total of 2.141 samples were collected: 1.077 conventional trees and 1.064 neglected trees.
Samplings were carried out between April and November each year at 10–15 day intervals from 2014 to 2016. The number of sampled trees per site was determined according to the total number of trees in each orchard (Table 1). On each sampling date, approximately 20 leaves per tree were taken from different parts of the tree canopy, i.e., lower, middle, and upper canopy. The samples were put into paper bags placed inside plastic bags, labeled, and transferred to the laboratory, where they were kept in a refrigerator at 4 °C for future examination.
Mites found on the adaxial and abaxial surfaces of the leaves were collected with a paintbrush (5/0) under a stereomicroscope (Leica S8 APO). Subsequently, the leaf samples were also placed in Berlese-Tullgren funnels for 24 hours to extract all mites. The specimens were preserved in vials containing 70% ethanol. All mites were cleared in a Lacto-phenol medium. Each mite was mounted in a drop of Hoyer's medium on microscope slides according to the method of Krantz and Walter (2009). On the other hand, the eriophyoid specimens were cleared in Keifer's booster medium and mounted using an ''F'' medium as suggested by Amrine and Manson (1996). The slides were dried in an oven (Ecocell EC111) at 50 °C for 5–7 days.
The identification of mites was performed using a light microscope equipped with phase contrast (Leica DM 2500, Heerbrugg, Switzerland). The species identifications were confirmed by Dr. Farid Faraji (Phytoseiidae), Prof. Dr. Serge Kreiter (Phytoseiidae), Prof. Dr. Eddie A. Ueckermann (Tydeidae, Stigmaeidae, Iolinidae, Triophtydeidae, Cunaxidae, Cheyletidae, Blattisociidae), Prof. Dr. Owen Seeman (Tenuipalpidae), Dr. Philippe Auger (Tetranychidae), Dr. Mariusz Lewandowski (Eriophyidae), and Prof. Dr. Antonio C. Lofego (Tarsonemidae).
The percentage of each species detected during the sampling period was calculated according to Yu et al. (2015) as follows:
Percentage of each species (%) = (Number of each mite species / Total number of collected mites) × 100
For the faunistic analysis of the similarity between the mite communities on pome fruits and to evaluate β- diversity, Sorensen's index (QS) or similarity coefficient was used. The value of Sorensen's index ranges from 0 to 1. Sorensen's index was calculated using the following formula (Southwood 1968):
QS = 2j / [a + b]
a = the number of species in habitat A
b = the number of species in habitat B
j: the number of common species in both habitats
To determine the frequency of mite species in individual sites, the coefficient of constancy (frequency of occurrence) index (C%) (Dajoz 1977) was used. According to C indexes, the species were classified as accidental, accessory, constant, euconstant, or close species associated with the considered habitat. C index values greater than 50% represent a close species associated with the considered habitat while those with values less than 25% represent accidental, 25.1–50% represent accessory, 50.1–75% for constant, and 75.1–100% euconstant species. C value was calculated using the following formula:
C = (Na / n) 100
Na = The number of samples containing species A
n = The total number of samples of all species
Jaccard index (JI) (Ludwig and Reynolds 1988) was used to determine the association for each pair of species (A and B). Interspecific associations between the 10 most predominant predaceous and phytophagous mite species were examined. The index was calculated using the following formula:
JI: a/ (a + b + c)
a = number of samples in which both species occur
b = number of samples in which only species A occur
c = number of samples in which only species B occur
d = number of samples in which neither A nor B occur
To examine the significance of obtained JI values, the Chi-square test was used. According to Ludwig and Reynolds (1988), if χ2 < 3.84, species A and B are significantly associated (*), if χ2 < 6.64, species A and B are very significantly associated (**). Chi-square values were calculated using the following formula (Ludwig and Reynolds 1988):
χ2 = N(ad-bc)2/ mnrs
m = a+b; n =c+d; r = a+c; s = b+d
N = total number of samples (a + b + c + d)
The expected frequency of both species in the samples was calculated using the following formula (Ludwig and Reynolds, 1988):
E(a) = f (B) (a+b) = F(A) (a+c)
F(A) = (a+b)/N
F(B) = (a+c)/N
There is a negative association when E(a) < c; a positive association when E(a) < c and no association when E(a) = c.JI (Ludwig and Reynolds 1988).
By association, it is meant the propensity of any pair of species to be found on the same leaf together. Any pair of species is positively associated if they occupy together more leaves than expected from random chance. On the contrary, any pair of species is negatively associated if they occupy together fewer leaves than expected from random chance.
During the study, a total of 3407 mite specimens were collected. A total of 42 species belonging to two super-orders were detected (Table 2). The mites were grouped into 2 orders, 12 families and 30 genera. Member of the family Phytoseiidae (16 species, 40.56%) were the most abundant mites collected, followed by Tenuipalpidae (1 species, 20.37%), Tetranychidae (4 species, 19.58%), Tydeidae (5 species, 5.58%), Stigmaeidae (2 species, 4.93%), Triophtydeidae (1 species, 2.76%), Iolinidae (3 species, 2.03%), Cunaxidae (2 species, 1.41%), Tarsonemidae (5 species, 1.26%), Eriophyidae (1 species, 0.88%), Cheyletidae (1 species, 0.44%) and Blattisociidae (1 species, 0.21%) (Table 2).
A total of 92.43% of all species were found on the neglected trees, while 7.57% were collected from the conventional orchards. Twenty-six species were found both on the neglected and conventional trees, 15 species were reported only on the neglected trees and only one species, Euseius stipulatus (Athias-Henriot) (Phytoseiidae), was found in just the conventional orchards (Table 2).
On neglected trees, the highest number of mites were found on apple (1883; 55.27%) followed by pear (517; 15.17%), quince (441; 12.94%), and loquat (308; 9.04%) (Table 3). In conventional orchards, the number of mites on apples (232; 6.81%) was higher than on pears (26; 0.76%) (Table 3).
The highest faunistic similarity was detected between the mite species on apple and quince in the neglected trees (QSAn/Qn = 0.825), and the lowest was found between pear and loquat (QSPn/Ln = 0.476). On the other hand, there was a low faunistic similarity between the mite complexes on apple and pear trees in the conventional orchards (QSAc/Pc = 0.313). When the conventional and neglected trees were compared, it can be clearly seen that there was a high faunistic similarity between the conventional apple trees and neglected apple, pear, quince, and loquat trees (QSAc/An, Pn, Qn, Ln = 0.537–0.794) (Table 4).
Among phytophagous mites, Amphitetranychus viennensis (Zacher) (Tetranychidae) was the predominant (21.32%) and most frequent (45%) species in the conventional orchards, whereas the second most abundant (9.21%) and common (15.5%) on the neglected trees (Tables 2, 5). It was a constant species (60%) in the conventional pear orchards, an accessory species on the neglected (34.2%), and conventional (40%) apple trees (Table 5). It was found on all pome fruit species sampled except loquat (Table 3).
Cenopalpus pulcher (Camestrini & Fanzago) was the only species identified from the family Tenuipalpidae. It was the most abundant (21.53%) and common (24.4%) phytophagous species on the neglected trees and the third most abundant (6.20%) and second most frequent (25%) in the conventional orchards (Tables 2, 5). It was an accessory species on the neglected (39.2%) and conventional (26.7%) apple trees (Table 5).
Other phytophagous mite species from the families Tarsonemidae and Eriophyidae showed highly overall lower abundance and frequency on pome fruit trees (Tables 2, 5). A total of three predatory mite species belonging to three genera of the family Stigmaeidae were detected. The most dominant (4.34%) and frequent (9%) species was Zetzellia mali (Ewing). It was the accessory species (53.3%) in the conventional apple orchards while it was proportionally less frequent on the neglected apple (20.6%). This predatory mite held less importance in terms of frequency (1.1–2.5%) on the other sampled neglected and conventional fruit trees. Moreover, it was not found in conventional pear orchards (Table 2, 5). Regarding the mite species from the family Phytoseiidae, the most abundant species, Phytoseius finitimus Ribaga and Transeius wainsteini (Gomelauri), (Table 2) showed the greatest overall constancy on pome fruits (Table 5). Both species were found on the neglected apple, pear, quince, loquat, and conventional apple trees, but not in the conventional pear orchards. Phytoseius finitimus was accessory species on the neglected apple (27.1%), loquat (48.9%), and conventional apple (40%) trees. Transeius wainsteini was constant in the conventional apple orchards (53.3%) and accessory on the neglected apple trees (38.7%). The rest of phytoseiids were less common (Table 5).
Other predatory species from the families Cunaxidae and Cheyletidae were also considerably less abundant and common on pome fruit trees.
Among tydeoid mites, the accidental species Tydeus triophthalmus (Oudemans) (20%) and Homeopronematus anconai (Baker) (20%) in the conventional pear orchards had the highest coefficient of constancy. Interestingly, any other tydeoid mite was not observed in these orchards. All other species held less importance on all sampled neglected and conventional trees (Table 5).
Associations between the ten most predominant predaceous and phytophagous mite species were examined (Table 6). A very highly significant positive association was obtained in sixteen pairs of species whereas a significant association was detected for seven pairs. Associations were found in the pair of eleven species of tetranychoid and predatory mites, pairs of six tetranychoid mite species, and pairs of six predatory mite species.
The pair of T. wainsteini-C. pulcher (JI = 0.289**) within predatory and tetranychoid mites, T. wainsteini – Z. mali (JI = 0.192**) within the predatory species, and A. viennensis-C. pulcher (JI = 0. 195**) within the tetranychoid mites had the highest interspecific association index (Table 6).
All the species detected during the current study were collected from different habitats in previous research in different regions of Turkey (Öksüz and Özman, 1999; Çobanoğlu 2000; 2004, Özman and Çobanoğlu 2001; İncekulak and Ecevit 2002; Akyazı and Ecevit 2003; Yanar and Ecevit 2005; 2008; Kasap and Çobanoğlu 2007; Kumral and Kovancı 2007; Kasap et al. 2013; Kasap et al. 2015; Kumral and Çobanoğlu 2015; Akyazı et al. 2017; 2022; Denizhan 2018; Soysal and Akyazı 2018; Altunç and Akyazı 2019; Çobanoğlu et al., 2020). Our results showed that pome fruits growing in agrochemical-free sites of Ordu were extremely rich in beneficial mite fauna, especially phytoseiids. İncekulak and Ecevit (2002) reported that spider mite populations were suppressed by predators in unsprayed apple orchards in Turkey (Amasya). Szabo et al. (2014) noted that phytoseiid mites were generally absent on nursery trees due to excessive use of insecticides and fungicides. Kasap (2011) and Kasap et al. (2019) indicated that in unsprayed apple orchards, the density of spider mites was very low because of the presence of predatory mites. Our results also are in agreement with Van de Vrie (1985), Amano and Chant (1990), Hardman et al. (1997), and Yanar and Ecevit (2008).
A high faunistic similarity indicates a non-selective distribution of mite species within pome fruit species. Unlike the conventional orchards, neglected trees generally exhibited strong and medium similarities in terms of mite fauna distribution. Contrary to conventional pear orchards, there was a high faunistic similarity between the conventional apple trees and all neglected trees. Stojnic et al. (2014) also found a great similarity between the cultivated and neglected apple orchards in Serbia. They added that the lowest similarity was found between the cultivated apple orchards and wild apples. Kumral and Kovancı (2007) found that the diversity of mites in conventional pome fruit orchards weakly resembled the diversity of agrochemical-free orchards in Turkey (Bursa). There were strong and medium relations among agrochemical-free orchards. Conventional orchards also generally exhibited strong and medium similarities in terms of mite fauna distribution.
The dominant phytophagous species in the conventional orchards was A. viennensis followed by Panonychus. ulmi (Koch) (Tetranychidae) and C. pulcher, while in the agrochemical-free sites the predominant species was C. pulcher followed by A. viennensis and Tetranychus urticae Koch (Tetranychidae). Yanar and Ecevit (2008) found that the dominant phytophagous mites in the sprayed apple orchard were A. viennensis and P. ulmi, whereas C. pulcher and also Eotetranychus uncatus Garman (Tetranychidae) were abundant in the unsprayed apple orchard in Turkey (Tokat). İncekulak and Ecevit (2002) also observed that the population of C. pulcher was able to reach high densities only in pesticide-free apple orchards in Turkey (Amasya). It was absent or its density was extremely low in the sprayed orchards. These data are confirmed by Çiftçi et al. (1985) who state that C. pulcher is very sensitive to pesticides. Contrary to our findings, Kumral and Kovancı (2007) found that A. viennensis was most frequently collected in the agrochemical-free deciduous orchard whereas P. ulmi and T. urticae were dominant in the conventional orchards in Turkey (Bursa). On the other hand, they noted that C. pulcher also was the dominant pest mite of agrochemical-free sites. In Serbia, it had been already mentioned that P. ulmi was the dominant pest mite species in cultivated and neglected apple orchards (Stojnic 2001). Kishimoto (2002) demonstrated that the dominant pest mites were A. viennensis in the agrochemical-free pear orchard, Panonychus citri (McGregor) (Tetranychidae) in the pesticide-free orchard, and T. urticae in the conventionally controlled pear orchard in Japan. Stojnic et al. (2014) declared that A. viennensis was accidental in the neglected apple orchards and accessory on wild apple trees.
Moreover, it was not determined any tetranychid mite species except A. viennensis in the conventional pear orchards in the current study. Stojnic et al. (2014) did not detect A. viennensis in the cultivated apple orchards. Interestingly, it was not detected any plant-parasitic mite species except C. pulcher on the neglected loquat trees in the current study. Hatzinikolis and Emmanouel (1987) reported loquat as a host for C. pulcher. It was also noted that this mite is an important pest on apple, quince, loquat, and pear by NAPPO (2008), Biosecurity Australia (2009), Beard et al (2012).
Phytoseius finitimus was the most abundant and common predatory species on pome fruits, followed by T. wainsteini and Z. mali. It is a very common phytoseiid species on pome fruit trees in Turkey. It was detected on apple trees in Sakarya, Giresun (Swirski and Amitai 1982), Ankara, Adapazarı, Niğde, Tokat, Burdur (Düzgüneş and Kılıç 1983), Gümüşhane, Bursa, İstanbul, Nevşehir, Isparta, Konya, Tokat (Çobanoğlu 1993d) and Amasya (İncekulak and Ecevit 2002), on apple, quince, medlar in Çanakkale and Balıkesir (Kasap et al. 2013), on persimmon in Ordu (Akyazı et al. 2017) in Turkey. It was also found commonly in Europe's apple orchards. (Nicotina 1996; Papaioannou-Souliotis et al. 1999; Kreiter et al. 2000; Ragusa and Tsolakis 2000). In the present study, it was generally collected from agro-chemical free sites. Moreover, it was not detected in conventional apple orchards. These data are in agreement with those of Duso and Vettorazzo (1999), who declared that P. finitimus proved to be susceptible to various pesticides.
Our findings showed that T. wainsteini was generally found on the neglected trees, especially apple, rather than in conventional sites. So far, T. wainsteini has been detected on rosehip (Faraji et al. 2011), persimmon (Akyazı et al. 2016), some vegetables (Soysal and Akyazı 2018) and stone fruits (Altunç and Akyazı 2019) in Turkey. Rahmani et al. (2010) found it on wild apple (Malus sp.) in Fandogloo. Tajmiri et al. (2014) detected T. wainsteini as dominant species in the plum orchards, adjacent raspberry hedgerows, and dominant orchard floor vegetation in Northern Iran (Guilan province).
The third most abundant and common predatory mite, Z. mali, was found in lower proportion on the agrochemical-free sites. Our result is in agreement with Kasap and Çobanoğlu (2006) and Kasap et al. (2019). They detected that Z. mali was the most abundant predatory mite species associated with B. rubrioculus in Van (Turkey) and with P. ulmi in Çanakkale (Turkey) in sprayed apple orchards. Abroad, it was found in the sprayed and unsprayed orchards (Woolhouse and Harmsen 1985; Strickler et al. 1987; Thistlewood 1991; Croft 1993). Santos (1976) and Clements and Harmsen (1993) found that Z. mali can have a high reproduction rate on P. ulmi.
Considering together phytoseiid and tetranychoid species, it was detected that T. wainsteini had a greater tendency to be found together with C. pulcher, A. viennensis and T. urticae (positive association). The pair of E. finlandicus – B. rubrioculus was also found very significantly associated. Significant positive associations were also found for the pairs of Typhlodromus rapidus Wainstein & Arutunjan (Phytoseiidae) – Bryobia. rubricolus(Scheuten) (Tetranychidae),T. rapidus – A. viennensis, and P. finitimus – P. ulmi. Transeius wainsteini was collected among the P. ulmi and Aceria sp. (Eriophyidae) populations on wild apple trees by Rahmani et al. (2010). On the other hand, it was found associated with T. urticae in hazelnut orchards and sunflowers by them. Euseius spp. are classified as Type IV Lifestyle – pollen feeding generalist predators by McMurtry et al. (2013). Euseius finlandicus is known to feed on tetranychid, eriophyid, tyroglyphid and tarsonemid species, pollen, fungal hyphae and spores, eggs and larvae of insects, honeydew, and plant liquids (Schausberger 1992; Kostiainen and Hoy 1994; Abdallah et al. 2001). Typhlodromus rapidus Wainstein & Arutunjan was detected on apple and oak trees in Russia (Wainstein and Arutunjan 1968), Betula spp., and Quercus spp. in Latvia (Salmane and Petrova 2002), Corylus sp. in İzmit (Çobanoğlu 1997) and walnut trees in Samsun in Turkey. Species in the genus Typhlodromus are classified as Subtype III-a – generalist predators living on pubescent leaves by McMurtry et al. (2013). Phytoseius finitimus had also positive and very significant associations with P. ulmi. It is a generalist phytoseiid mite (Pappas et al. 2013; Tixier et al. 2017). Its food range includes tetranychids, eriophyoids, and pollen (Nomikou et al. 2001; Momen and El-Borolossy 2010).
Within predatory species complex, the pair of Z. mali – T. wainsteini had the greatest tendency to be found together. The pairs of E. finlandicus – T. rapidus and T. rapidus – Z. mali had also very highly positive associations. It is known that Z. mali may feed on other predator mite eggs (Kain and Nyrop 1995). Croft (1993) noted that it can prey on eggs of the predatory phytoseiid mites Galendromus (Galendromus) occidentalis (Nesbitt) and Typhlodromus (Typhlodromus) pyri Scheuten and other Z. mali. Schausberger (1997) declared that E. finlandicus showed the great tendency to interspecific predation on motile immatures of T. pyri and Kampimodromus aberrans (Oudemans) (Phytoseiidae).
Considering only the tetranychoid mites, positive and very significant associations were observed for the pair A. viennensis – B. rubrioculus, A. viennensis – P. ulmi, C. pulcher – A. viennensis, C. pulcher – B. rubrioculus, and C. pulcher – T. urticae. As far as we know, these are previously unstudied.
Our results demonstrate a strong effect of agrochemicals on the diversity and distribution of mite species. The main conclusion can be drawn that richer beneficial mite fauna occurs on pome fruit trees in the agrochemical-free sites compared to the conventional orchards. In addition, dominant phytophagous and predatory species of agrochemical-free sites and conventional orchards were different. Moreover, some species could only be found in the commercial orchards, whereas some only in neglected ones, and some in both areas. Very significantly positive association indexes were found for mite pairs within the predatory and phytophagous species complex. The finding may help to determine the potential predatory species for the applied biological control approaches of phytophagous mites in the pome fruit orchards. Finally, the economic importance of phytophagous mites detected on the pome fruit trees in the Ordu region can be considered to be negligible because these mites are vulnerable to predatory mites and pesticides.
We are grateful for the financial support of this work to the Ordu University Scientific Research Project Coordination Unit (ODUBAP) (Project No: TF-1510). The authors also very much appreciate the help of Dr. Farid Faraji (University of Amsterdam, The Netherlands), Prof. Dr Serge Kreiter (Institut Agro Montpellier, UMR CBGP, France), Prof. Dr Eddie A. Ueckermann (North-West University, South Africa), Prof. Dr Owen Seeman (Collection Arachnida Queensland Museum, Australia), Dr. Philippe Auger (French National Institute for Agricultural Research, France), Dr. Mariusz Lewandowski (Warsaw University of Life Sciences, Poland), and Prof. Dr Antonio C. Lofego (Universidade Estadual Paulista, Brazil) in the confirmation of species identifications.
Part of this research was presented at the 8th Plant Protection Congress with international participation held between 24-28 August 2021 in Turkey and published as an abstract in the abstracts book. This manuscript is a part of the first author's M. Sc. thesis.