Population dynamics of the citrus nematode Tylenchulus semipenetrans Cobb, 1913 in an infested orchard in Fars province, southern Iran

doi:10.21203/rs.3.rs-3585538/v1

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Population dynamics of the citrus nematode Tylenchulus semipenetrans Cobb, 1913 in an infested orchard in Fars province, southern Iran

https://doi.org/10.21203/rs.3.rs-3585538/v1

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The citrus nematode Tylenchulus semipenetrans Cobb, 1913 is one of the most important threats limiting the growth of citrus trees around the world. In recent years, efforts have been made to control this pathogen. Determining the number of generations and population peaks of this nematode is necessary for its control. This study was conducted to investigate the fluctuations of the citrus nematode population in Fasa, an important citrus growing city in Fars province, southern Iran, between 2018 and 2019. The results showed that the lowest levels of soil nematodes including second-stage juveniles (J2s) and males, and root nematodes (eggs, juveniles and females) occurred in July. However, the peak of population levels were different for root and soil nematodes. For root nematodes, two peaks were recorded in late May and November, while for soil nematodes, two peaks were recorded in late May and December. From the results, the nematode population in the roots (especially the female ones) was less subject to fluctuations compared to the soil population. In most samples, the nematode populations in the roots decreased with increasing distance from the tree trunk. Overall, the results showed that there are two population peaks per year, suggesting that two generations of the citrus nematode occur in Fasa orchards. From a management perspective, the results of this study can be generalized to all citrus orchards with the same geographic and environmental factors.

Population dynamics. Citrus nematode. Tylenchulus semipenetrans. Fasa city

Citrus is one of the most economically important crops in the world. With a total production of 3,865,098 tons of citrus, Iran is among the top 10 citrus producing countries in the world (Food and Agriculture Organization of the United Nations 2023). Fars province produces about 24.47% of the total citrus in Iran and is considered the second largest citrus producer after Mazandaran province in the north (Ahmadi et al. 2021). More than 40 species of plant parasitic nematodes [PPN] have been reported from citrus orchards around the world. However, only a few species can cause economically serious losses to citrus trees (Timmer et al. 2000). The slow decline of citrus plants is caused by infection with Tylenchulus semipenetrans and Radopholus citrophilus (Duncan 2005). The citrus nematode is the most common PPN of citrus, affecting about 80 species or cultivars of the genus Citrus (Timmer et al. 2000; Ahmad et al. 2004). To date, three biotypes of the citrus nematode are known worldwide, which differ in their host range (Inserra et al. 1980; Verdejo-Lucas et al. 2003; Inserra et al. 1994). The life span of the citrus nematode varies depending on environmental and edaphic conditions and ranges from four to eight weeks (Van Gundy 1964; Pretorius 2017). T. semipenetrans has spread across both northern and southern provinces (especially Fars) of the country at various population levels. Studies are available reporting the frequent occurrence of this pathogen in citrus orchards of Fars province (Izadpanah and Saffarian 1968; Abiverdi et al. 1970; Minassian and Moadab 1970; Ayazpour and Ghanaatian 2004; Tanhamaafi and Damadzadeh 2008). Nematode-infected seedlings are the most important factor for the spread of the nematode in the world (Timmer et al. 2002).

Crop losses caused by the citrus nematode reach 90% in some heavily infested areas (Baines et al. 1962; Duncan 2005). The economic threshold for nematode infestation depends on the nematode reproduction rate, host and environmental factors (Duncan 1999), rootstock susceptibility (Duncan 1999), the cost of nematode management (Sorribas et al. 2008), climatic conditions (O 'Bannon 1968; Bello et al. 1986; Navas et al. 1992; Timmer et al. 2000), and soil physicochemical properties such as moisture (Duncan and Eissenstat 1993; Sorribas et al. 2000), density, texture (Baines et al. 1962; Martin et al. 1963; Duncan 2005; Sorribas et al. 2008; Rashidifard et al. 2015b), organic matter, salinity and soil acidity (Timmer et al. 2000; Sorribas et al. 2008; Salahi Ardakani et al. 2014). In addition, seasonal fluctuation of the citrus nematode populations varies with environmental and geographic conditions.

The use of nematode-resistant or -tolerant citrus rootstocks is considered the most promising and sustainable measure to prevent damage from this pathogen (Kaplan 1981; Lee et al. 1999; Ling et al. 2000; Galeano et al. 2003). However, replacing susceptible rootstocks with resistant cultivars is an expensive and time-consuming process. Therefore, monitoring nematode population density in the rhizosphere and roots of infested citrus trees can lead to obtaining information about the peak of the population and consequently implementing IPM strategies at the right time. In northern Iran, the citrus nematode population peaks in summer and declines to lower levels in autumn and winter (Tanhamaafi and Damadzadeh 2008). A preliminary study conducted in Khafr region of Fars province revealed that the citrus nematode has two generations per year. It was demonstrated that the life cycle of T. semipenetrans begins with egg laying in the soil in mid-May (Sharafeh 1972). Moreover, the peak of the citrus nematode population in Kerman province was observed in autumn, while the minimum was recorded in spring (Rashidifard et al. 2015b). Despite the remarkable importance of T. semipenetrans in the country, its life cycle and biology have hardly been studied. The biology and population dynamics of this pathogen in citrus-growing areas of Iran have not been extensively studied. Therefore, this study investigated the biology and monthly fluctuations of citrus nematode populations in the roots and rhizosphere of infested citrus trees in Fasa. The correlation between nematode numbers and temperature was also investigated.

Survey area

A 2-ha nematode-infested citrus orchard was selected as part of a preliminary sampling of several areas in Fasa. The orchard trees used for the study were drip irrigated and planted approximately 5 m × 6 m apart. Three 10- to 12-year-old orange trees (Citrus sinensis L. var. Valencia) were sampled to ensure an approximately even distribution of the selected trees in the orchard (828: 28°95′54.5′′N & 53°60′14.2′′E, 829: 28°95′60.3′′N & 53°60′19.3′′E and 830: 28°95′58.1′′N & 53°60′16.8′′E). Monthly samples were collected from the roots and rhizosphere for 14 months. Samples were collected from the soil at a depth of 20 or 30 cm below each of the selected trees. To minimize sampling errors and allow simultaneous sampling, trees were selected close to each other in an orchard. The experiment was conducted randomly in three replicates (tree). The physicochemical properties of the soil were measured using a composite sample of three trees studied.

Species identification

After extraction, the nematodes were fixed with hot FAA (4:1), transferred to anhydrous glycerol, and microscopic preparations were made. Identification was based on morphological and morphometric characteristics and using nematode identification keys (Inserra et al. 1988; Tanha Maafi et al. 2012), Dino Capture software, and a light microscope. To visualize root populations, nematode-infested roots were stained with acid fuchsine. To confirm the results of the morphological and morphometric studies, genomic DNA was extracted and the ITS fragment and D2–D3 expansion segments of 28S were sequenced.

Sampling

Sampling was done by taking two composite samples from both sides of the drippers as hypothetical inner (A: four subsamples) and outer (B: six subsamples) circles under each tree canopy (Rumiani et al. 2021). The subsamples were 10–15 cm in diameter and 20–30 cm deep. Composite samples A and B were taken at a radius of 60 and 120 cm around the tree trunk, respectively. The subsamples in each circle were mixed and gently homogenized, then approximately 2 kg of soil (1550 cm³) was collected, placed in separate labeled bags, and transported to the laboratory.

Nematode extraction and counting

Soil nematodes, including males and second-stage juveniles (J2s), were extracted using the tray method (Whitehead and Hemming 1965). After 48 hours, the nematodes were collected, transferred to a counting dish, and counted under a stereomicroscope in three replicates. To estimate the root nematode population, including eggs, juveniles and females, the roots of each composite sample were removed from the soil by sieving and washed thoroughly. Moisture from the root samples was removed with tissue paper and then chopped. Nematodes were extracted from 5 g of a subsample using a mixing container with 0.05% NaOCl solution. The roots were mixed at high speed for 30 seconds (in two consecutive 15-second intervals). To remove root debris, the nematode-containing suspension was sieved through a 200-mesh sieve and placed on another 500-mesh sieve (to concentrate the collected nematodes) and then diluted with water. To count the root nematodes, the suspension was mixed thoroughly and 1 ml of the obtained mixed solution was used for counting. The counting was repeated three times and expressed per 5 g of fresh root tissue (McSorley et al. 1984; Sorribas et al. 2008). Finally, the mean number of extracted soil and root nematodes from the two composite samples (A & B) was considered as the final nematode population per citrus tree.

Soil temperature

Due to the geographic distance of the sampling site, it was too time consuming to record daily soil temperature. Therefore, soil temperature was estimated using mean monthly air temperature data and empirical models (Islam et al. 2015). The equations y = 0.9x + 3.83, y = 0.842x + 6.224 and y = 0.708x + 9.871 were used to estimate soil temperature at three depths of 5, 10 and 20 cm, respectively (Islam et al. 2015) where x and y are the monthly mean air temperature (Farsmet 2020) and the monthly mean ground temperature of Fasa, respectively. Microsoft® Excel® 2013 (15.0.4420.1017) software was used to draw the graphs.

The studied populations were identified as T. semipenetrans basis on morphological and morphometric characteristics and identification keys (Inserra et al. 1988; Tanha Maafi et al. 2012). In addition, the sequencing results (ITS fragment and D2– D3 expansion segments of 28S rRNA) confirmed our identification. NCBI blast showed that the sequences of the present study differed from corresponding sequences of the T. semipenetrans populations deposited in the database by only a few nucleotides and had an identity of more than 99%. The feeding apparatus, including the stylet and pharyngeal region of adult males was poorly developed and hardly visible compared to the females.

Based on the physicochemical analysis, the soil under the canopy of the test trees was classified into the group of silt-loam soils with 25.08% sand, 57.64% silt and 17.28% clay. The organic matter content and pH of the soil were 1.96% and 7.56, respectively, and the electrical conductivity (EC) was 1900 µmhos/cm. The test soil contained 71.6 mg/kg phosphorus, 15.26 mg/kg potassium, 55.00 mg/kg calcium carbonate, 4.3 mg/kg calcium, 7.3 mg/kg magnesium, 125.41 milliequivalents (meq)/liter sodium, 1.05 mg/kg zinc, 3.5 mg/kg iron, 1.26 mg/kg copper and 2.20 mg/kg manganese.

Monitoring the citrus nematode population showed fluctuation of root and rhizosphere nematodes under the canopy of citrus trees. The lowest number of nematodes in the soil was recorded in July (931 J2s/ 100 ml soil), while the highest numbers were recorded in two separate peaks in May (3900/ 100 ml soil) and December (5403/ 100 ml soil) (Fig. 1). Root nematodes populations (5 g fresh roots) declined in June, July and August. The peak of female population was recorded in late May and October (1561 and 3582 females per 5 g of root, respectively). Also, the highest number of eggs and juveniles in the root was observed in late May (3178 and 3013, respectively) and November (19044 and 15486, respectively) (Fig. 2). The nematode data showed that in most cases, the average number of nematodes in the roots and soil was higher in the inner part of the irrigation drip line (A circle) than in the outer part (B circle) [the A and B nematode data are not presented separately here].

Mean monthly air temperature in the warmest (July) and coldest months during 2019–2020 in Fasa was found to be 31.9 and 8°C, respectively (Farsmet 2020). Mean soil temperature at a depth of 5 to 20 cm under a tree canopy was also estimated to be 32.7 and 13.2°C in the warmest and coldest months, respectively (Islam et al. 2015). Soil temperature was estimated to be 29°C for the first peak of the nematode population in the soil and roots (May). For the second peak of the soil and the root populations (December & November), the above values were 13.2°C and 14.8°C, respectively (Fig. 3).

The citrus nematode can reproduce in citrus growing areas around the world, and environmental conditions and soil physico-chemical properties significantly affect its reproduction rate (Baines et al. 1962; O ‘Bannon 1968; Martin et al. 1963; Bello et al. 1986; Navas et al. 1992; Duncan and Eissenstat 1993; Sorribas et al. 2000; Duncan 1999; Timmer et al. 2000; Duncan 2005; Sorribas et al. 2008; Salahi Ardakani et al. 2014; Rashidifard et al. 2015a). Therefore, the seasonal dynamics of populations vary according to environmental conditions and region, and should be studied separately in each region.

The results of the present study showed that root nematodes infestation and populations decreased when soil temperature was above 30°C. This is consistent with the research showing that the citrus nematode invading citrus roots, and thus their populations, decreased with an increase in soil temperature above 30°C (O’Bannon et al. 1966). The higher temperatures in the summer months, especially in June and July, were not conducive to J2s penetration into the roots, so the nematode population decreased drastically in the present study. However, soil moisture content did not significantly affect T. semipenetrans, especially the female population in the roots. Because the citrus nematode co-evolved with deep-rooted woody plants, these plants could support the nematodes during the dry season by hydraulic upwelling via the root xylem from deep in the soil to the drier surface soils (Duncan and El-Morshedy 1996). In this study, the nematode does not suffer water deficit along the rhizoplane even when the soil is very dry overall. On the other hand, juvenile and male nematodes cannot survive in soil under drought conditions. Duncan and El-Morshedy (1996) found that almost no eggs of T. semipenetrans hatched after 23 and 37 days of uniform drought. Other nematologists have also demonstrated that adequate soil moisture is required for nematode eggs to hatch (Timmer et al. 2000). Therefore, along with high soil temperature, inadequate moisture is considered to be one of the causes of the sharp decline in the nematode population (especially eggs, J2s and males) during the summer in the present study. The marked decrease in the nematode population in June suggests the roots of the citrus plants were affected to a much lesser extent by the nematodes that had been infesting them. As a result, the increase in root population, especially the female, was not exponential in the following months [July & August] (Fig. 2).

The citrus nematode population peaked twice during this study, which can be attributed to nematode generations. The first generation (or peak) occurred in spring, and the second, which was higher in population, occurred in late autumn and early winter (Figs. 1 and 2). Soil temperature was 23°C during the first peak and 13–14°C during the second (Fig. 3). However, the peak of T. semipenetrans population in soil was recorded in July and August in northern Iran and the lowest in autumn and winter (Tanhamaafi and Damadzadeh 2008). The timing of the peak of nematode populations varies. However, the soil temperature at the time of the first peak in our study and the peak of the citrus nematode population in the north were almost the same (23°C) (Figs. 1 and 2; Table 1). Another difference between the present survey and the northern study (Tanhamaafi and Damadzadeh 2008) was the number of peaks, which was two and one, respectively. The main reason for this discrepancy is probably related to environmental conditions, especially temperature. The average winter soil temperature in the Fasa region was higher (14°C) than in the study carried out in the north (6.5°C) (Tanhamaafi and Damadzadeh 2008; Farsmet 2020). Thus, suitable basic conditions for the reproduction of the nematode were present, so that the nematode had time to base its second peak in the present study.

Table 1

Estimation of mean monthly soil temperature at a depth of 5, 10 and 20 cm, using mean monthly air temperature in Fasa region, Fars province, from 2019 to 2020
Temperature	Time (month)
Temperature	Jan-19	Mar-19	Apr-19	May-19	Jun-19	Jul-19	Aug-19	Sep-19	Oct-19	Nov-19	Dec-19	Jan-20	Feb-20
AT	9.8	15.4	20.5	27.8	31.9	31.1	28.5	23.9	15.4	10.0	8.0	8.1	12.2
ST 5 cm	12.7	17.7	22.3	28.9	32.5	31.8	29.5	25.3	17.7	12.8	11.0	11.1	14.8
ST 10 cm	14.5	19.2	23.5	29.6	33.1	32.4	30.2	26.3	19.2	14.6	13.0	13.0	16.5
ST 20 cm	16.8	20.8	24.4	29.6	32.5	31.9	30.0	26.8	20.8	17.0	15.5	15.6	18.5
Mean ST	14.6	19.2	23.4	29.3	32.7	32.0	29.9	26.2	19.2	14.8	13.2	13.3	16.6
AT: Monthly air temperature (mean) in Fasa region retrieved from Fars Meteorological Office (2022).
ST: Estimated soil temperature (monthly mean) at a depth of 5, 10 and 20 cm using the equations y = 0.9x + 3.83, y = 0.842x + 6.224, and y = 0.708x + 9.871, respectively (Islam et al. 2015).

It was also reported that the population of citrus nematode increases in winter. A study conducted in South Africa showed that in areas with summer rains, the J2 population of the citrus nematode peaked after each rooting period in spring, summer and autumn. However, in areas with winter precipitation (e.g., Fasa city), seasonal changes, including temperature, are more effective than the timing of rooting. In such regions, the J2 population begins to increase with the onset of precipitation and then peaks in winter (Le Roux 1995).

The results of the present study showed that the slope of the citrus nematode population line was positive (Figs. 1 and 2). This means that the nematode population may increase annually followed by a slow decline, the well-known nematode symptom, occurs over time.

Citrus root proved to be a safe harborage for nematodes during environmental changes, especially extreme moisture (Le Roux 1995). The lower fluctuation of the root nematode population compared to soil nematodes (Fig. 3) suggests that root nematodes are less affected by environmental conditions such as drought (Duncan and El-Morshedy 1996). The results of the present work showed that the citrus nematode population decreased with increasing distance from the tree trunk, which is consistent with other studies (Duncan 1986). A direct relationship between nematode counts and root density (Duncan et al. 1993) was also confirmed by the results of the present study.

As claimed by other researchers, hatching of the citrus nematode eggs in vitro takes 12–24 days. After that, the hatched J2s were attracted to the root exudates (Timmer et al. 2000). After completion of the juvenile stages and formation of immature females, invasion of the root interior and formation of nurse cells occurs. The egg-to-egg life cycle of T. semipenetrans lasts 4–8 weeks (Van Gundy 1964; Pretorius 2017). Previous studies have shown that males do not feed (Timmer et al. 2000). Therefore, in the present study, degeneration of stylet and pharynx was observed in males.

From the results, the soil temperature was above 30°C in summer (Table 1). Furthermore, the temperature tolerance of most PPNs is low, and they become inactivated at high temperatures (Dwinell 1990). Therefore, the oversummering of PPNs in warm climates such as the Fasa region seems to be more important than their overwintering, as shown in the present study, where a low population of nematodes occurred in summer (Fig. 3). T. semipenetrans can survive as eggs in the absence of citrus trees. In the absence of a host, T. semipenetrans has been detected in the soil for up to nine years (Van Gundy et al. 1967).

It appears that the life cycle of the citrus nematode in the Fasa region begins when soil temperatures fall in late summer. Then, surviving eggs from the summer hatch and in September, favorable conditions such as root exudates attract the J2s to the roots of citrus trees. As mentioned earlier, the life cycle of this nematode lasts between one and two months (Van Gundy 1964). Thus, invading nematodes complete their life cycle in the roots of citrus plants after September. Consequently, the peak population of root nematodes (so-called second generation) was detected in the following months [November/December] (Fig. 3). In November, however, not only did the soil population not increase significantly, but in some cases it even decreased slightly (rep. B), indicating that the nematode population had invaded the roots at this time. After the females matured, the root nematodes laid their eggs in the soil, so most of the soil nematodes were seen in December (Fig. 1). The newborn individuals then re-invade the citrus roots in December and January. It takes about two months for this generation to complete. Finally, the peak of the total nematode population (referred to as the first generation) may be reached in May (Figs. 1 and 2).

In summary, the citrus nematode, T. semipenetrans, is capable of completing its life cycle within two months and possibly producing multiple generations per year. However, the environmental conditions in Fasa, Fars province were not favorable for the completion of all cycles. Therefore the nematode completes only two generations per year. The peak population of the first generation occurs in late May and the second in November/December. Therefore, it is strongly recommended that management measures against this pathogen be implemented during these two periods. The results of this study can be implemented and applied in citrus orchards in areas with the same or similar geographic and environmental conditions.

Acknowledgement

The authors greatly acknowledge Shiraz University for providing financial support to carry out this work.

Conflict of Interest Authors have no potential conflict of interest pertaining to this submission to journal of plant diseases and protection

Funding This study was financially supported by Department of Plant Protection, School of Agriculture, Shiraz University

Abiverdi C, Izadpanah K, Sharafeh M (1970) Plant parasitic nematodes associated with citrus decline in southern Iran. Plant dis Rep 56: 186-188
Ahmad MS, Mukhtar T, Ahmad R (2004) Some studies on the control of citrus nematode (Tylenchulus semipenetrans) by leaf extracts of three plants and their effects on plant growth variables. Asian J Plant Sci 3: 544-548
Ahmadi K, Ebadzadeh H, Hatami F, Afruzi S, Taleghani R, Yari S, Kalantari M (2021) Iranian Agricultural Statistics in 2019-2020 Crop Years, Part III Gardening Products. Agricultural ministry press, Tehran
Ayazpour K, Ghanaatian A (2004) Determination of root parasite nematodes of citrus in Jahrom (Fars province, Iran). Master’s thesis, Islamic Azad University of Jahrom
Baines RC, Martin JP, De Wolf TA, Boswell SB, Garber MJ (1962) Effects of high doses of D-D on soil organisms and the growth and yield of lemon trees. Phytopathology 52: 723 (abstract)
Bello A, Navas A, Belart C (1986) Nematodes of citrus groves in the Spanish Levanter Ecological study focused to their control. In: Cavalloro R, Di Martino E (ed) Integrated Pest Control in Citrus groves, 1st edn. Balkema Publishing, South Africa, pp 217-226
Duncan LW (1986) The spatial distribution of citrus feeder roots and of the citrus nematode, Tylenchulus semipenetrans. Revue Nématol 9: 233–240
Duncan LW (1999) Nematode diseases of citrus. In: Timmer LW, Duncan LW (ed) Citrus Health Management, Volume 1. American Phytopathological Society Press, California, pp 136-148. https://doi.org/10.1079/9780851997278.0437
Duncan LW (2005) Nematode parasites of citrus. In: Luc M, Sikora RA, Bridge J (ed) Plant Parasitic Nematodes in Subtropical and Tropical Agriculture, 2nd Edition. Wallingford, UK, pp 437-466
Duncan LW, Eissenstat DM (1993) Responses of Tylenchulus semipenetrans to citrus fruit removal: implications for carbohydrate competition. J Nematol 25: 7–14
Duncan LW, El-Morshedy MM (1996) Population changes of Tylenchulus semipenetrans under localized versus uniform drought in the citrus root zone. J Nematol 28(3): 360
Duncan LW, Graham JH, Timmer LW (1993) Seasonal pattern associated with Tylenchulus semipenetrans and Phytophtora parasitica in the citrus rhizosphere. Ecol Epidemiology 83: 573-581
Dwinell ID (1990) Heat treatment southern yellow pine lumber to eradicate Bursaphalenchus xylophilus. Nematologica 36: 346-347
Fars Meteorological Bureau (2020) Farsmet: agricultural meteorology. http://www.farsmet.ir/DM/Files/files/9.jpg. Accessed 04 August 2022
Food and Agriculture Organization of the United Nations (2023) FAOSTAT Crops and livestock products. https://www.fao.org/faostat/en/#compare. Accessed 12 April 2023
Galeano M, Verdejo-Lucans S, Sorribas FJ, Ornat C, Forner JB, Alcaide A (2003) New citrus selections from Cleopatra mandarin Poncirus trifoliata with resistance to Tylenchulus semipenetrans Cobb. Nematology 5: 227-234
Inserra RN, Duncan LW, O'Bannon JH, Fuller SA (1994) Citrus nematode biotypes and resistant citrus rootstocks in Florida. Nematology 205: 1-4
Inserra RN, Vovias N, O'Bannon JH (1980) A classification of Tylenchulus semipenetrans biotypes. J Nematol 12: 283-287
Inserra RN, Vovlas N, O'Bannon JH, Esser RP (1988) Tylenchulus graminis n. sp. and T. palustris n. sp. (Tylenchulidae) from native flora of Florida, with notes on T. semipenetrans and T. furcus. J Nematol 20: 266-287
Islam KI, Khan A, Islam T (2015) Correlation between atmospheric temperature and soil temperature: A case study for Dhaka, Bangladesh. Clim Atmos Sci 5(03): 200
Izadpanah K, Safarian A (1968) Possible role of citrus nematode (Tylenchulus semipenetrans Cobb) in the citrus decline in southern Iran. In: Proceeding of the 1st National Congress of plant protection of Iran, September, 1968. Tehran, Iran. Iranian Research Institute of Plant Protection, pp 40-41
Kabata-Pendias A (2000) Trace Elements in Soils and Plants. CRC Press, Florida
Kaplan DT (1981) Characterization of citrus rootstock responses to Tylenchulus semipenetrans (Cobb). J Nematol 13: 492-498
Le Roux HF (1995) Control of the citrus nematode in South Africa. Dissertation, Pretoria University
Lee RF, Lehman PS, Navarro L (1999) Nursery practices and certification programs for bud wood and rootstocks. In: Timmer LW, Duncan LW (ed) Citrus Health Management, Volume 1. American Phytopathological Society Press, California, pp 35-46. https://doi.org/10.1079/9780851997278.0437
Ling P, Duncan LW, Deng Z, Dunn D, Hu X, Huang S, Gmitter FG (2000) Inheritance of citrus nematode resistance and its linkage with molecular markers. Theor Appl Genet 100: 1010-1017
Martin JP, Van Gundy SD (1963) Influence of soil phosphorous level on the growth of sweet orange seedlings and the activity of the citrus nematode (Tylenchulus semipenetrans). Soil Sci 96: 128-135
McSorley R, Parrado JL, Dankers WH (1984) A quantitative comparison of some methods for the extraction of nematodes from roots. Nematropica 14: 72-84
Minassian V, Moadab H (1970) The occurrence and distribution of citrus nematode Tylenchulus semipenetrans Cobb in Khuzestan, Iran. Iran J Plant Pathol 6: 25-28. (In Persian with English summary)
Navas A, Nombela G, Bello A (1992) Caracterización de la modalidad de distribución de Tylenchulus semipenetrans en elevate Española. Nematropica 22: 205-216
O’Bannon JH (1968) The influence of an organic soil amendment on infectivity and reproduction of Tylenchulus semipenetrans on two citrus rootstocks. Phytopathology 58: 597–601
O’Bannon JH, Reynolds HW, Leathers CR (1966) Effects of temperature on penetration, development, and reproduction of Tylenchulus semipenetrans. Nematologica 12: 483–487
Pretorius MC, Le Roux HF (2017) Nematode pests of citrus. In: Fourie H, Spaull VW, Jones RK, Daneel MS, De Waele D (ed) Nematology in South Africa: a view from the 21st century, Springer International Publishing, New York, pp 311-32
Rashidifard M, Shokoohi E, Hoseinipour A, Jamali S (2015a) Tylenchulus semipenetrans (Nematoda: Tylenchulidae) on pomegranate in Iran. Australas Plant Dis Notes 10(1): 1-6
Rashidifard M, Shokoohi E, Hoseinipour A, Jamali S (2015b) Distribution, morphology, seasonal dynamics, and molecular characterization of Tylenchulus semipenetrans from citrus orchards in southern Iran. Biologia 70: 771-781
Rumiani M, Hamhehzarghani H, Karegar A, Ghaderi R (2021) Optimization of citrus tree sampling pattern for estimating population of citrus nematode in the soil of infested orchards in Fars province, southern Iran. Crop Prot 142 105523. https://doi.org/10.1016/j.cropro.2020.105523
Salahi Ardakani A, Tanha Mafi Z, Mokaram Hesar A, Mohammadi Goltappeh E (2014) Relationship between soil properties and abundance of Tylenchulus emipenetrans in citrus orchards, Kohgilouyeh va Boyerahmad province. J Agric Sci Technol 16: 1699-1710
Sharafeh M (1972) Preliminary study on population dynamics of the citrus nematode, Tylenchulus semipenetrans Cobb, in Khafr, an important citrus growing region of Fars. Entomol Phytopathol Appl 33: 26-30
Sorribas FJ, Verdejo-Lucas S, Forner JB, Alcaide A, Pons J, Ornat C (2000) Seasonality of Tylenchulus semipenetrans Cobb and Pasteuria sp. in citrus orchards in Spain. J Nematol 32: 622-632
Sorribas FJ, Verdejo-Lucas S, Pastor J, Ornat C, Pons J, Valero J (2008) Population densities of Tylenchulus semipenetrans related to physicochemical properties of soil and yield of clementine mandarin in Spain. Plant Dis 92: 445-450
Tanha Maafi Z, Amani M, Stanley JD, Inserra RN, Van Den Berg E, Subbotin SA (2012) Description of Tylenchulus musicola sp. n. (Nematoda: Tylenchulidae) from banana in Iran with molecular phylogeny and characterization of species of Tylenchulus Cobb, 1913. Nematology 14: 353-369
Tanha Maafi Z, Damadzadeh M (2008) Incidence and control of citrus nematode Tylenchulus semipenetrans Cobb in north of Iran. Nematology 10: 113-122
Timmer LW, Garnsey SSM, Graham JH (2000) Compendium of citrus diseases. The American Phytopathological society
Van Gundy SD, Bird AF, Wallace HR (1967) Ageing and starvation of larvae of Meloidogyne javanica and Tylenchulus semipenetrans. Phytopathology 57: 571–599
Van Gundy SD, Martin JP, Tsao PH (1964) Some soil factors influencing reproduction of the citrus nematode and growth reduction of sweet orange seedlings. Phytopathology 54: 294-299
Verdejo-Lucas S, Galeano M, Sorribas FJ, Forner JB, Alcaide A (2003) Effect on resistance to Tylenchulus semipenetrans of hybrid citrus rootstocks subjected to continuous exposure to high population densities of the nematode. Eur J Plant Pathol 109: 427–433
Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55: 25-38. https://doi.org/10.1111/j.1744-7348.1965.tb07864.x

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Population dynamics of the citrus nematode Tylenchulus semipenetrans Cobb, 1913 in an infested orchard in Fars province, southern Iran

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Abstract

Figures

Introduction

Materials and Methods

Survey area

Species identification

Sampling

Nematode extraction and counting

Soil temperature

Results

Discussion

Conclusion

Declarations

References

Status:

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