The Hidden Enemy

 Edward J. Sikora, Elizabeth A. Guertal, and Kira L. Bowen

Bermudagrass and bentgrass greens on golf courses sometimes show signs of poor vigor even when they have been carefully maintained. The likely culprits in these situations are plant parasitic nematodes, which AAES research has shown abound in numerous species and in large numbers in the soils of Alabama’s golf courses.

Nematodes are microscopic roundworms that often live in the soil and attack a wide range of host plants. Most nematodes that attack turfgrass are microscopic, slender, largely transparent, unsegmented roundworms (Figure 1). These nematodes live in the soil and feed on the roots of turfgrass, greatly reducing plant growth by damaging the root system (Figure 2). As many as 20,000 individuals can be found in one pint of soil.

Figure 1. Lance nematodes feeding in and on a grass root segment.

Figure 2. Spiral nematodes were commonly found in both hybrid bermudagrass and creeping bentgrass putting greens.

At least 10 genera of plant parasitic nematodes have been recovered in routine tests of soil from putting greens in Alabama. Many of these genera, at high population levels, can cause severe damage to greens. Putting greens on the more than 300 golf courses in Alabama are comprised of either hybrid bermudagrass or creeping bentgrass. Detailed information concerning the distribution, population levels, and economic importance of plant-parasitic nematodes associated with putting greens in Alabama is lacking. An AAES study was conducted to determine which nematode genera were most commonly associated with bermudagrass and bentgrass putting greens in Alabama, and to ascertain their infestation levels.

Soil samples were collected from one to three putting greens on each of 70 golf courses throughout Alabama in 1996. Fifty-seven courses had hybrid bermudagrass putting greens and 13 had creeping bentgrass putting greens. A total of 29 courses were sampled in South Alabama in June, 19 in Central Alabama in July, and 22 in North Alabama in August. Each green was sampled by removing 20 soil cores at roughly equal intervals in a zig-zag pattern across the green. Nematodes were extracted from a 100-cm³ subsample and plant-parasitic nematodes were identified, based on genus, and counted.

Population levels of individual genera were compared to threshold levels (minimum levels of nematodes that may justify nematicide treatment) used by the Alabama Cooperative Extension System for making nematicide recommendations for commercial golf courses. For both bermudagrass and bentgrass greens, the threshold levels per 100 cm³ soil are: ring (Criconemella) = 500; spiral (Helicotylenchus) = 300; lance (Hoplolaimus) = 60; root-knot (Meloidogyne) = 80; stunt (Tylenchorynchus) = 1,000; sheath (Hemicycliophora) = 80; sting (Belonolaimus) = 10; and stubby root (Paratrichodorus) = 100, per 100 cm³ soil.

From the 57 hybrid bermudagrass courses, nine genera of plant-parasitic nematodes were extracted from soil cores collected from a total of 157 putting greens (Table 1). The genera most frequently found were Criconemella, Helicotylenchus, Hoplolaimus, and Meloidogyne, which were found on 96, 61, 46, and 37% of the golf courses surveyed and on 80, 39, 31, and 16% of the putting greens sampled, respectively. The five other genera identified were found on less than 23% of the golf courses surveyed and on fewer than 10% of the putting greens sampled. Hoplolaimus appeared to be causing the greatest problem as populations above action threshold levels for nematicide treatment were found in five of the putting greens sampled.

Table 1. Frequency of Occurrence and Population Density of Plant Parasitic Nematodes in Soil Samples from Hybrid Bermudagrass Putting Greens in Alabama, 1996
Nematode genera	Golf courses with nematodesa, %	Greens with nematodesb, %	Nematodes/100 cm3 soil		Populations above threshold levelse
			averagec	maximumd
Criconemella	96.4	80.2	34.1	306	0
Helicotylenchus	61.4	39.4	33.7	664	1
Hoplolaimus	45.6	30.5	25.9	126	5
Meloidogyne	36.8	15.9	11.1	58	0
Tylenchorynchus	22.8	9.5	15.6	58	0
Hemicycliophora	21.0	9.5	26.1	204	1
Belonolaimus	8.7	3.8	4.3	12	1
Paratrichodorus	5.2	1.9	2.3	4	0
Pratylenchus	1.7	1.2	3	4	0
aPercentage of golf courses with at least one nematode infested putting green. Percentage based on 57 golf courses with one to three putting greens sampled on each golf course. bPercentage based on a total of 157 bermudagrass putting greens with one to three greens sampled from each course. cMean population density from bermudagrass putting greens in which the nematode was found. dMaximum population found in soil samples from individual bermudagrass putting greens. eThreshold levels (minimum levels of nematodes that may justify nematicide treatment): Criconemella = 500, Helicotylenchus = 300, Hoplolaimus = 60, Meloidogyne = 80, Tylenchorynchus = 1,000, Hemicycliophora = 80, Belonolaimus = 10, Paratrichodorus = 100.

Five genera of plant parasitic nematodes were extracted from soil samples collected from 36 creeping bentgrass putting greens collected from 13 golf courses (Table 2). Helicotylenchus, Criconemella, and Tylenchorhynchus were the most frequently occurring genera found on 77, 69, and 46% of the golf courses surveyed and on 56, 53, and 28% of the putting greens sampled, respectively. Populations above treatment thresholds were observed on two putting greens for Helicotylenchus and on one green for Tylenchorhynchus.

Table 2. Frequency of Occurrence and Population Density of Plant Parasitic Nematodes in Soil Samples From Creeping Bentgrass Putting Greens in Alabama, 1996
Nematode genera	Golf courses with nematodesa, %	Greens with nematodesb, %	Nematodes/ 100 cm3 soil		Populations above threshold levelse
			averagec	maximumd
Helicotylenchus	76.9	55.5	146	1318	2
Criconemella	69.2	52.7	131.9	366	0
Tylenchorynchus	46.1	27.7	350.3	1608	1
Hoplolaimus	15.3	11.1	10	32	0
Meloidogyne	7.6	5.5	27	36	0
aPercentage of golf courses with at least one nematode infested putting green. Percentage based on 57 golf courses with one to three putting greens sampled on each golf course. bPercentage based on a total of 157 bermudagrass putting greens with one to three greens sampled from each course. cMean population density from bermudagrass putting greens in which the nematode was found. dMaximum population found in soil samples from individual bermudagrass putting greens. eThreshold levels (minimum levels of nematodes that may justify nematicide treatment): Criconemella = 500, Helicotylenchus = 300, Hoplolaimus = 60, Meloidogyne = 80, Tylenchorynchus = 1,000, Hemicycliophora = 80, Belonolaimus = 10, Paratrichodorus = 100.

Nematode genera that occurred in 5% or more of the putting greens sampled were distributed throughout the state. Nematodes were found on a higher proportion of bermudagrass than on bentgrass greens, with the exception of Hoplolaimus and Tylenchorhynchus spp. (Tables 1 and 2). Four genera found on hybrid bermudagrass were not found on creeping bentgrass. However, average population size for four of the five genera associated with both turfgrass species was higher on bentgrass than on bermudagrass.

Results of this study agree with previous reports that indicate a variety of nematode genera are associated with turfgrass in the southeastern region of the United States. Criconemella and Helicotylenchus spp. were both found in a high percentage of hybrid bermudagrass and creeping bentgrass putting greens, which is also similar to what had been observed in the other states.

The greater number of nematode genera isolated, and the higher percentage of bermudagrass putting greens infested, compared to bentgrass greens, is likely due to the period when soil samples were obtained. The optimum time to take samples for nematode assay in the southeastern United States for warm-season grasses such as bermudagrass is June through August, whereas, the optimum months for sampling a cool-season turfgrass, such as creeping bentgrass, are in the fall.

Nematode populations were found above threshold levels in 11 of the 193 putting greens sampled (Tables 1 and 2). Hoplolaimus and Helicotylenchus were the only genera found above threshold levels on more than one green in this survey. It is believed that golf greens that are well maintained through a proper fertility and water management program may withstand higher nematode populations than the action thresholds reported.