265 International Turfgrass Society Research Journal Volume 10

International Turfgrass Society
Research Journal Volume 10, 2005.
265
INFLUENCE OF SOIL TEMPERATURE ON HOST SUITABILITY OF EIGHT TURFGRASS SPECIES TO
THE LANCE NEMATODE (HOPLOLAIMUS GALEATUS).
Derek M. Settle, Tim C. Todd, Jack D. Fry and Ned. A. Tisserat*
ABSTRACT
The lance nematode (Hoploloaimus galeatus) has been reported from a number of turfgrasses although its
ability to reproduce on these hosts is poorly understood. We examined and compared the host suitability of eight
turfgrass species representing both C3 and C4 photosynthetic pathways to H. galeatus in a cool and warm soil environment.
Separate soil temperature treatments were established using a randomizable soil heating/cooling system. Both C3 and
C4 turfgrasses supported H. galeatus reproduction, but greatest populations occurred on C3 hosts at a 30 C soil temperature.
Additionally, the 30 C soil temperature resulted in lowest root biomass in C3 turfgrasses, a factor that further enhances
H. galeatus root feeding pressure. No individual C3/C4 host was found to consistently favor H. galeatus reproduction,
indicating that this nematode is capable of feeding and reproducing on a wide host range.
Keywords
Criconemella, Helicotylenchus, Hoplolaimus galeatus, nematode, turfgrass
INTRODUCTION
Numerous genera of plant parasitic nematodes
are part of the microfauna associated with turfgrass roots
(Davis and Dernoeden, 2002). The lance nematode
[Hoploloaimus galeatus (Cobb) Thorne] is often found in
abundance feeding on roots of a number of turfgrass
species (Feldmesser and Golden, 1972; Good et al., 1959;
Lucas et al., 1974) although its overall impact on turfgrass
health is variable and dependent on several factors
including environmental and soil chemical/physical,
geographic location, host susceptibility and cultural
practices (Browning et al., 1999; Davis and Dernoeden,
2002; Giblin-Davis et al., 1991; Lewis and Fassuliotus, 1982;
Lucas et al., 1978; Lukens and Miller, 1973; Myers et al.,
1992; Settle et al., 2002; Todd and Tisserat, 1990; Walker et
al., 2002).
High populations of H. galeatus have been
associated with a general thinning and decline of
bermudagrass (Cynodon spp..), centipedegrass [Eremochloa
ophiuroides (Munro) Hack.], and St. Augustinegrass
[Stenotaphrum secondatum (Walt.) Kuntze] swards in the
southern United States (Dudeck and Murdoch, 1999;
Giblin-Davis et al., 1988; Good et al., 1956; Hixson and
Crow, 2003; Johnson, 1970; Perry et al., 1971). Henn and
D.M. Settle, T.C. Todd, N.A. Tisserat, Department of Plant
Pathology, Kansas State University, Manhattan KS 66506,
USA. J. D. Fry Department of Horticulture and Recreation
Resources, Kansas State University, Manhattan 66506,
USA. *Corresponding author:’s curent address;
Department of Bioagricultural Sciences and Pest
Management, Colorado State University, 80523, USA.
Dunn (1989) reported that seven cultivars of St.
Augustinegrass were suitable hosts for H. galeatus.
However, Giblin-Davis et al. (1995) found no differences
in root or shoot growth between inoculated and noninoculated St. Augustinegrass and concluded that H.
galeatus was only mildly pathogenic to this host.
H. galeatus also has been reported on a number
of grasses growing in more northern regions of the United
States. Feldmesser and Golden (1972) reported a thinning
and chlorosis of Kentucky bluegrass (Poa pratensis L.) and
zoysiagrass (Zoysia japonica Steud.) lawns in Maryland that
had mixed nematode populations including H. galeatus,
but they did not show that nematode feeding was the
primary cause of the decline. Hoveland et al., 1975 reported
H. galeatus on tall fescue (Festuca arundinacea Schreb.) used
for forage. Todd and Tisserat (1990) reported that visual
quality of creeping bentgrass (Agrostis palustris Huds.) was
negatively correlated with lance nematode populations
but only during conditions of heat stress. However, high
soil temperatures in mid summer may directly damage
bentgrass root and result in a loss of turf quality regardless
of the presence of plant parasitic nematodes (Huang and
Liu, 2003). H. galeatus has been recovered from roots of
other turfgrasses including perennial ryegrass (L. perenne
L.) but its suitability as a host for this nematode has not
been studied in detail (Blackburn et al., 1997; GiblinDavis et al., 1991; Good et al., 1959; Hoveland et al., 1975;
O’Day et al., 1993; Rodriguez-Kabana et al., 1978).
Soil temperature influences both reproduction
of H. galeatus and root growth. Optimal soil temperatures
for reproduction of H. galeatus are 25 to 29 C (McGlohon
et al., 1961), and maximum egg hatching occurs at 32 C
(Rivera-Camarena, 1964). Optimal temperatures for root
growth are 10 to 18 C for turfgrasses with a C3
266
photosynthetic pathway (Huang et al., 1998; Fry and
Huang, 2004) and 27 to 35 C for those with C4
photosynthetic pathway (Beard, 1973;). However, the
influence of soil temperatures on host suitability to H.
galeatus has not been studied in detail. For example,
relatively high soil temperatures should increase H.
galeatus reproductive rates but may reduce overall root
biomass of C3 grasses and limit feeding sites.
The objective of our study was to examine the
host suitability of four turfgrass species with C3 and four
grasses with C4 photosynthetic pathways to H. galeatus at
soil temperatures of 20 and 30 C. We also report on a
modification of a randomizable water-controlled system
(Russell, 1984) to maintain constant soil temperatures in
the greenhouse.
MATERIALS AND METHODS
Experiment I
Soil naturally infested with H. galeatus was
collected from a sand-based (organic matter content of
2.1%, pH 7.3, and a bulk density of 1.5 g cm-1) creeping
bentgrass putting green at the Turfgrass Research Center,
Manhattan KS. Soil was carefully separated from the sod,
mixed thoroughly and stored at 4 C until placed in pots.
An initial soil population of 254 H. galeatus and 51
Criconemella sp. (adults + juveniles) g-1 dry weight soil as
determined by sucrose density centrifugation (Jenkins,
1964). Plastic pots (10 cm square x 15 cm deep) were filled
with the infested soil and then sodded with one of four
turfgrass species having a C3 photosynthetic pathway or
four species having a C4 photosynthetic pathway. The C3
grasses were ‘L-93’ creeping bentgrass, ‘Unique’ Kentucky
bluegrass, a perennial ryegrass varietal blend of ‘Charger
II’, ‘Manhattan II’, and ‘Chaparral’, and a tall fescue varietal
blend of ‘Tomahawk’, ‘Apache II’, ‘Coronado’, ‘Safari’,
‘Barlexas’, and ‘Tar Heel’. The four C4 grasses were
‘Midlawn’ bermudagrass, ‘NE 91-118’ buffalograss [Buchloe
dactyloides (Nutt.) Engelm.], ‘Meyer’ zoysiagrass and
‘Raleigh’ St. Augustinegrass. All sod except St.
Augustinegrass was collected from established swards at
the Rocky Ford Turf Experiment Station. St.
Augustinegrass was grown in the greenhouse in flats
containing sand. All plants were washed thoroughly with
water to remove soil adhering to roots before being placed
in pots. Pots were placed in a randomized complete block
design on a greenhouse bench, allowed to root for one
month and then transferred to a heating mat (Gro-mat,
GroForIt Products, Chicago, IL) that maintained soil
temperature at 30° C.
All pots were watered at first sign of turfgrass wilt,
fertilized weekly with a 20-10-20 N-P-K solution (Peters
Watersoluable M-77 Formula, The Scotts Co., Marysville,
OH) at 0.113 kg N ha-1, and clipped three days weekly at 2.5
mm height. The insect growth regulator fenoxycarb
(Precision, Syngenta, Greensboro, NC) at 0.3 g l-1 soil , was
applied every 14 to 21 days to control fungal gnats (Bradysia
sp.) and thrips (Frankliniella sp.). After one and three
months, two 1.5-cm-diam soil cores were removed to a
depth of 10 cm from each pot, bulked, and processed for
nematodes by sucrose density centrifugation. The roots
from each pot were harvested, dried and weighed. H.
galeatus populations were initially analyzed by the GLM
procedure (SAS Inst, 200 2) using root biomass as a
covariate. Because the covariate did not alter the overall
analysis, nematode means were not adjusted for root
biomass.
Experiment II
A second greenhouse study was initiated to
elucidate the effects of soil temperature on lance nematode
development on the eight turfgrass species. Soil infested
with 172 H. galeatus and 13 Crinonemella sp. 100 g-1 soil
was collected, added to pots, and sodded with one of eight
turfgrass species as previously listed. Populations of
Criconemella sp. remained at low levels (average of <14
100 g-1 soil) throughout the experiment. The turfgrass was
allowed to root in pots for one month before temperature
treatments were initiated. All other cultural treatments
were the same as the first experiment except that
nematodes were extracted from soil samples at monthly
intervals.
Soil temperatures were maintained in pots with a
modified randomizable water circulation system
developed by Russell (1984). A U-shaped segment of epoxycoated copper tubing (0.3 cm inside diam.) was embedded
in soil in each pot such that the open ends of the tube
protruded through drain holes in the pot bottom (Fig. 1).
The copper tubing was connected to polyethylene tubing
that was connected to manifolds. The manifolds were
connected by tubing to 190-liter tanks. The tanks were
filled with water that was either cooled to 20° C using an
aquarium chiller (CustomSeaLife, Inc., San Marcos, CA)
or heated to 30° C with an L-shaped heating element
(Cleveland Process Corp., Homestead, FL). Water was
circulated by stainless steel water pumps (Velocity S1,
CustomSeaLife, Inc, San Marcos, CA) from the holding
tank through the hoses and copper tubes and back to the
tank. The system was designed such that water only ran
through copper tubes in three pots before returning to the
reservoir. This insured that the water temperature did not
change significantly during circulation. Soil temperatures
in one arbitrarily selected pot at each temperature in each
block were monitored by thermistors. The system was
completely randomizable, so that pots with different soil
temperatures could be placed side by side.
Three replicate pots of each grass species by
temperature combination were arranged in a randomized
complete block design on a greenhouse bench. After three
months pots were scored for percent coverage of the pot
surface by the grass. H. galeatus population densities and
root dry weights for each pot were then determined as
previously described.
267
Figure 1. (A) A completely randomized block designed greenhouse experiment, consisting of eight turfgrass species.
(B)Two soil temperatures were maintained using 190 liter water reservoirs that were either heated to 30° C or chilled
(two square white chillers visible) to 20° C. Water was circulated in a closed-loop using in-line pumps (four red pumps
visible). (C) Water was initially pumped to a manifold and then routed through small diameter hoses which were
connected to epoxy-coated, U-shaped copper tubing that was embedded in the center of each pot.
Experiment III
The second experiment was repeated using most
of the same methods. Soil contained an initial population
of 101 H. galeatus, 122 Criconemella sp., and 251
Helicotylenchus sp. 100 g-1. The experimental design was
modified to a split plot with temperature (20° and 30° C) as
the main plot and grass species as the subplot. After three
months, dry clipping weight, percentage pot coverage by
the grass and nematode populations in the soil were
determined as previously described. In addition, H. galeatus
was extracted from the roots collected in samples for each
pot, and nematode numbers were adjusted to a 100 g dry
soil basis for comparison to soil populations.
RESULTS AND DISCUSSION
Populations of H. galeatus declined during the
first month of each study but then stabilized (Fig. 2). The
decline was probably associated with the initial lack of
roots (feeding sites) following turf establishment in pots.
All of the turfgrass species were suitable hosts for H.
galeatus based on the presence of second-stage juveniles
268
penetration and feeding by H. galeatus. Giblin-Davis et
al. (1995) reported that 85% of lance nematodes associated
with St. Augustinegrass were endoparasitic, and the most
frequent life-stage inside roots were juveniles. If this
population structure is similar in other turfgrasses, then
finer roots of C3 grasses could enhance nematode feeding
and reproduction. Rodriguez-Kabana et al. (1978) found
that tolerance of tall fescue to H. galeatus was associated
with its ability to produce large numbers of small diameter
roots. Thus grasses with small diameter roots may enhance
H. galeatus development, but also be more tolerant of
feeding injury.
Figure 2. Monthly populations of Hoplolaimus galeatus
averaged across 8 turfgrass species and two soil
temperatures (Experiments II and III only).
after three months under greenhouse conditions. This
was not surprising since H. galeatus is associated with roots
of a number of plant hosts including many turfgrass species
(Feldmesser and Golden, 1972; Good et al., 1959; Lucas et
al., 1974). Orr and Dickerson (1967) reported that other
native grasses growing in Kansas harbor H. galeatus and
it is likely this nematode species is indigenous to the Great
Plains region of the United States. Additionally, we
confirmed that buffalograss, which is native to the
shortgrass prairie ecosystem of the United States, is a host
for H. galeatus.
The C3 turfgrasses supported higher ectoparasitic
populations of H. galeatus than C4 grasses, but only at the
higher soil temperature of 30° C (Tables 1-3, Figures 3-5).
Relatively high soil temperatures enhance H. galeatus
feeding and reproduction (Rivera-Camerena, 1964), but
this cannot completely explain our results since elevated
nematode counts were not observed in C4 grasses grown
at 30° C. Furthermore, root biomass was lowest in C3
grasses grown at high temperatures in Experiments II and
III (Figs. 4 and 5) hence higher nematode populations
cannot be attributed to increased root growth.
Alternatively, C3 grasses may be preferred hosts of the
nematode because of physiological or physical attributes
of the roots. Hetrick et al. (1988) reported that roots of C3
grasses are smaller in diameter and finer than those of C4
grasses. This type root architecture may favor root
We did not detect differences in adult H. galeatus
populations among individual turfgrass species in
Experiments I or III (Tables 1 and 3), although in
Experiment I Kentucky bluegrass supported a higher
(P<0.05) juvenile population than all other grasses except
buffalograss (Fig. 6). In experiment II (Table 2), highest
(P< 0.05) juvenile numbers (63 g-1 soil) were observed in
tall fescue at 30 C whereas no juveniles were found in soil
extractions from tall fescue, zoysiagrass and bermudagrass
at 20C or St. Augustinegrass at 30° C (Fig. 6). The elevated
juvenile populations in soil of tall fescue and Kentucky
bluegrass may have been due to nematode migration from
damaged roots. Lance nematode juveniles are primarily
endoparasitic in St. Augustinegrass (Giblin-Davis et al.,
1995), corn (Norton and Edwards, 1988) and possibly other
monocots. Therefore high juvenile numbers in soil may
be an indicator of turfgrass root stress or mortality.
Nyczepir and Lewis (1979) found increased juvenile
populations H. columbus in soil following exposure of
soybeans to 30 C. They concluded that the juveniles had
migrated from roots damaged by the high temperature into
the soil.
In contrast to H. galeatus, final populations of
Criconemella and Helicotylenchus spp. in Experiment III
tended to be greater in the presence of C4 grasses compared
to C3 grasses (Fig. 7). No temperature effects were observed
for these taxa, and based on the consistency of the H.
galeatus response across experiments, their contribution
to the results of this particular experiment was likely
negligible.
Using a novel experimental system for
controlling soil temperature in greenhouse pots, we have
demonstrated that host suitability and temperature
preference are interdependent for H. galeatus. Nematode
densities were consistently greater in C3 compared to C4
turfgrasses only at the temperature that was near the
reported optimum for H. galeatus reproduction. These
maximum populations were concomitant with reduced
root biomass for C3 grasses at the higher soil temperature.
Together these observations suggest that, while coolseason turfgrasses may be relatively tolerant of nematode
parasitism under conditions optimal for the plant,
increased nematode reproduction and normal root stress
may combine to increase their susceptibility during
periods of heat stress.
269
Table 1. Analysis of variance table for Hoploliamus galeatus populations on four C3
turfgrasses (creeping bentgrass, Kentucky bluegrass, perennial ryegrass, and tall
fescue) and four C4 turfgrasses (bermudagrass, buffalograss, St. Augustinegrass and
zoysiagrass) incubated at a soil temperature of 30 C for 3 months in the greenhouse.
P-values are signified by **P < 0.05, ***P < 0.01, and NS = not significantly
different by Fisher's LSD test.
Experiment I
Total
Adult
Juveniles
Root Biomass
Block
NS
NS
NS
NS
C3/C4 Pathway
**
**
NS
NS
Species (C3/C4)
NS
NS
**
***
Table 2. Analysis of variance table for Hoploliamus galeatus populations on four C3 turfgrasses
(creeping bentgrass, Kentucky bluegrass, perennial ryegrass, and tall fescue) and four C4 turfgrasses
(bermudagrass, buffalograss, St. Augustinegrass and zoysiagrass) incubated at a soil temperature of 20
C or 30 C for 3 months in the greenhouse. P-values are signified by **P < 0.05, ***P < 0.01, and
NS = not significantly different by Fisher's LSD test.
Experiment II
Total
Adults
Juveniles
Root Biomass
Block
**
**
NS
NS
Temperature
**
NS
***
***
C3/C4 Pathway
**
NS
***
***
Species (C3/C4)
NS
NS
***
***
C3/C4 x Temperature
NS
NS
***
**
Species x Temperature (C3/C4)
**
NS
***
NS
Table 3. Analysis of variance table for Hoploliamus galeatus populations on four C3 turfgrasses (creeping
bentgrass, Kentucky bluegrass, perennial ryegrass, and tall fescue) and four C4 turfgrasses (bermudagrass,
buffalograss, St. Augustinegrass and zoysiagrass) incubated at a soil temperature of 20 Cor 30 C for 3 months
in the greenhouse. P-values are signified by **P < 0.05, ***P < 0.01, and NS = not significantly different by
Fisher's LSD test.
Experiment III
Total
Adults
Juveniles
Root Biomass
Temperature
NS
NS
NS
NS
C3/C4
NS
NS
NS
***
Species (C3/C4)
NS
NS
NS
***
Temperature x C3/C4
NS
**
NS
**
Temperature x Species (C3/C4)
NS
NS
NS
NS
Endo-/Ecto-
***
***
***
Temperature x Endo-/Ecto-
NS
NS
NS
C3/C4 x Endo-/Ecto-
NS
NS
NS
Temperature x C3/C4 x Endo/Ecto
***
**
NS
Species x Endo/Ecto x C3/C4
NS
NS
NS
Temperature x Species x Endo/Ecto (C3/C4)
NS
NS
NS
270
Figure 3. Experiment I: (A) Adult and juvenile populations
of Hoplolaimus galeatus and (B) root biomass in C3
(creeping bentgrass, Kentucky bluegrass, perennial
ryegrass and tall fescue) or C4 turfgrasses (bermudagrass,
buffalograss, zoysiagrass, and St. Augustinegrass) following
incubation at a soil temperature of 30° for 3 months. Means
not followed by the same letter are significantly different
by Fisher’s LSD test (P < 0.05).
Figure 4. Experiment II: (A) Adult and juvenile
populations of Hoplolaimus galeatus and (B) root biomass
in C3 (creeping bentgrass, Kentucky bluegrass, perennial
ryegrass and tall fescue) or C4 (bermudagrass, buffalograss,
zoysiagrass, and St. Augustinegrass) turfgrasses following
incubation at a soil temperature of 20° C or 30° for 4 months.
Means not followed by the same letter are significantly
different by Fisher’s LSD test (P < 0.05). At 30° C, total H.
galeatus populations (adults + juveniles) were significantly
higher (P<0.05) at 30°C than at 20° C.
Figure 5. Experiment III: Adult and juvenile populations
of Hoplolaimus galeatus extracted from (A) soil and (B)
roots in C3 (creeping bentgrass, Kentucky bluegrass,
perennial ryegrass and tall fescue) or C4 (bermudagrass,
buffalograss, zoysiagrass, and St. Augustinegrass)
turfgrasses and (C) root biomass following incubation at a
soil temperature of 20° C or 30° for 4 months. Means not
followed by the same letter are significantly different by
Fisher’s LSD test (P < 0.05).
Figure 6. Adult and juvenile populations of Hoplolaimus
galeatus in four C3 and four C4 turfgrasses incubated for 3
months at 30° C in Experiment I and 4 months at 20° C or
30° C in Experiment II. Means not followed by the same
letter are significantly different by Fisher’s LSD test (P <
0.05).
271
Good, J. M., J. R. Christie, and G. C. Nutter. 1956.
Identification and distribution of plant parasitic
nematodes in Florida and Georgia. Phytopathology
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Good, J. M., A. E. Steele, and T. J. Ratcliffe. 1959.
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Figure 7. Populations of Criconemella sp., Helicotylenchus
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Kentucky bluegrass, perennial ryegrass and tall fescue) or
C4 (bermudagrass, buffalograss, zoysiagrass, and St.
Augustinegrass) turfgrasses. Means within nematode
species not followed by the same letter are significantly
different by Fisher’s LSD test (P < 0.05).
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