Ann. appl. Bid. ( I 977). 86,405-413 Printed in Great Britain

405

The long-term effects of four monocultural regimes on two field populations of the nematodes Xiphinema

diversicaudatum and Longidorus spp.

BY D. G. McNAMAR4 AND R. S. PITCHER East Mulling Research Station, Maidstone, Kent, ME19 6BJ

(Accepted 14 Fekuary 1977)

SUMMARY

Population density changes of Xiphinema diversicaudatum and several Longidorus spp. were observed under four cultural regimes in long-term field experiments. Numbers of X. diversicaudatum increased under strawberry and, to a lesser extent, ryegrass, but remained more or less un- changed in hop and fallow plots. A mixture of four Longidorus spp. increased in numbers under grass but stayed static, or declined slowly under the other cultural regimes.

All changes in population density were slow to occur, taking 3 or 4 yr for differences to become statistically significant. Fluctuations in larval numbers were mainly responsible for overall population changes; numbers of adults showed little difference over 5 yr.

I N T R O D U C T I O N

Field observations on the distribution of Xiphinema diversicaudatum (Micol.) in relation to plant hosts have been made by Pitcher & Jha (1961), Harrison & Winslow (1961), Fritzsche (1966) and Cohn (1969) and laboratory assessment of the suitability of various hosts for feeding and/or short-term breeding of this species by Fritzsche & Hofferek (1969~) and Thomas (1970). The ecology of Longidorus marnosma Hooper has been studied by Fritzsche (1968) and its feeding on a range of plant species examined by Fritzsche & Hofferek (1969b) and Cotten (1976), while Taylor (1967) and Thomas (1969) have described the suitability of various hosts for L. elongatus (de Man); Taylor (1967) also reported some long-term effects of plant hosts on population densities of Xiphinema and Longidorus. This paper presents data obtained from experiments designed primarily to investigate cultural methods to control infection by the hop strain of arabis mosaic virus (AMV-H), which is transmitted by X . diversicaudatum. Other aspects of these and related trials will be published elsewhere.

406 D. G. MCNAMARA AND R. S. PITCHER

E X P E R I M E N T A L P R O C E D U R E

Site data Two sites were chosen for their suitability for the main objective of the experiments,

virus/vector studies on hops (Humulus lupulus). The first, (R) at Rosemaund Experi- mental Husbandry Farm, Hereford, had carried hops, apart from a I yr break, for 17 yr before they were removed in preparation for the experiment, by which time there was a patchy distribution of X. diversicaudatum with a mean density of c. 30/l soil in the trial area; a few Longidorus caespiticola Hooper (c. 5/1) were also present. The soil was a well-drained silt loam over a silty clay loam subsoil. The second site, (H), an old pasture at Horsmonden, Kent, adjoining a hop garden, was also a silt loam overlying about 3 m of well-drained alluvium. Before cultivation the pasture soil contained about twenty-five X. diversicaudatum and 1000 Longidorus spp./l; L . caespiticola, L . leptocephalus Hooper, L. goodeyi Hooper and L . elongatus being present in the approximate proportions of 3 : 2 : 2 :I respectively.

Treatments At both sites four cultural regimes were introduced to establish a range of X.

diversicaudatum densities in preparation for the planned virus studies. These comprised a bare fallow maintained by herbicides (paraquat and simazine), and plantings of hops (cv. Fuggle at R and cv. Progress at H), grass or strawberries (Fragaria ananassa, cv. Cambridge Favourite). The large plot size required for hope (40 ma at R and IOO ma at H) allowed only fourfold replication at each site.

Both trials were planned in two phases, the first comprising 3 yr of the four cultural regimes (phase I), after which all plants were to be removed, with a minimum of soil disturbance, and the whole area planted with hops to act as ‘bait’ plants for the detection of any residual AMV-H infectivity (phase 11). There were minor differences in phase I treatments; at R the grass regime consisted of a perennial ryegrass ley (Lolium perenne) kept free of broad-leaved weeds by regular herbicide sprays (MCPA) whereas at H it was simply a continuation of the old, rather weedy pasture. For reasons beyond the scope of this paper, phase I at H was extended to 4 yr and phase I1 was omitted. At R the strawberries grew little in the first year because the foliage was repeatedly grazed by rabbits, but after being protected with wire netting they grew well, forming matted rows on each plot. At H the strawberries grew well from the outset and formed a matted bed covering each plot.

Estimation of nematode numbers At both sites samples were taken from the 15-30 cm soil layer, the depth at which

prior sampling suggested that longidorid numbers would be maximal. T o minimize the effect of seasonal variations in numbers recovered, the data presented in Figs 1-6 are mainly based on means of samples taken in spring and autumn. At R at least twelve cores were taken from each plot with a 2.5 cm diameter cheese sampler and at H five larger samples were taken with a trowel, after the 0-15 cm layer had been removed by spade. Extraction procedure was identical for both sites, the bulked samples of

Population changes in Xiphinema and Longidorus 407

2 -

I \

lo:&H ----A

- = - - -3 - % - - - -

,P 1 1 2 1 3 -1 4 1 1 5

I . / 4 E 50 (a) /--- 1'' .

1969 1970 1971 1972 1973

Fig. I. Mean density per litre of Xiphinema diversicaudatum at Rosemaund (R). (a) Phase I: strawberry (O), ryegrass (e), hop (A), fallow (A). (b), Phase I1 all treat- ments grubbed and replanted with hop. Densities back-transformed from log,, (x+ I) transformations based on eight 200 ml soil samples per treatment. Vertical lines indicate L.S.D. (P = 0 .05 ) at each sampling occasion. P, pre-plant sample; 1-5, post-plant samples.

4 0 c

3 E Fig. 2.

about 600 ml/plot being gently crumbled and well mixed by hand, after which two zoo ml aliquot samples were taken and the nematodes extracted by a modified Cobb gravity and sieving technique (Flegg, 1967b).

RESULTS

At each site the numbers of adults remained relatively constant and did not differ significantly between treatments. Larvae were more numerous than adults and changes in their numbers were mainly responsible for fluctuations in total numbers,

408 D. G. MCNAMARA AND R. S. PITCHER

1970 1971 1972 1973 E

Fig. 3. Mean density per litre of Xiphinema diwersicaudatum at Horsmonden (H), under strawberry (O), old pasture (a), hop (A), fallow (A). No phase 11; other details as Fig. I .

1 , 2 , 3 , 4

1970 1971 1972 1973

Fig. 4. Mean density per litre of Longidorus spp. at Horsmonden (H). Other details as Fig. 3.

as illustrated by a comparison of the data for Longidorus spp. at site H (Figs 4, 5 , 6). Accordingly only total numbers (i.e. adults plus larvae) will be considered henceforth. Population data were transformed by square root and by loglo (x + I), the latter being more suitable where there is a tendency towards aggregation within a population (Bartlett, 1947). However, as there were no great differences between the results using the two transformations, it was concluded that aggregation, although of frequent occurrence in longidorid populations, had not seriously distorted these data. Never- theless the patchy distribution of longidorids over the trial plots often resulted in large variations between replicates and correspondingly large L.S.D.’s. Hence only the larger treatment differences are significant, although any slow but steady density changes which culminated in significant differences probably represent real trends.

Despite the considerable ecological differences between the two sites prior to these

Population changes in Xiphinema and Longidorus 409

I I 2

P 8 3

, ;>? -3 6 50

8 1970 1971 1972 1973 z Fig. 5 . Mean density per litre of Longidorus spp. adults at Horsmonden (H).

Other details as Fig. 3.

P 1 2 3 4

1970 1971 1972 1973 1 I 1 I L

Fig. 6. Mean density per litre of Langidorus spp. larvae at Horsmonden (H). Other details as Fig. 3.

experiments, population trends were broadly similar in both. There were marked differences, however, in the responses of Xiphinema and Longidorus to some of the cultural regimes, as noted below.

Strawberry. X . diversicaudatum responded positively to the presence of an abund- ance of strawberry roots, but major effects were not apparent for 3-4 yr. At R the rabbit damage to strawberry growth probably accounted for the initial fall in numbers (Fig. I, Samples I and 2). By the third year, however, numbers significantly exceeded those in the fallow plots and continued to rise even into the first year of phase I1 (R only); strawberry was then replaced with hops and under this crop nematode numbers significantly exceeded all but those in the grass plots (Fig. I , Sample 4).

D. G. MCNAMARA AND R. S. PITCHER

5 * * * 5 * * * 5 * * *

Fig. 7. Degrees of significance of differences between treatment effects on Xiphinema diversicuudatum ( X . d.) and Longidorus spp. ( L ) at two sites; (a), Rosemaund; (b), Horsmonden. 1-5, post-treatment samplings; *, **, ***, significant at P = 0.05, 0.01, O*OOI respectively; F, bare fallow; G, grass; H, hops; S, strawberry.

Thereafter it declined, but remained significantly higher than in the fallow and hop plots. At H no significant increase was apparent under strawberry until the fourth year, when the numbers exceeded those in all other treatments (Fig. 3). Longidorus spp. however, did not respond positively to strawberry at either site, numbers remaining much as in the fallow plots (Figs 2, 4).

Grass. X . diversicaudatum responded quickly and positively to ryegrass at R, the numbers being significantly greater than in the fallow plots from the third sampling onwards (Fig. I). In the second sampling, numbers significantly exceeded those in the strawberry plots probably because rabbits checked their growth. On the permanent pasture at H, Xiphinema numbers remained similar to those in the hop and fallow plots (Fig. 3). A grass regime favoured Longidorus spp. at both sites, despite the considerable initial difference in population densities, so that the numbers under grass became significantly greater than all others in the fourth and fifth samples

Hops. Hops had little impact on the initial Xiphinema densities at either site (Figs I , 3). However, at R the greater densities stimulated by strawberry and grass in phase I appeared to increase still further in the first year of hops (Fig. I , Sample 4). Thereafter they declined slowly, but throughout phase I1 they remained significantly greater than those in the former hop or fallow plots. Longidorus spp. were little affected by hops on either site and numbers were similar to those under fallow and strawberry (Figs 2, 4).

Fallow. Figs 1-4 suggest a slow decline of both genera at both sites, but only once (Fig. I, Sample 3) was there a significantly smaller number of Xiphima under fallow than under hops. At H, Xiphinema numbers in fallow plots did not differ significantly from those on either hops or grass (Fig. 3), and at neither site did the Longidorus density differ from that on strawberry (Figs 2, 4).

(Figs 2, 4).

Population chunges in Xiphinema and Longidorus 41 1

Statistical analysis. Significant differences referred to above and shown graphically in Figs 1-6 are at the 5 % level. Figs 7 a , b illustrate the level of significance between pairs of treatments on each sampling occasion. At both sites the positive effects of strawberry on Xiphinema and grass on Longidorus are clearly shown. The additional response of Xiphinema to grass at R led to a more complex picture (Fig. 7 a ) , but the contrasts of grass and strawberry with hops and fallow are quite clear.

D I S C U S S I O N

The slow reaction of X . diversicaudatum to a change in food source was to be expected from its long life cycle and low reproductive potential (Flegg, 1968; Flegg, Baxendale & Popham, 1970). Similar factors probably operated for the four Longidorus spp. present in these experiments. It is therefore logical that any increase in numbers should first manifest itself in the density of larval stages (cf. Figs 5 , 6). Had the favourable phase I crop regimes lasted longer than 3 or 4 yr there would probably have been a corresponding, but possibly less marked, increase in adult numbers.

Strawberry and ryegrass have been reported as good hosts for X. diversicaudatum (Flegg, 1967a; Fritzsche & Hofferek, 1969a; Pitcher & Jha, 1961 ; Thomas, 1970; Cotten, 1977) and for L. elongatus (Sharma, 1965; Taylor, 1967; Graham & Flegg, 1968; Thomas, 1969). The observed population increases on these hosts could there- fore be predicted, but some of the negative responses were unexpected. As already mentioned, the slight decline of X. diversicaudatum numbers in the first year of strawberry at R (Fig. I ) was probably attributable to the delayed establishment of the maiden plants. The poor long-term responses of Longidorus to strawberry could indicate that, although a good host for L . elongatus, strawberry is less suitable for L . caespiticola, L . leptocephalus and L. goodeyi which formed a large proportion of the population at H, while only L. caespiticola was present at R. The contrast in the positive response of X . diversicaudatum to ryegrass at R and its failure to increase on continuing pasture at H may reflect the relative nutrient potential of the fresh young roots of a ley as compared with the compact, slow-growing mat of a permanent pasture containing little ryegrass (Troughton, 1970). Moreover at H the initial population of X . diversicaudatum was much smaller and this species may have suffered from competition with greatly superior numbers of Longidorus spp. The steady increase of the latter, presumably a stable population, long-established on this old pasture site, is surprising, as the only change under experimental conditions was the removal of grazing pressure, resulting in more foliage growth and, probably, more roots.

More than 500 X . diversicaudatum/l have occasionally been recorded under indivi- dual hop hills, but mean populations in hop gardens rarely exceed 50/1, the higher counts usually occurring where weed control is poor. There are few experimental data on hops as a host of X . diversicaudatum, but Valdez (1971) found that although this species would feed on the roots, hop was inferior to all except two of a range of fourteen hop garden weeds and virus indicator species, and Cotten (1977) showed hops to be inferior to many other hosts. Even less is known of hop as a host of Longi- dorm spp., but hop gardens seem unable to support more than small numbers of L. caespiticola or, more rarely, L . Zeptocephalus (D. G. McNamara & R. S. Pitcher,

412 D. G. MCNAMARA AND R. S. PITCHER unpublished). For instance, in a 10-yr-old hop garden which had been planted on another part of the same permanent pasture field at H, which presumably initially contained similar numbers of the four Longidorus spp., L . goodeyi had virtually disappeared, while L . caespiticola fell to densities rarely exceeding 50/1 and L . lepto- cephalus and L . elongatus to even smaller numbers. Consequently it was not surprising that there was no increase in the densities of either Xiphinema or Longidorus under hops. The increases recorded under hops at R (Fig. I, Sample 4) are probably attributable to the strawberry or ryegrass of phase I rather than to the recently planted hops of phase 11. The subsequent declines of both genera under hops (Sample 5 ) support this hypothesis.

Harrison & Hooper (1963) and van Hoof (1970) have shown that longidorids can survive up to 3 yr in soil samples kept moist, but plant-free, in polyethylene bags, but it had been anticipated that under the more rigorous conditions of the field their numbers would have declined more rapidly than they in fact did. Especially remarkable was the survival for over 2 yr of large numbers of Longidorus spp. at H. Despite initial shallow rotavation of the soil, followed by the suppression of all except a few perennial weeds by repeated herbicidal sprays, the numbers under fallow remained similar to those under hop or strawberry. The numbers of L . goodeyi declined more rapidly than those of L . caespiticola and L . leptocephalus, both of which may be less dependent on grasses and, as already mentioned, are able to survive in small numbers in established hop gardens.

Although limited in scope, these two experiments support the accumulated evidence of many observers that field populations of longidorids are often remarkably stable, reacting only slowly to quite strong environmental pressures. The positive responses of X . diversicaudatum to strawberry and ryegrass and its generally poor response to hops correspond well with recent microplot work by Cotten (1977). These and the responses of Longidorus spp. to grass and hop are probably valid pointers to their behaviour on other sites. The most intriguing aspect, however, was the unexplained ability of some species of both genera to persist and maintain their health and food reserves in the virtual absence of the roots of vascular plants.

We thank Messrs G. P. Chater and F. J. Dickens of Rosemaund Experimental Husbandry Farm and Mr E. Cheesman of Nevergood Farm, Horsmonden for allowing us the use of the sites and for much help in establishing and maintaining the experi- ments. The Hops Marketing Board provided financial support for the experiment at Horsmonden. Our virologist colleagues, Dr J. M. Thresh and Mr P. J. Ormerod were jointly responsible with us for the planning and execution of the experiments and Mr G. P. Barlow, also of East Malling Research Station, carried out the statistical analyses.

Population changes in Xiphinema and Longidorus 413

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