The Ecology of Globodera pallida (Stone) Mulvey & Stone (Nematoda, Heteroderidae) at Pukekohe, New Zealand

Abstract

The ecological status of Globodera pallida (Stone) Mulvey & Stone in the potato-growing district of Pukekohe, in the North Island of New Zealand was examined. A study of population dynamics provided the basis on which interactions with the local ecosystem could be assessed; the ecosystem was considered with respect to its influence on G. pallida, and conversely with respect to the influence of G. pallida upon it; and finally, some aspects of the capacity of G. pallida to survive and adapt to local conditions were considered. Research was carried out under strict quarantine conditions within the 0.2 ha potato cyst nematode research compound at the DSIR Vegetable Research Station, Pukekohe, using microplot techniques. A technique was developed for rearing G. pallida in the laboratory. Potato root systems were grown in sand in closed, clear plastic canisters which inhibited foliage growth and stabilised moisture balance. Potato cyst nematode eggs were inoculated into the sand, and at optimum temperatures of 15-20°c one generation lasted 8-12 weeks. The method had the advantage of not requiring light, and rearing canisters could be stacked in standard incubators. Its high reliability rendered the method particularly suited to pathotype analysis, and to general biological studies. Population dynamics of G. pallidawere studied by the life equation method of age-specific life tables analysis. Instead of comparing ecdysial stadia, analysis was based on a functional, or 'life-style' subdivision of the life cycle. Only the active part of the life cycle in the presence of a host plant was examined. Four distinct life styles, each with a particular set of functions to perform and survival hurdles to overcome, were identified: A, life within the cyst (from planting of host onward); B, life of second stage juveniles within the soil; C, life within the root (feeding second and third stage juveniles); and D, sub-adult/adulthood (fourth stage juveniles and adults, where sexual dimorphism in feeding habits and function is distinct). Further modifications to standard procedure included cohort replication to allow destructive sampling, and containerisation of cohort/host units to provide isolation in the field and to facilitate retrieval and assessment of animals. The cohort/host unit comprised a single potato plant with a 2.5 l rhizosphere plus a cohort of inoculum cysts. To obtain estimates of numbers of individuals entering each life style, a set of equations was derived from a series of parameters which were measured at each sample date. A limitation of the method was the long sample interval relative to duration of early juvenile stages, which enforced a modification to assessment equations on occasions. Recent developments in analysis (Manly, 1976, 1977) allow a flexible sampling plan which would overcome this problem. Survival within the life cycle was examined in relation to two variables, season and population density. Life tables were constructed over each of the four seasons during 1975 at a moderate population density (10 live eggs/g soil), and over three population densities (1, 10, 50 live eggs/g soil) during the spring season. Survival to reproductive adulthood was highest in spring, moderately high in summer and winter, but very low in autumn, effective population multiplication rates being 15.6, 6.5, 2.5, and 0.6 times, respectively. Egg-hatch was generally high, but delayed by two to three weeks in winter. Sex ratio was approximately 0.7 in all except the summer generation. Winter-produced cysts were not fully mature at harvest, which resulted in reduced egg viability. Durations of pre-adult stadia were seasonally stable, but in winter the migratory phase was extended, and in summer the duration of second stage juveniles in the root was shortened. Survival curves had a characteristic sigmoid shape, reflecting high juvenile mortality, which indicated that G. pallida had basically a type III survivorship curve. Seasonal effects caused small perturbations in slope of the curve, but were mainly reflected in final survival levels. The population density range of life tables displayed typical density-dependent effects, effective population multiplication rates being 20.1, 15.6, and 4.2 times for low, medium, and high densities, respectively. Sex ratio showed a positive relationship with population density, whilst female fecundity showed a negative relationship. Mortality during life style D (subadult/adulthood) doubled under high population density. Survival curves again showed a typical sigmoid shape. Key factor and correlation analyses were carried out on all components contributing to final population multiplication rate: fecundity, and mortality of second stage juveniles within the soil were important determinants on a seasonal basis; fecundity, subadult/adult mortality, and sex ratio were important on a density basis. Environmental influences on the two seasonally important components of multiplication rate were found to be soil moisture, which had a marked negative influence on mortality of second stage juveniles in the soil, and soil temperature, which influenced fecundity, with an optimum at 15-18°C. Mean range of soil temperatures at Pukekohe fell just within either cardinal limit for successful development of G. pallida. During winter, a temperature-related delay in egg-hatch shifted the active part of the nematode life cycle into more favourable early spring temperatures, but the life cycle as a result, was barely complete at harvest. Soil moisture was the prime determinant of multiplication rate during the summer season. The autumn season presented the most adverse conditions for G. pallida. Although mean soil temperature and moisture were virtually identical with those of spring, the sequence of falling temperature and increasing moisture coincided unfavourably with events within the potato cyst nematode life cycle. Biotic factors in the Pukekohe soil ecosystem with potential influence on G. pallida were: Nematode competitors - Meloidogyne incognita, Pratylenchus pratensis, Helicotylenchus digonicus, H. pseudorobustus, Paratrichodorus (Nanidorus) sp..Nematophagous fungi - Trapping hyphomycetes - Arthrobotrys oligospora, Dactylella brochopaga, Monacrosporium parvicollis, M. eudermatum; endozoic hyphomycetes - Harposporium anguillulae, Acrostalagmus obovatus; trapping phycomycetes - Stylopage hadra, and an unidentified species. A. oligospora, D. brochopaga, and S. hadra were most abundant; and the latter two species constitute new records for New Zealand. Fungal egg pathogens - No recognised fungal pathogens were found, but Fusarium sp. and Humicola sp. were frequently isolated from cysts with a high proportion of dead eggs. Sporozoa - A 'Dubosquia-like' pathogen of active nematodes was abundant; and an unidentified sporozoan was associated with cysts, but caused little damage to the contents. Predacious nematodes - Clarkus propapillatus, Seinura sp., Acrostichus sp., Sectonema sp. and Nygolaimus sp.. The first three species were seasonally abundant. An Aporcelaimellus sp. was often found inside intact but empty cysts, and was thought to feed on contents. Miscellaneous predators - several species of mite were identified, of which Veigaia serrata and Parasitus fimetarum were considered to be particularly voracious; a staphylinid insect, Anopylus sp. fed on eggs; and a predator which was not identified, chewed large holes in cyst cuticles and apparently devoured the contents. Organisms thought to have most potential as biological control agents were the 'Dubosquia-like' sporozoan; nematode predators Acrostichus sp. Seinura sp., and Aporcelaimellus sp.; and the unidentified cyst predator. Influence of an invading population of G. pallida on the local soil ecosystem was considered, using the soil nematode community as an example. To isolate effects due to the invading species, and due to potato monoculture, community composition was examined under grass (undisturbed habitat), under potato monoculture both alone (cultivated), and in the presence of G. pallida (cultivated/invaded). The two-year study followed changes in community structure from an initially impoverished state (12 months' fallow), to stabilisation of each habitat. The nematode community was divided into six feeding groups according to predominant food preferences: plant parasites, root hair feeders, fungal feeders, predators, miscellaneous feeders, and bacterial feeders. Higher plant feeders were split into two groups, those known to have pathogenic effect (plant parasites), and others (root hair feeders), because the former were considered more likely to interact with G. pallida. Under grass, the nematode community underwent a large increase in numbers and a significant increase in species diversity. All feeding groups were well represented, with bacterial feeders dominant. As the habitat became established, root hair feeders and fungal feeders increased in abundance whilst predators and miscellaneous feeders decreased. The plant parasitic group remained relatively low throughout. There was an apparent succession in relative abundance of predators, root hair feeders, and fungal feeders during establishment of the grass plot, each lasting approximately six months or one to two generations. Seasonal cycling began to appear as the community stabilised. Under potato cultivation the community remained in a permanently immature state, or disclimax; both total numbers and species diversity remained low compared with the grass habitat, and seasonal cycling did not occur. Bacterial feeders remained high, but the plant parasitic group gained relative dominance, increasing from 2-5 to 40-50%. The remaining four groups declined markedly, the root hair group in particular almost disappeared. Invasion by G. pallida had far less impact on community structure than did potato monoculture, however two effects were noted: G. pallida had a strong depressant effect on the frequency of all other plant parasitic species, and showed obvious competitive superiority under potato monoculture; and significantly higher predator levels were recorded in the G. pallida plot. Incidence of selected species within each habitat was compared; the species were: Plant parasites - Meloidogyne incognita, Pratylenchus pratensis, Helicotylenchus digonicus and H. pseudorobustus, Paratrichodorus (Nanidorus) sp.; predators - Clarkus propapillatus, Seinura sp., Acrostichus sp.; root hair feeders - Aglenchus costatus, -Tylenchus (Filenchus) neoaberrans; fungal feeders - Aphelenchoides bicaudatus, Aphelenchus avenae. In general, behaviour of populations was typical of the feeding group to which the species belonged. Survival and adaptability of G. pallida was considered in relation to temperature, and to weed hosts. Temperature profiles were constructed for the Pukekohe population of G. pallida, and for one population each of G. pallida and G. rostochiensis from Canterbury. Temperature ranges for population increase were: Pukekohe G. pallida, 8° to 22°C; Canterbury G. pallida, 9° to 23°; and G. rostochiensis 10° to approximately 25°. Although the optimum temperature lay between 15 and 20° for all populations, G. rostochiensis showed a far greater potential for increase over this range than G. pallida; only below 13 to 14° did G. pallida have a greater potential than G. rostochiensis. The slightly but significantly lower temperature range of Pukekohe G. pallida than Canterbury G. pallida may have been a pathotype difference (Pa2 compared with Pa3), but could also have been an adaptation of that population to repeated winter cropping of potatoes in soil temperatures of 6-14°. Subjection of Pukekohe G. pallida to temperature extremes of 9° and 21° for five generations in the laboratory did not induce adaptive shifts in the temperature profile. Two weed pests of New Zealand potato-growing land, Solanum nigrum and S. sarrachoides, were assessed for host status in relation to local potato cyst nematode populations. S. nigrum was a non-host for all populations; S. sarrachoides was a poor host for G. pallida and a non-host for G. rostochiensis. There was some indication of possible adaptation to S. sarrachoides by Canterbury G. pallida. A summary of environmental influences on G. pallida at Pukekohe is presented, and the basis for a predictive population model is suggested. It is concluded that G. pallida can adequately cope with the local environment, and is capable of rapid and successful establishment within it. A consideration of ecological strategies indicated that although potato cyst nematode evolved as a K-selected animal, it now encounters strong r-selection through an intimate association with Man, and because of this relationship, has become a highly successful coloniser.