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Abstract
Nematodes are the most abundant metazoa. Their food specicity, the high number of species and high abundance in every
habitat where decomposition takes place indicates that the structure of the nematode community has a high information
content. Since nematodes respond rapidly to new resources, and the nematode fauna can be efciently analyzed, the structure
of the nematode community offers an instrument to assess (changes in) the conditions of soils. A functional grouping of
nematodes is generally synonymous with allocation into feeding groups. However, soil quality assessment indices based on the
presence of all feeding groups still provide insufcient information regarding the functioning of soil ecosystems and their
threats. An alternative concept of functional groups is based on the life history of nematodes. In this paper we present the most
recent colonizerpersister allocation and the application of this scaling in the Maturity Index, cp-triangles, MI(25) and PPI/
MI-ratio. We propose to integrate the life strategy approach and trophic group classication to obtain a better understanding of
nematode biodiversity and soil functioning. Attention is given to competitive exclusion and coexistence and we summarize
present concepts regarding succession and degradation. # 1998 Elsevier Science B.V.
Keywords: Trophic groups; Maturity index; Succession; Guilds; Biodiversity; Competitive exclusion; Functioning
1. Introduction
With increasing concerns for soil functioning and
pollution-induced threats, there has been growing
interest in the nematode fauna of soils (Zullini and
Peretti, 1986; Bernard, 1992; Freckman and Ettema,
1993; Yeates et al., 1993; de Goede and Bongers,
1994; Neher and Campbell, 1994; Wasilewska, 1994;
Popovici and Korthals, 1995). The use of nematodes
as indicators of soil functioning could strongly benet
*Corresponding author. Tel.: +31 317 483350; e-mail:
tom.bongers@medew.nema.wau.nl
1
Present address: Department of Ecology and Ecotoxicology,
Vrije Universiteit, De Boelelaan 1087, NL-1081 HV Amsterdam,
The Netherlands.
0929-1393/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved.
PII S0929-1393(98)00123-1
240
Sufcient basic knowledge to allow routine identication of nematodes at family/genus level can be
reached within 2 weeks. With sufcient experience,
the analyses of the nematode fauna of a typical soil
sample takes about 2 h.
Usually six or seven feeding groups are distinguished among nematodes but, as in a soil tens of
species coexist, for example, the group `bacterialfeeders' is generally composed of more than ten
species (de Goede and Bongers, 1994). This raises
questions regarding functional diversity and redundancy of taxa using the same resources. In this article
the nematode fauna is considered in relation to this
functional diversity, ecosystem functioning and disturbances.
2. Grouping based on ecological characteristics
In ecological studies, functional groups of terrestrial nematodes are generally treated synonymously
with feeding groups. In addition to feeding on the
roots of higher plants, nematodes feed on bacteria,
fungi or are carnivorous. Change in relative abundances of bacterial or fungal feeding nematodes mirrors change in the decomposition route and width of
energy channels.
Within nematodes several life strategies have been
developed. Colonizers (r-strategists, in the broad
sense) produce many small eggs and exploit a nutrient-rich habitat rapidly. In contrast, persisters (Kstrategists, in the broad sense) hardly react at transient
conditions of high food availability. We propose to
integrate the feeding group and life strategy concept,
resulting in the concept of nematode `guilds.'
2.1. Feeding groups
The allocation of nematodes to feeding groups is an
effective method to condense information. Yeates et
al. (1993) published a synthesis in which the following
groups were distinguished:
1. Plant feeding
1a. Sedentary parasites
1b. Migratory endoparasites
1c. Semi-endoparasites
1d. Ectoparasites
241
fertilization or other disturbances resulting in accelerated decomposition (Sachs, 1950; Huhta et al., 1979;
Wasilewska et al., 1981; Sohlenius and Bostrom,
1984; Dmowska and Kozlowska, 1988; Ettema and
Bongers, 1993).
A decrease in the dominance of bacterial feeding
nematodes and an increase of fungal feeders is
observed under conditions of acidication or heavymetal-induced stress. Sturhan (unpublished data) analyzed soil nematode communities which had been
exposed to heavy-metal stress for a decade. At low
soil concentrations of chromium the ratio between
fungal feeders and bacterial feeders was 0.95, while at
a higher pollution level the ratio was 3.19; increasing
levels of nickel changed the ratio from 1.26 to 69.0.
Also Zn-, Mn-, Mo- and Cu-stress resulted in an
increasing number of fungal feeding Aphelenchoides
specimens (Sturhan, unpubl.). Comparable shifts have
been observed after soil Cu pollution (Korthals et al.,
1996b). Increase in the number of fungal feeders is an
indirect effect and shows that toxicological effects
observed in acute single species tests cannot simply be
extrapolated to chronic conditions in the eld.
2.2. Allocation of nematodes based on life strategy
characteristics
Rhabditid nematodes are typical opportunists. They
are easily transported by insects to places with high
microbial activity (e.g. dung). Rhabditids are characterized by a short generation time of about 1 week but
in this period they produce a high amount of small
eggs resulting in a high reproduction rate. As soon as
microbial activity decreases these r-strategists form
`dauerlarvae' awaiting better conditions.
Dorylaimid nematodes, on the other hand, show a
character complex of K-strategists. With a generation
time of months, producing few but large eggs, these
persisters cannot rapidly respond numerically to new
food resources. Some nematode taxa, however, do not
t in this system: for example, nematodes feeding on
higher plants and marine Oncholaimids.
Based on life strategy Bongers (1990) allocated
terrestrial and freshwater nematodes on a continuum
from colonizers to persisters (r- to K-strategists, sensu
lato) followed by a similar proposal for marine
nematodes (Bongers et al., 1991). After crystallization
and inclusion of further information regarding the
242
few but large eggs and motility is low. With a permeable cuticle they are very sensitive to pollutants and
other disturbances. This group is composed of the
larger dorylaimids: omnivores, predators and plant
feeders.
The above described cp-scaling or rK continuum is
not linear, the enrichment opportunists (cp-1) form a
characteristic group because they only occur under
enriched conditions. In marine habitats the large
oncholaimids are typical K-strategist but indicative
for enriched conditions (Bongers et al., 1991).
Moens et al. (1996) compared the life strategy of
Pellioditis marina (cp-1) and Diplolaimelloides meyli
(cp-2), both occurring under food-rich conditions, and
showed that the food uptake of P. marina was much
more inuenced by bacterial density than the food
uptake of D. meyli. P. marina prefers extremely high
bacterial densities; by feeding they reduce bacterial
numbers to below an optimal density and are themselves replaced by D. meyli. The sex ratio of P. marina
is less temperature-dependant than that of D. meyli. In
soil microarthropods, parthenogenetic reproduction is
generally a character of r-strategists (Siepel, 1994).
With nematodes, however, both parthenogenetic and
amphimictic reproduction occurs in opportunists and
persisters.
In Table 1 updated cp-values are given for terrestrial and freshwater nematodes. Further calibration
may be necessary. The main criterion to allocate taxa
in cp-1 is the ability to form dauerlarvae. For Panagrolaimidae and Bunonematidae, dauerlarvae formation is presently under study (Sudhaus, pers. comm.).
If they do not form dauerlarvae these taxa have to be
allocated to cp-2.
The diplogastrids are bacterial-feeding enrichment
opportunists. As an exception, the aquatic Pareudiplogaster pararmatus and Fictor ctor feed on diatoms. The latter nematode is an indicator for
oligotrophic waters (Zullini, 1976, 1988; Niemann
et al., 1996).
Body size shows a relation with metabolic rate and
cp scaling. Colonizers are generally smaller than
persisters but only when comparing species at order
levels. Within the Rhabditidae (cp-1) many species
reach lengths exceeding 2 mm, within the dorylaimids
(cp-4) species occur (Tylencholaimus, Dorydorella,
Microdorylaimus, Diphtherophora, Doryllium, Longidorella) which never exceed 1 mm in length.
3
5
4
1
4
21)
2
2
5
3
3
4
5
1
2
4
3
5
(3)
3
3
3
1
1
3
1
5
(3)
4
(2)
3
3
(3)
(3)
(3)
3
Ironidae
Leptolaimidae
Leptonchidae
Linhomoeidae
Longidoridae
Meloidogynidae
Microlaimidae
Monhysteridae
Mononchidae
Myolaimidae
Neodiplogasteridae
Neotylenchidae
Nordiidae
Nygolaimidae
Odontolaimidae
Odontopharyngidae
Onchulidae
Ostellidae
Panagrolaimidae
Paratylenchidae
Plectidae
Pratylenchidae
Prismatolaimidae
Psilenchidae
Qudsianematidae
Rhabditidae
Rhabdolaimidae
Teratocephalidae
Thornenematidae
Tobrilidae
Trichodoridae
Tripylidae
Tylenchidae
Tylodoridae
Tylopharyngidae
Xyalidae
4
22)
4
3
(5)
(3)
23)
24)
4
14)
1
2
4
5
3
1
3
2
1
(2)
2
(3)
3
(2)
4
1
3
3
5
3
(4)
3
(2)
(2)
1
2
243
244
Fig. 2. Relation between Cu dosage, pH and MI (25) in an agroecosystem, 10 years after the set up of the experiment (after Korthals et al.,
1996a).
Plant feeders
Bacterial feeders
Fungal feeders
Carnivorous nema.
Omnivorous nema.
cp-1
cp-2
cp-3
cp-4
cp-5
Ba-1
Pl-2
Ba-2
Fu-2
Pl-3
Ba-3
Fu-3
Ca-3
Pl-4
Ba-4
Fu-4
Ca-4
Om-4
Pl-5
Ca-5
Om-5
Plant feeders
Bacterial feeders
Fungal feeders
Carnivorous
Omnivorous
6
11
2
4
4
1
0
1
2
1
1
1
2
0
3
245
Heterocephalobus, Cephalobus, Acrobeles, Cervidellus, Eumonhystera, Anaplectus, Plectus and Wilsonema. Are eight of these redundant because they all
use the same resources? Will organic material be
decomposed and nutrient leaching prevented if only
Acrobeloides nanus is present? If there is a constant
decomposition rate at which it will still function
although bacteria cannot be scraped from sand particles by Acrobeloides as do species of Acrobeles.
Species of Acrobeloides, unable to swim actively, will
not easily reach new areas of increased microbial
activity; Acrobeloides species are unable to form a
buffer at a uctuating decomposition rate. Other problems arise if the soil dehydrates or if osmolarity of
soil capillary water otherwise increases: then the
presence of plectids is desired. Under oxygen-poor
conditions monhysterids are able to take over the role
of Acrobeloides and Plectus species.
Beside co-existence at genus-level, many of the
genera are represented by more than one species,
for example, the genus Plectus. Seasonal inuences
and heterogeneity of the soil system certainly play a
role in the co-existence of closely related species. We
assume that no two nematode species have identical
ecological properties. Factors which inuence competitive ability of nematodes include temperature
(Anderson and Coleman, 1982; Sohlenius, 1985),
moisture (Sohlenius, 1985), number of dauerlarvae
(Strauch and Rehfeld, 1989), body sizes (Yeates et al.,
1985; Yeates, 1986, 1987a), stylet length (Yeates,
1986) and colonizing pattern (Sohlenius, 1988).
We might conclude here that each of the `guilds'
described above, is still composed of a high number of
taxa. The number of genera per group might be a
useful ecosystem parameter to measure biodiversity.
Biodiversity, when viewed in relation to the condition
of a system and succession, is a matter not only of a
high number of species, but also concerns the life
strategy of the constituent species. From an appreciative point of view the number of colonisers (Ba-1) is
hardly interesting. They occur in every habitat, generally as dauerlarvae, but even in the most stable
tropical forest, fruits and carcasses are assumed to
offer habitats for enrichment opportunists.
In order to represent the biodiversity of a habitat the
most promising method would be to enumerate the
total number of species of the higher scaled taxa (cp-4
and cp-5), or to express their percentage abundance as
246
proposed indirectly by Johnson et al. (1974); Wasilewska (1974); Zullini and Peretti (1986). Generally,
however, these persisters occur in low densities which
means that from a practical point of view a high
number of nematodes has to be identied to obtain
reliable information. A pragmatic alternative would be
to establish the number of species in group Ba-2, as
these occur in every habitat, even the most stressed,
and are generally well represented.
4. Competitive exclusion and co-existence
The observation that Ba-2 can be composed of as
many as ten co-existing genera raises questions
regarding whether they really co-exist or whether they
are spatially isolated. At the species level closely
related species often co-exist. The case of co-existence
of Pratylenchus penetrans and P. crenatus under
agricultural conditions is well-known; the same holds
for Amplimerlinius caroli and A. icarus and a range of
Meloidogyne species (Bongers, 1988).
A study of natural habitats in the Netherlands (de
Goede and Bongers, 1994) revealed the co-existence
of two or more species in each of the genera Filenchus,
Neopsilenchus, Criconema, Paratylenchus, Hemicycliophora, Rhabditis, Acrobeloides, Eucephalobus,
Heterocephalobus, Plectus, Teratocephalus, Tripyla,
Alaimus, Eudorylaimus and Trichodorus.
In addition to cases of co-existence, these observations reect heterogeneity of the habitat species A in
the litter, and B in the mineral layer or perhaps of the
genus concept (Plectus-Hemiplectus; ParatylenchusGracilacus). Based on the distribution of nematodes in
a chalk grassland, Hodda and Wanless (1994b) concluded that the competitive exclusion principle is
largely responsible for limiting the number of fungivorous nematodes.
Cases of competitive exclusion are not well documented as far as nematodes are concerned. Yeates et
al. (1985) demonstrated that different plant feeders on
clover showed complementary distribution patterns.
Boag and Alphey (1988) argued plausibly that competition was the main factor which prevented Paratylenchus nanus from increasing in plots where
Rotylenchus robustus was present.
In 1985 a study was carried out regarding the
nematode fauna of declining forests in the Netherlands
Table 4
Criconematid species living in the rizosphere of a declining
Juniperus communis (Bongers, 1985) and stylet lengths in mm
according to Bongers (1988)
Species
Stylet length in mm
3851
4768
101130
247
248
249
References
Alphey, T.J.W., 1985. A study of spatial distribution and population
dynamics of two sympatric species of trichodorid nematodes.
Ann. Appl. Biol. 107, 497509.
Anderson, R.V., Coleman, D.C., 1982. Nematode temperature
responses: A niche dimension in populations of bacterialfeeding nematodes. J. Nematol. 14, 6976.
Andrassy, I., 1976. Aglenchus costatus. C.I.H. Descriptions of
plant-parasitic Nematodes 6, 80.
Armendariz, I., Hernandez, M.A., Jordana, R., 1996. Temporal
evolution of soil nematode communities in Pinus nigra forest
of Navarra. Spain. Fundam. Appl. Nematol. 19, 561577.
Bernard, E.C., 1992. Soil nematode biodiversity. Biol. Fertil. Soils
14, 99103.
Boag, B., Alphey, T.J.W., 1988. Influence of interspecific
competition on the population dynamics of migratory plantparasitic nematodes with r and K survival strategies. Revue
Nematol. 11(3), 321326.
Bongers, T., 1985. Nematodes in Dutch forests (in Dutch). Meded.
175, Vg. Nematologie, Wag. Agric. Univ.
Bongers, T., 1988. De Nematoden van Nederland. KNNV
Bibliotheekuitgave 46, Pirola, Schoorl, Netherlands, 408 pp.
Bongers, T., 1990. The maturity index: An ecological measure of
environmental disturbance based on nematode species composition. Oecologia 83, 1419.
Bongers, T., Alkemade, R., Yeates, G.W., 1991. Interpretation of
disturbance-induced maturity decrease in marine nematode
250
Johnson, S.R., Ferris, J.M., Ferris, V.R., 1974. Nematode community structure of forest woodlots: III. Ordination of taxonomic
groups and biomass. J. Nematol. 6, 118126.
Khera, S., Zuckerman, B.M., 1963. In vitro studies of host-parasite
relationships of some plant-parasitic nematodes. Nematologica
9, 16.
Korthals, G.W., de Goede, R.G.M., Kammenga, J.E., Bongers, T.,
1996a. The maturity index as an instrument for risk assessment
of soil pollution. In: van Straalen, N.M., Krivolutsky, D.A.
(Eds.), Bioindicator Systems for Soil Pollution. Kluwer, pp.
8593.
Korthals, G., Lexmond, T., Kammenga, J., Bongers, T., 1996b.
Long-term effects of copper and pH on the nematode
community in an agroecosystem. Environ. Tox. Chem. 15,
979985.
Moens, T., Vierstraete, A., Vincx, M., 1996. Life strategies in two
bacterivorous marine nematodes: Preliminary results. P.S.Z.N.
I. Marine Ecology 17, 509518.
Neher, D.A., Campbell, C.L., 1994. Nematode communities and
microbial biomass in soils with annual and perennial crops.
Appl. Soil Ecol. 1, 1728.
Niemann, R., Arens, R., Koczwara, K., Sturhan, D., 1996.
Untersuchungen ueber die Eignung von Nematoden zur
Guetebewertung von Fliessgewaessern. Mitt. Biol. Bundesanst.
Land-Forstwirtsch. Berlin-Dahlem 317, 195208.
Popovici, J., Korthals, G., 1995. Soil nematodes used in the
detection of habitat disturbance due to industrial pollution.
Stud. Univ. Babes-Bolyai, Biol. (1993) 30, 3741.
Sachs, H., 1950. Die Nematodenfauna der Rinderexkremente.
Zool. Jahrb. Syst. 79, 209272.
Siddiqi, M.R., 1986. Tylenchida, Parasites of Plants and Insects.
CAB, Commonwealth Inst. Parasitology, London.
Siepel, H., 1994. Life-history tactics of soil microarthropods. Biol.
Fertil. Soils 18, 263278.
Sohlenius, B., 1985. Influence of climatic conditions on nematode
coexistence: A laboratory experiment with a coniferous forest
soil. Oikos 44, 430438.
Sohlenius, B., 1988. Interactions between two species of
Panagrolaimus in agar cultures. Nematologica 34, 208217.
Sohlenius, B., 1993. Chaotic or deterministic development of
nematode populations in pine forest humus incubated in the
laboratory. Biol. Fertil. Soils 16, 263268.
Sohlenius, B., Bostrom, S., 1984. Colonization, population
development and metabolic activity of nematodes in buried
barley straw. Pedobiologia 27, 6778.
Strauch, O., Rehfeld, K., 1989. Untersuchungen zur Populationsoekologie, Umweltkapazitaet und Koexistenzfaehigkeit der Zwillingsarten Rhabditis icosiensis und Rh.
cylindrica (Nematoda: Rhabditida). Verh. Gesellsch. Oekol.
18, 807812.
Sudhaus, W., 1981. Ueber die Sukzession von Nematoden in
Kuhfladen. Pedobiologia 21, 271297.
Wasilewska, L., 1974. Rola wskaznikowa wszystkozernej grupy
nicieni glebowych. Wiad. Ekol. XX, 385390.
Wasilewska, L., 1994. The effect of age of meadows on succession
and diversity in soil nematode communities. Pedobiologia 38,
111.
251