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Applied Soil Ecology 10 (1998) 239251

Functional diversity of nematodes


Tom Bongers*, Marina Bongers1
Laboratory of Nematology, Wageningen Agricultural University, Pb. 8123, NL-6700 ES, Wageningen, The Netherlands
Received 1 April 1997; accepted 25 May 1997

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

from the techniques and mass of information available


for plant-feeding nematodes.
In order to condense information and facilitate
interpretation, often obscured by long species lists,
terrestrial nematodes are usually allocated to functional groups. Functional groups of nematodes can be
regarded as groups of species that have similar effects
on ecosystem processes. These functional groupings
are a practical necessity because we can never determine how each single species affects ecosystem processes (Chapin et al., 1992). A functional group is not
restricted to a phylogenetic unit (nematodes, protozoa
or another taxon) and moreover, they are not sharply
demarcated from each other. If we consider the function of a group `to release nutrients from bacterial
biomass,' then this functional group consists of a

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T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

number of nematodes, protozoa, tardigrades and other


taxa; even nematodes feeding on protozoa inuence
the structure of this trophic group and its functioning.
Additionally, there is no single unique ecosystem
function: the grouping of species strongly depends
on the ecosystem and function under study.
A pragmatic ecological grouping represents a compromise between practical necessity and a high number of functions/species. It can be routinely realised by
recognition of individuals at a high taxonomic level,
without help of specialized identication keys. An
efcient level for nematode identication lies between
the genus and family level, depending on the taxon.
Identication at family level provides considerable
information to reach a better understanding of soil
functioning. Identication at the species level will
undoubtedly reveal more information regarding biodiversity, redundancy and other ecological concepts
but is still hindered by the lack of identication keys.
The density of nematodes in the soil is generally
expressed in millions per square meter of land
surface. Highest densities, exceeding 50 million per
m2, have been found in the upper surface 10 cm
of highly productive salt marshes (Bongers and
Claassen, 1991). Probably, more than four out of ve
metazoic individuals on earth are nematodes, and
about 15 000 nematode species have been described.
Typically, a soil sample of 100 g yields around 3000
nematodes.
The species diversity of the terrestrial nematode
community is high. In practice it is almost impossible
to identify all nematodes in a soil sample to establish
how many species coexist. Indeed, a sample of 150
individuals will generally yield between 30 and 60
(morpho) species. Hodda and Wanless (1994a, b)
identied 154 different nematode taxa from two sites
in a heterogenous English chalk grassland during 2
years of sampling.
The structure of the nematode community offers an
efcient instrument for the biological assessment of
the quality and functioning of soils because: (a)
nematodes occur everywhere where decomposition
takes place, (b) their morphology reects feeding
behaviour, (c) of their interactions with other soil
biota, (d) of their food-specicity, (e) they have a
short response time, (f) they are easily isolated from
the substrate and (g) genus identication is relatively
simple.

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

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

1e. Epidermal cell and root hair feeders


1f. Algal and moss feeders
1g. Feeders on above-ground plant tissuea
2. Fungal feeding
3. Bacterial feeding
4. Substrate ingestion
5. Animal predators
5a. Ingesters
5b. Piercers
6. Unicellular eucaryote feeding
7. Dispersal or infective stages of animal parasites
8. Omnivorous
[in footnote: anot previously included.]
One of the most important discussion points
amongst nematologists is still the allocation of
Tylenchidae: are these fungal feeders or epidermal
cell feeders? The present practice is to allocate them to
the epidermal and root hair feeders. According to
Siddiqi (1986), the Tylenchidae are algal and moss
feeders and parasites of lower and higher plants.
Cephalenchus emarginatus is a migratory root ectoparasite feeding on epidermal cells (Hooper, 1974)
and Coslenchus costatus feeds undoubtedly on plant
roots (Andrassy, 1976). Cabbage is a good host for
Malenchus bryophilus and average host for Aglenchus
(Khera and Zuckerman, 1963). Hitherto, as far as we
know, no accurately identied Tylenchidae have been
observed reproducing on fungi.
In general, nematodes within a genus use the same
food source but there are exceptions. Species within
the genera Aphelenchoides and Ditylenchus, as far as
known, can be cultivated on fungi (Yeates et al., 1993).
Some species, however, have also evolved to be
important plant pathogens such as Ditylenchus dipsaci
and Aphelenchoides ritzemabosi. Also, differences in
feeding behaviour between developmental stages blur
the strict use of the trophic group designation; for
example, juveniles of the carnivorous mononchids
feed on bacteria (Yeates, 1987b). Nematodes feeding
on protozoa belong to trophic group 5 but information
regarding preying of nematodes on protozoa is scarce.
Feeding group analyses offer opportunities to
describe changes in decomposition pathways. There
are numerous examples from which it appears that
bacterial feeders increase in number as a result of
increasing microbial activity caused by, for example,

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

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T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

peculiar status of nematodes that are able to form


dauerlarvae (Bongers et al., 1995), the following
groups can be distinguished on the colonizerpersister
(cp) scale:
cp-1. Nematodes with a short generation time,
producing many small eggs resulting in an explosive
population growth under food-rich conditions, for
example, bacteria blooming in enriched soils. They
are relatively tolerant to pollution-induced stress. In a
petri dish, in water or on agar, these nematodes are
always active; for example, Rhabditidae are continuously pulsing with their oesophagus. Obviously they
have a high metabolic activity. These enrichment
opportunists show a phoretic relation with insects
and other vectors and are only active under transient
conditions of high microbial activity, they form dauerlarvae as microbial activity decreases. This group is
composed of rhabditid, diplogastrid and panagrolaimid bacterial feeders.
cp-2. Nematodes with a short generation time and
a high reproduction rate, but do not form dauerlarvae.
They occur under food-rich as well as food-poor
conditions and are very tolerant to pollutants and other
disturbances. This group is composed of the smaller
tylenchids, mainly feeding on epidermal cells; the
fungal feeding aphelenchoids and anguinids and the
bacterial feeding cephalobids, plectids and monhysterids.
cp-3. Nematodes with characteristics between
groups 2 and 4; they have a longer generation time
and are relatively sensitive to disturbances. This group
is composed of the bacterial feeding teratocephalids,
the Araeolaimida and Chromadorida; the larger
tylenchid nematodes that feed on deeper cell layers
in the roots; the diphtherophorids, assumed to feed on
fungi, and the carnivorous tripylids.
cp-4. Small dorylaimids and large non-dorylaimids. These nematodes are characterized by a long
generation time, permeable cuticle and sensitivity to
pollutants. The non-carnivorous nematodes in this
group are relatively sessile, whereas carnivorous have
to move. This group is composed of larger carnivores,
the bacterial feeding Alaimidae and Bathyodontidae,
the smaller dorylaimid nematodes and the plant feeding trichodorids.
cp-5. Large dorylaimid nematodes with a long life
span and low reproduction rate; both probably a
corollary of low metabolic activity. They produce

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.

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251


Table 1
cp-values of terrestrial and freshwater nematodes
Achromadoridae
Actinolaimidae
Alaimidae
Alloionematidae
Anatonchidae
Anguinidae
Aphelenchidae
Aphelenchoididae
Aporcelaimidae
Aulolaimidae
Bastianiidae
Bathyodontidae
Belondiridae
Bunonematidae
Cephalobidae
Choanolaimidae
Chromadoridae
Chrysonematidae
Criconematidae
Cyatholaimidae
Desmodoridae
Diphtherophoridae
Diplogasteridae
Diplogasteroididae
Diplopeltidae
Diploscapteridae
Discolaimidae
Dolichodoridae
Dorylaimidae
Ecphyadophoridae
Ethmolaimidae
Halaphanolaimidae
Hemicycliophoridae
Heteroderidae
Hoplolaimidae
Hypodontolaimidae

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

Classification follows Bongers (1988), values between brackets


refer to plant feeding taxa (PPI-calculation).
1) plant feeding Anguinidae: (2)
2) refers to Leptolaimus (see Bongers et al., 1991).
3) refers to Microlaimus (see Bongers et al., 1991).
4) See Bongers et al. (1995).

Within a number of taxa, species with smaller


individuals occur which are probably more opportunistic than those indicated for the whole family (Acrobeloides in Cephalobidae and Microdorylaimus in
Qudsianematidae).
Under nutrient-enriched conditions, group cp-1 is
dominant; cp-2 is dominant under heavy-metalinduced stress; whereas the presence of species from
groups 3, 4 and 5 indicates absence of stress and more

243

advanced successional stage. The Maturity Index (MI)


is dened as the (weighed) mean cp-value for the
nematodes in a sample, excluding the plant feeders
listed in Bongers (1990) and dauerlarvae. The value of
the MI varies from 1 (in cow pats or after heavy
manuring) to a value of around 4 under undisturbed
conditions. The MI has been shown to be a sensitive
instrument for monitoring the recovery after disturbances (Ettema and Bongers, 1993; Essink and
Romeyn, 1994), comparison of agricultural systems
(Freckman and Ettema, 1993; Neher and Campbell,
1994) and measuring pollution-induced stress (Popovici and Korthals, 1995; Korthals et al., 1996a, b).
The plant-feeding taxa were originally omitted for
calculation of the MI; a plant parasite index (PPI) was
calculated because of the inverse relationship of MI
and PPI under certain conditions. However, Yeates
(1994); Wasilewska (1994); Hodda and Wanless
(1994b) included plant-feeding taxa in their MI calculations.
Under the inuence of N-fertilization the MI
decreases because of higher microbial activity, but
the PPI increases probably as a result of the higher
carrying capacity of plants on which these nematode
feed (Bongers et al., 1997). The ratio PPI/MI (Bongers
and Korthals, 1995) appears to offer possibilities for
comparison among tillage regimes and for indicating
the nutrient status of a soil (Bongers et al., 1997).
As cp-1 is indicative of a high nutrient status, the
presence of these enrichment opportunists under agricultural conditions can mask the effect of heavymetal-induced stress. In order to measure the stress
independently of the enrichment effect, the enrichment opportunists should be omitted. Korthals et al.
(1996b) studied the chronic effect of 10 years copper
stress in relation to pH in agroecosystems (Fig. 1; for
further explanation see Korthals et al., 1996a). This
gure shows that despite the enriched conditions the
MI offers opportunities to measure the effect of the
stressor.
In a stressed environment with a low soil microbial
activity, such as an acidied forest, cp-2 nematodes
tend to dominate (de Goede and Bongers, 1994). After
eliminating the stress factor by liming, for example,
soil microbial activity increases resulting in an
increase of cp-1, but also the environment becomes
more suitable for the higher cp-groups. Such changes
are not necessarily expressed in the MI (De Goede

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T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

Romeyn, 1994; Bongers et al., 1995). The shifts in


a nematode community as a result of manuring,
acidication and recovery, are shown in Fig. 2.
In summary, the MI offers possibilities to measure
changes in the functioning of the soil ecosystem as a
result of disturbances and subsequent recovery. The
MI (25) offers possibilities to measure pollutioninduced stress factors, the PPI/MI-ratio is useful as
an indicator of soil fertility. Graphical presentation
can demonstrate changes not apparent in the calculation of the MI, and is a potential tool to bridge the gap
between soil ecologists and users of the information.
Fig. 1. Cp triangle showing shifts during (a) eutrophication, initial
situation and 2 weeks after adding powdered cow dung (Ettema and
Bongers, 1993; Table 2); (b) artificial acidification of coniferous
forest soil (Hyvonen and Persson, 1990; Table 3) and (c) recovery,
33 and 44 weeks after organic manuring (Ettema and Bongers,
1993) (after Bongers et al., 1995).

et al., 1993a). A graphical presentation of the cp-group


distribution offers the possibility to prevent loss of
information because of the contrasting inuences on
the MI. For that purpose cp-groups 3, 4 and 5 are
combined and the percentage distribution of cp-1, cp-2
and cp-3/5 plotted in a cp-triangle (De Goede et al.,
1993a; Ettema and Bongers, 1993; Essink and

3. Integration of feeding groups and cp-scaling


Both the feeding group classication as well as cpgrouping hide relevant information. If the K-strategists among the bacterial feeding nematodes are
replaced by enrichment opportunists, the frequency
of the feeding groups does not change. If the bacterial
feeding group Acrobeloides (cp-2) is replaced by the
fungal feeding Aphelenchoides (cp-2) the MI does not
change. Integration of these trophic group classications and division into cp-groups results in a classication of `guilds' with relatively strong interactions
within groups and weaker interactions between

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).

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251


Table 2
Functional diagram with possible combinations of feeding groups
and life-history characteristics

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

groups. The combination of groupings that currently


exist, based on present knowledge, is given in Table 2.
If a nematode community is composed of ve
species, for example, one member each of the genera
Rhabditis, Aphelenchoides, Pratylenchus, Anatonchus
and Prodorylaimus then all trophic groups and all cpgroups are present. However, rhabditids only feed
under conditions of high microbial activity; if microbial activity decreases they stop feeding. Under less
articial conditions the role of the rhabditids would be
taken over by Acrobeloides sp. (Ba-2). Assessing soil
quality based on the presence of all trophic groups and
all cp-groups alone is not sufcient to predict whether
the soil ecosystem functions or not. Integration currently offers 16 distinct combinations each with their
specic role.
In a 100 m2 grassland plot, we identied about 900
nematodes to the generic level (not published). The
number of genera in each group is indicated in
Table 3.
Only Ca-3 and Ca-5 are lacking but all other
combinations of trophic and cp-groups are present.
The bacterial feeders of cp-2 (Ba-2) are represented by
11 different genera of which two (Drilocephalobus
and Eucephalobus) were only represented by one
specimen. The other nine genera are Acrobeloides,
Table 3
Nematode genera in each of the `guilds' in a grass-land community
cp-group

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

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T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

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

Mesocriconema crenatum (Loof, 1964)


Mesocriconema curvatum (Raski, 1952)
Criconema sphagni (Micoletzky, 1925)

3851
4768
101130

(Bongers, 1985). In the rhizosphere of a declining


Juniperus communis, three criconematid species were
found in relatively high numbers. In discussing this
coexistence in terms of redundancy, Yeates (pers.
comm.) suggested that stylet lengths could be indicative of niche differentiation, nematodes with a long
stylet feeding at deeper cell layers in the root than
those with a short stylet (Yeates, 1986). In Table 4 the
stylet lengths of the three criconematids are given.
The barely overlapping stylet lengths might indicate
competitive exclusion. In the suborder Criconematina
(ectoparasites) numerous genera occur in which species show a wide divergence in stylet lengths (see also
Yeates, 1986). We have noted the co-existence of
criconematid genera with overlapping stylet lengths
but hitherto did not nd examples of co-existence of
criconematid species with comparable stylet lengths
that could not be explained by the heterogeneity of the
sample. Xenocriconemella macrodora can occur
together with Criconema annuliferum, both with a
long stylet, but this could also be explained by host
preference: X. macrodora feeds on Quercus roots.
Other genera within the Criconematina characterized
by a high divergence in stylet length are the Paratylenchus/Gracilacus-complex and Hemicycliophora.
Hemicycliophora conida Thorne 1955 is a
dimorphic species, one of the morphs has a stylet
length of 6986 mm, the other has a stylet length of
7896 mm (Bongers, 1988). Does the occurrence of
one of these morphs indicate a case of character
displacement, caused by the presence of another closely related species of which the length of the protrudable part of the stylet overlaps those of H. conida
on the same roots? Further research should indicate
whether Criconematina and other taxa can be distinguished in functional groups based on stylet lengths.
This adaptive radiation is particularly developed in the
Criconematoidea. The fact that other ectoparasites

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

(Tylenchidae, Dolichodoridae, Hoplolaimidae) do not


show this divergence might indicate the relatively
early branching of the suborder Criconematina.
Adaptive radiation in `stylet' length also occurs in
the Longidoridae and Trichodoridae, but in the trichodorids comparable spear lengths are no hindrance to
coexistence. According to Loof (pers. comm.) the
sample from which the holotype of P. anemones
was selected contained four other trichodorids with
strongly overlapping spear lengths (T. primitivus, T.
similis, T. pachydermis en Paratrichodorus nanus).
Alphey (1985) explained the coexistence of T. primitivus and P. pachydermis in effects of starvation,
patterns of aggregation, depth distribution and reproduction rate.
5. Biodiversity development
5.1. Primary succession
Faunal re-colonisation of areas treated by soil
fumigation or thermal cleaning is chaotic and recovery
often takes a long time (Ettema and Bongers, 1993;
Yeates and Van der Meulen, 1996). The rst nematodes that appear are those which can withstand
dehydration or which developed other mechanisms
to reach the habitat, there is no strict relation between
ability to reach the habitat and reproduction rate under
optimal conditions with the exception of enrichment
opportunists. Enrichment opportunists (Ba-1) are
transported by insects but fail to establish under
food-poor conditions. As soon as the supercial soil
is covered by unicellular algae, dorylaimids (cp-4 and
cp-5) are able to develop. Sohlenius (1993) concluded
that the development of nematode populations in
sieved pine forest humus under laboratory conditions
was unpredictable. The MI does not have predictive
value in the rst phase of colonisation of nutrient-poor
defaunated areas; only if the initial phase is food-rich
as in cow pats (Sudhaus, 1981) or manured soils
(Ettema and Bongers, 1993), does the MI increase
during primary succession.
5.2. Secondary succession
Recovery from a moderate disturbance, such as
tillage or fertilization, which does not eliminate soil

247

fauna, results in an increase of the dominance of


opportunistic bacterial feeders. Whether Ba-1 or
Ba-2 become dominant depends on the nutrient
status and microbial activity of the disturbed habitat.
Colonization of and population development on buried barley straw was monitored by Sohlenius and
Bostrom (1984). The material was initially colonized
by Ba-1 and Ba-2, subsequently Fu-2 appeared and
Ba-1 disappeared. Disturbance caused by adding
manure led to a comparable increase in Ba-1; this
treatment may secondarily also have affected persisters by production of toxic metabolites such as
ammonia. During succession, and correlated with
decreasing microbial activity, Ba-1 disappears. The
general opportunists (Ba-2) by contrast do not
disappear they are not replaced but replenished
by higher cp-groups (Ettema and Bongers, 1993).
This is a principal difference between nematode
succession and plant succession and raises the question whether opportunistic nematode species as
Acrobeloides sp. (Ba-2) are also r-strategists in the
strict sense.
5.3. Time scale
Plant succession from a bare substrate to a climax
vegetation is such a slow process by comparison to
changes in the nematode community that each characteristic successional stage offers the nematode fauna
enough time to develop towards the climax community that is typical for that vegetation type. Changes in
PPI/MI ratio, observed after ceasing N-fertilization
(Bongers et al., 1997) are not directly related to
vegetational changes but both are inuenced by the
nutritional status of the soil.
De Goede et al. (1993b) studied the succession from
drift sand to a 150 year-old pine forest. In each of the
major successional stages the structure of the nematode community was different. Replacement was more
pronounced than replenishment. Nematodes like the
algal feeding dorylaimids present in the rst phase
(drift sand) disappeared because of changing conditions during plant succession. In such a successional
series the MI does not provide information: changes in
other biotic and abiotic conditions (nutrients, pH,
humidity, vegetation and formation of a litter layer)
inuence the ultimate MI much more than the age of
the forest.

248

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

Armendariz et al. (1996) started from the opposite


standpoint. They assumed that a 20 year-old Pinus
nigra plantation had a lower MI than a 50 year-old
forest but found no correlation between time since
reforestation and MI. Subsequently, they assigned
alternative cp-values for nematode species typical
for the younger forest (a value of 1), via intermediate
values to a cp-value of 5 for nematodes typical of 50
year-old forests. Using these alternative cp-values
they found a signicant correlation between MI
(termed MI0 ) and the age of the forests under study.
However, comparison of their 50 year-old forest with
an 80 year-old forest deserves another ad hoc cpscaling.
5.4. Climax-communities
Dispersal of nematodes by wind, water and biotic
vectors to new habitats is a continuous process; also
under climax conditions nematodes are constantly
supplied, but the lack of suitable niches generally
prevents population establishment. Under natural conditions, the nematode community develops to a climax, occupied by species with a narrow niche breadth.
These niches can temporarily change in width or
disappear as a result of stress factors such as dehydration, changing CO2/O2 ratio, or temperature changes.
This might result in higher competition and extinction
of species in the micro-environment where they previously co-existed. Therefore, under mildly uctuating non-stressed conditions the highest diversity is
maintained. In this respect high diversity can be seen
as a result of relatively stable conditions. The ultimate
number of species in a habitat is a consequence of the
number of disturbances to which the habitat has been
subjected in the past and the number of species that are
potentially able to live there.
The most diverse nematode communities are found
in the tropics. In our opinion, this reects the geological longevity which is correlated with the time in
which species could develop. Regarding aquatic
nematodes it is remarkable that nematode diversity
in freshwater sediments is much lower than in marine
sediments or terrestrial systems. This might reect the
shorter timeframe of freshwater habitats from a geological point of view.
With the exception of resting spores of bacteria and
fungi we might expect that biodiversity of different

taxa of soil biota are correlated; that is, that a high


diversity of mites, collembola or protozoa under stable
conditions is correlated with high nematode diversity
because they are each determined by the stability
of the system. For vegetation diversity this is not
always the case, the monotonous Scandinavian pine
forests show a higher soil nematode diversity than
some heavy-metal-polluted sites with a diverse
vegetation.
5.5. Degradation
Degradation of a nematode community does not
necessarily turn out in a previous successional stage
regarding community structure. The scaling sequence
of the sensitivity of nematodes is not identical for all
stressors. Ultimately, a condition dominated by
enrichment opportunists will never be reached as a
result of, for example, heavy-metal-induced stress, cp2 species (Acrobeloides, Aphelenchoides and Tylenchidae) are the last metazoa to disappear in terrestrial
systems (TB, pers. observ.).
6. Biodiversity and functioning
Agroecosystems are generally characterized by
periodic disturbances such as tillage, use of pesticides
and fertilization that impede natural succession. Each
of these disturbances has a specic effect but each
results in a diversity decrease. Ploughing stimulates
mineralisation and results in increase of the number
and dominance of an opportunistic taxa, pesticides
inuence soil biota directly or indirectly via plants,
and fertilization in the form of manure results in an
sudden increase in biomass of Ba-1 (Dmowska and
Kozlowska, 1988).
The aim of agricultural tillage regimes is to stop
natural succession and to keep the system in imbalance to allow the crop, generally an r-strategist with
low competitive abilities, to compete for nutrients and
light. These conditions result in a high PPI/MI ratio
(Bongers et al., 1997).
An extreme method to create this imbalance is to
use the soil as substrate by eliminating the whole soil
biota, including competitors, and to add nutrient solutions as in hydroculture. However, if one plant pathogen is able to reach the system it can multiply rapidly

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

in the absence of antagonists. Another consequence


would be nutrient loss which can be prevented by
more sustainable methods as the timing and placement
of the nutrient supply of the soil to the nutrient demand
of the plants regarding place and time (Brussaard
et al., 1988)
In a complex soil ecosystem any nutrient ush is
assumed to be rapidly used by bacteria, protozoa,
nematodes and other consumers and converted to
biomass. Nematodes and other soil biota play an
important role in releasing nutrients from bacterial
biomass for uptake by plant roots. Those nematodes
that respond rst are enrichment opportunists, their
biomass uptake continues as long as the bacterial
activity is high. In the meantime populations of Ba2, generally Acrobeloides, start to develop followed by
other species. As the soil dehydrates, some species
cannot survive. However, Plectus is present in each
soil and can easily recover and take over the place of
Acrobeloides which has to recolonize the desiccated
habitats. Rhabditidae are an important buffer against
high ushes of nutrients, Acrobeloides of ushes
resulting in a microbial level below the carrying
capacity for Rhabditidae. Some soil pores will be to
narrow for Acrobeloides. In a diverse community there
will be nematodes with a narrow head or nematodes
that can scrape bacteria from soil particles. In a
sustainable system a high soil biota diversity is
required to prevent leaching by uptake in biomass
and to reduce local multiplication of soil-borne plant
pathogens. Each organism plays a role, the more the
species the more the interactions.
Regarding the structure of the nematode community, a stress factor such as copper pollution might
have a considerable effect on functioning and stability
because of disappearance of the most sensitive species
(cp-4 and cp-5) resulting in decreasing diversity
(Korthals et al., 1996b). Undoubtedly, the most sensitive nematode species regarding pollutants and other
disturbances are the carnivorous and omnivorous
nematodes. They can be considered to wield a regulating function: the carnivorous regulate other soil
biota numerically by feeding at the most dominant
prey and thus increasing biodiversity, the omnivorous
`assist' carnivores, bacterial and fungal feeders where
necessary. As these persisters are the rst to disappear
it is likely that the system becomes less stable functionally in terms of soil-borne plant pathogens and

249

buffering against seasonal and unpredictable nutrient


ushes.
This carries the implication that high diversity is
particularly important under changing conditions such
as uctuations in temperature, humidity, osmotic
value of pore capillary water, CO2 and O2 concentrations, pH and seasonal inputs of organic material. We
hypothesise that under uctuating natural conditions
in temperate zones nutrient leaching increases with
decreasing nematode biodiversity.
Acknowledgements
This paper benetted from discussions with the
participants of the `Soil Biodiversity Workshop' held
in Giessen in September 1996 and discussions with
Ron de Goede and Mike Jeger. We wish to thank
Dieter Sturhan for permission to use his unpublished
data. This paper was written within the DEGREE
project, funded by the European Commission (DGXII,
Contract-No. ENV4-CT95-0029).

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

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251

assemblages by means of the maturity index. Mar. Ecol. Progr.


Ser. 76, 135142.
Bongers, T., Claassen, Y., 1991. Bepaling van de effecten van
toxicanten op de nematodenfauna van het Land van Saeftinghe
(in Dutch). Meded. 248, Nem. Dept. Wag. Agric. Univ.
Bongers, T., de Goede, R.G.M., Korthals, G.W., Yeates, G.W.,
1995. Proposed changes of c-p classification for nematodes.
Russ. J. Nemat. 3, 6162.
Bongers, T., Korthals, G., 1995. The behaviour of MI and PPI
under enriched conditions. Nematologica 41, 286.
Bongers, T., van der Meulen, H., Korthals, G., 1997. Inverse
relationship between the nematode maturity index and plant
parasite index under enriched nutrient conditions. Appl. Soil
Ecol. 6, 195199.
Brussaard, L., Van Veen, J.A., Kooistra, M.J., Lebbink, G., 1988.
The Dutch programme on soil ecology of arable farming
systems I. Objectives, approach and some preliminary results.
Ecological Bull. 39, 3540.
Chapin, F.S., Schulze, E.D., Mooney, H.A., 1992. Biodiversity and
ecosystem processes. Trends in Ecol. and Evol. 7, 107108.
Dmowska, E., Kozlowska, J., 1988. Communities of nematodes in
soil treated with semi-liquid manure. Pedobiologia 32, 323
330.
De Goede, R.G.M., Bongers, T., Ettema, C., 1993a. Graphical
presentation and interpretation of nematode community
structure: C-P triangles. Med. Fac. Landbouww. Univ. Gent.
58/2b, 743750.
De Goede, R.G.M., Verschoor, B.C., Georgieva, S.S., 1993b.
Nematode distribution, trophic structure and biomass in a
primary succession of blown-out areas in a drift sand landscape.
Fund. Appl. Nemat. 16, 525538.
de Goede, R.G.M., Bongers, T., 1994. Nematode community
structure in relation to soil and vegetation characteristics. Appl.
Soil Ecol. 1, 2944.
Essink, K., Romeyn, K., 1994. Estuarine nematodes as indicators of
organic pollution; an example from the Ems estuary. Neth. J.
Aq. Ecol. 28, 213219.
Ettema, C.H., Bongers, T., 1993. Characterization of nematode
colonization and succession in disturbed soil using the maturity
index. Biol. Fertil. Soils 16, 7985.
Freckman, D.W., Ettema, C.H., 1993. Assessing nematode
communities in agroecosystems of varying human intervention.
Agric. Ecosyst. Environ. 45, 239261.
Hodda, M., Wanless, F.R., 1994a. Nematodes from an English
chalk grassland: Species distributions. Nematologica 40, 116
132.
Hodda, M., Wanless, F.R., 1994b. Nematodes from an English
chalk grassland: Population ecology. Pedobiologia 38, 530
545.
Hooper, D.J., 1974. Cephalenchus emarginatus. C.I.H. descriptions
of plant-parasitic nematodes 3, 35.
Huhta, V., Ikonen, E., Vilkamaa, P., 1979. Succession of
invertebrate populations in artificial soil made of sewage
sludge and crushed bark. Ann. Zool. Fenn 16, 223270.
Hyvonen, R., Persson, T., 1990. Effects of acidification and liming
on feeding groups of nematodes in coniferous forest soils. Biol.
Fertil. Soils 9, 205210.

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.

T. Bongers, M. Bongers / Applied Soil Ecology 10 (1998) 239251


Wasilewska, L., Paplinska, E., Zielinski, J., 1981. The role of
nematodes in decomposition of plant material in a rye field.
Pedobiologia 21, 182191.
Yeates, G.W., 1986. Stylet and body lengths as niche dimensions in
plant-parasitic nematodes. Zool. Anz. 216, 327337.
Yeates, G.W., 1987a. Significance of developmental stages in the
coexistence of three species of Mononchoidea (Nematoda) in a
pasture soil. Biol. Fertil. Soils 5, 225229.
Yeates, G.W., 1987b. Nematode feeding and activity: The importance of development stages. Biol. Fertil. Soils 3, 143146.
Yeates, G.W., 1994. Modification and qualification of the nematode
maturity index. Pedobiologia 38, 97101.
Yeates, G.W., Bongers, T., de Goede, R.G.M., Freckman, D.W.,
Georgieva, S.S., 1993. Feeding habits in nematode families and
genera an outline for soil ecologists. J. Nemat. 25, 315331.

251

Yeates, G.W., Van der Meulen, H., 1996. Recolonization of methyl


bromide sterilized soils by plant and soil nematodes over 52
months. Biol. Fertil. Soils 21, 16.
Yeates, G.W., Watson, R.N., Steele, K.W., 1985. Complementary
distribution of Meloidogyne, Heterodera and Pratylenchus
(Nematoda: Tylenchida) in roots of white clover. Proc.
Australasian Conf. Grassl. Invert. Ecol. vol. 4, pp. 7179.
Zullini, A., 1976. Nematodes as indicators of river pollution.
Nemat. Medit. 4, 1322.
Zullini, A., 1988. The ecology of the Lambro river. Riv. di Idrobiol.
XXVII, 3958.
Zullini, A., Peretti, E., 1986. Lead pollution and moss-inhabiting
nematodes of an industrial area. Water, Air, Soil Pollut. 27,
403410.