Post on 30-Mar-2023
Tom Moens , Ulrike Braeckman , Sofie Derycke , Gustavo Fonseca , Fabiane Gallucci , Ruth Gingold , Katja Guilini , Jeroen Ingels , Daniel Leduc , Jan Vanaverbeke , Carl Van Colen , Ann Vanreusel and Magda Vincx
3 Ecology of free-living marine nematodes 3.1 General introduction To the public at large, the phylum Nematoda is mostly
known by its pathogenic species, causing some of the
most infectious diseases in humans and animals and more
crop losses worldwide than all arthropods. The majority
of nematode species and individuals, however, are free-
living in terrestrial soils and aquatic sediments, occupy-
ing basically all soft sediment habitats and, albeit in lower
abundances, biofilms on secondary and/or hard subst-
rata. Although nematodes may be found adrift in oceanic
plankton, they require a “ solid ” substratum for growth
and reproduction. Animals found in the water column are
individuals that have become eroded from sediments or
are rafting on drifting algae. In terms of abundance, an
estimated three-quarters, or more, of all animals on earth
are nematodes. Although the number of species that have
actually been properly described is limited (ca. 30,000,
including all parasitic taxa (Hugot et al. 2001)), the real
species diversity in the phylum may be one or more orders
of magnitude higher (Lambshead 1993, Coomans 2002),
an idea that has been further strengthened by the recent
discovery that many morphospecies are in fact comple-
xes of several genetically distinct species that are hard or
impossible to discriminate based on morphology (treated
in Section 3.7 ). A substantial part of that diversity and
abundance is present in marine habitats.
Despite their high abundance, the extant biomass of
nematodes in many marine sediments is much lower than
that of bacteria and macrobenthos (Heip et al. 1985), and
the question as to whether nematodes significantly contri-
bute to ecosystem processes, therefore, depends at least
in part on their biomass turnover and activity. Although
novel tools have been adopted to address this issue, subs-
tantial controversy remains on the importance of nemato-
des for ecosystem functioning in marine sediments.
At the same time, nematodes are definitely involved
in particular ecosystem functions, such as decomposi-
tion of organic matter and stabilization of intertidal muds
(see Section 3.11 ). As local diversity of marine nematodes
is typically high – a 10-cm 2 surface area meiocore will
often yield several tens of species – and it is common to
find several congenerous species, or species from closely
related genera, together, nematode community structure
offers a fascinating research model in at least two ways.
First, what are the principal drivers of nematode com-
munity structure and diversity at scales from a few cm to
many hundreds of km? And on a smaller scale: is com-
munity structure principally determined by the environ-
ment, or by interactions with other species? Second, does
the high local diversity of nematodes matter for ecosystem
functioning? How different or similar are nematodes from
a functional perspective, across the often used feeding
types, but also within these guilds? Put differently: what
is the extent of redundancy among nematode species? As
such, nematode communities offer models with which
we can address some of the most fundamental issues in
current ecological research.
More than 25 years have passed since the publication
of the comprehensive and detailed review “ The ecology
of marine nematodes ” (Heip et al. 1985). Even today, this
review is the paper we most frequently refer to in the present
book chapter. Timely though it would have been, our aim
with this chapter was not to produce a new, updated and
complete review of marine nematode ecology, but rather to
provide an accessible overview of current state of the art
research and hypotheses on a number of important aspects
of nematode ecology. Obviously, we have been selective in
our choice of foci as well as of literature citations. We also
present some syntheses and concepts on aspects of nema-
tode assemblage structure that go beyond the state of the
art and are not widely accepted, perhaps not even by all
authors who have contributed to this chapter. In doing
so, we hope to provoke discussion, initiate more in-depth
(meta)analyses of patterns and further science. We dedi-
cate this chapter to the memory of Prof. Dr. Carlo Heip, who
sadly passed away in February 2013, but who continues to
be a source of inspiration and motivation to many a marine
biologist and nematologist.
3.2 Spatial distribution patterns 3.2.1 Horizontal distribution
Spatial distribution patterns of marine nematodes can
be investigated at a mm to global scale. At the micro- or
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110 3 Ecology of free-living marine nematodes
small scale (mm-cm), nematodes show an aggregated
distribution in virtually all marine habitats (Hogue 1982,
Decho & Fleeger 1988, Eckman & Thistle 1988, Hodda
1990, Li et al. 1997, Gallucci et al. 2009) with patch sizes
smaller than 4 – 5 cm in diameter (Findlay 1981, Hogue
1982, Blanchard 1990, Hodda 1990, Gallucci et al. 2009).
The causes for such a clustered distribution are multiple
and depend on complex interactions between biotic and
abiotic factors. Microtopographic irregularities and the
aggregate distribution of food sources are among the most
important factors related to changes in the abundance
and composition of nematode assemblages at the small
scale (Lee et al. 1977, Bell et al. 1978, Montagna et al. 1983,
Blanchard 1990, Rice & Lambshead 1994). Microtopogra-
phic irregularities can be generated by hydrodynamic
action (waves and currents) as well as biological activi-
ties, such as bioturbation and the construction of biogenic
structures by other benthic organisms (Reise 2002). The
response of nematodes to such topographic irregularities
is varied; both increases and decreases in density and
diversity of nematode assemblages have been observed.
For instance, nematodes can accumulate in depressions
or around biogenic structures due to the aggregation of
food sources and/or to the reduction in hydrodynamics
(Findlay 1981, Hogue & Miller 1981, DePatra & Levin 1989).
However, the disturbance and predation generated by the
feeding activities of some organisms can cause reduc-
tions in nematode densities ( Ó lafsson & Elmgren 1991,
Dittmann 1996, Schratzberger & Warwick 1999, Danovaro
et al. 2007) (see Section 3.10 ). Some food sources, such as
microphytobenthos, exhibit aggregate distribution pat-
terns mainly due to the physical-chemical heterogeneity
of the sediment, created by bioturbation and topographic
irregularities. Microphytobenthos spatially correlates with
total nematode abundances, suggesting that they are both
structured by a common driver, or that there is a direct
relationship between them. Microphytobenthos may thus
play a role in structuring nematode small-scale spatial
distribution and vice versa (Montagna et al. 1983, Blan-
chard 1990). Such pronounced small-scale heterogeneity
contributes to generate a micro-distribution of nemato-
des in mosaics. Small-scale patches of organic matter and
disturbance create microhabitats in space and time that
harbor distinct nematode assemblages in different succes-
sional stages, allowing the coexistence of many different
species at very small scales (e.g., Gallucci et al. 2008b).
At the mesoscale (m-km), nematode distribution
patterns have been linked to variations in the physical-
chemical properties of the sediment matrix (e.g., Steyaert
et al. 2003), with sediment grain size being one of the main
factors related to the structure of nematode assemblages.
Muddy and sandy habitats harbor different assemblages
with distinct characteristics: nematodes from sandy habi-
tats tend to be more slender as they have to move through
the interstitial apertures, whereas nematodes from muddy
habitats are generally more robust for burrowing through
the sediment (Tita et al. 1999). Meso-scale distribution
patterns are also influenced by physical-chemical factors
like salinity and tidal exposure. Salinity, in particular, is
one of the main structuring factors in estuarine regions.
Freshwater species are mostly restricted to salinities lower
than 10, whereas several marine species can be found in
almost freshwater conditions or at salinities up to 50 or
higher (Heip et al. 1985), although it is not clear whether
they can truly establish populations under such condi-
tions or merely tolerate them for a limited time. In general,
brackish waters (frequently the intermediate portion of
estuaries) are characterized by a lower number of species
than either marine or freshwater regions (Heip et al. 1985).
This may be due to the often high variability in salinity
at this portion of estuaries. The tides also cause signifi-
cant changes in sediment temperature, water content,
oxygen and hydrodynamics. These alterations generate
horizontal distribution patterns (zonation) and vertical
stratification in accordance with the tidal cycle (Steyaert
et al. 2001). Organisms inhabiting lower intertidal zones
are more prone to suffer from wave action. Those living
in the upper intertidal area are more subject to exposure
during low tide. The intermediate intertidal zone is gene-
rally characterized by a greater equilibrium between wave
action and exposure and, therefore, shows higher abun-
dance and diversity (Nicholas & Hodda 1999, Gheskiere
et al. 2004, Gingold et al. 2010).
Generalizations about the distribution patterns at the
large (global) scale are still problematic as species distri-
bution at such large scales has been meagerly investiga-
ted. Moreover, the comparison among studies is hampered
by the fact that studies are either conducted at the genus
level, or based on a separation into morphospecies. Until
recently, nematodes were thought to exhibit a cosmopoli-
tan distribution. However, with the more advanced mole-
cular techniques, this scenario has changed. Molecular
studies have shown that one morphological species may
actually be a complex of several phylogenetically distinct
species, each with a restricted distribution (e.g., Derycke
et al. 2008b; see Section 3.7 ). Despite evidence for a more
restricted species distribution, there is also evidence of
species with an eurybathymetric distribution (Muthumbi &
Vincx, 1997) and with distributions across multiple scales
or habitats (Derycke et al. 2008b, Bik et al. 2010, Miljutin
et al. 2010). Another large-scale pattern recently shown is
a decrease in nematode species ranges toward the tropics
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3.2 Spatial distribution patterns 111
(Lee & Riveros 2012). Climatic variability has been sugge-
sted as the major cause. More pronounced climatic varia-
bility at higher latitudes would have selected organisms
with wider climatic tolerances and, therefore, wider lati-
tudinal ranges (Stevens 1989). This latitudinal pattern on
species range seems to be consistent across multiple taxa
and environments (Stevens 1989). Finally, food availability
is an important factor influencing species distribution at
large scales. Deep-sea sites with higher content of organic
matter and chloroplastic pigments generally show a lower
turnover of species than oligotrophic sites (Fonseca &
Soltwedel 2007). A possible explanation is that over large
areas, population sizes increase and species become more
widespread when more food is available. This pattern has
been observed for the food-limited deep sea. Whether this
relationship is valid for other environments is a matter for
further research.
3.2.2 Vertical distribution
Nematode abundances are generally higher in the upper
centimeters of the sediment. Although vertical distribu-
tion patterns are rather complex, this higher abundance
in the upper layers is related to food and oxygen gradi-
ents. Sediment oxygen concentration decreases with
depth down to the limit where anaerobic processes start
to dominate. The transition zone between oxygenated
and reduced conditions is called the redox potential dis-
continuity (RPD) layer and appears as a thin grey layer
above the black anoxic sediment (Gray 1981). Because
sulfide ions produced in the anoxic layer are toxic to most
aerobic species, the RPD layer indicates the lower limit of
depth distribution for many species. In coarser sediment,
the RPD layer lies deeper, whereas in finer sediments it
can be restricted to the first cm (or even mm). As a con-
sequence, nematode vertical distribution differs among
sediment types, and vertical gradients are more evident
in finer sediments. For instance, in mud or detritus-rich
sediments, nematodes are generally restricted to the first
few mm or cm (Steyaert et al. 2003). In sandy sediments,
however, nematode assemblages reach deeper layers
and can be found down to depths of 50 cm in reflective
beaches (Renaud-Debyser 1963).
Although the RPD layer represents an ecological
barrier, some nematode species tolerate hypoxic or anoxic
conditions and occur below the RPD layer (Fenchel &
Riedl 1970, Ott & Schiemer 1973). These species show
adaptations that allow them to survive or even thrive in
anoxic environments. For instance, the elongation of the
body, typical of some species living in the deeper layers, is
related to an increase in the ratio of body surface area to
body volume, which facilitates the absorption of oxygen
(Jensen 1986), as well as the epidermal absorption of
dissolved organic matter as an additional food source
(Schiemer et al. 1990, Soetaert et al. 2002). In addition,
an elongated body may increase mobility, allowing short
excursions from the anoxic to the oxic layer (Fonseca et al.
2007, Gallucci et al. 2008b, Vanreusel et al. 2010a). Phy-
siological adaptations, such as the presence of elemental
sulphur granules accumulated in the epidermis, have also
been observed in some nematode species (Thiermann
et al. 2000). Sulfur inclusion in the epidermis temporarily
reduces the concentrations and toxic effect of H 2 S and at
the same time provides an energy deposit for later oxida-
tion under oxic conditions (Thiermann et al. 2000).
The vertical gradient in oxygen concentration is highly
influenced by tides and currents, which directly affect the
oxygenation of the interstitial water. However, bioturba-
tion and bioconstructions generated by other meio-and
macrobenthic organisms modify the hydrodynamics and,
therefore, locally change vertical physical-chemical gra-
dients of the sediment (e.g., Callaway 2006) (see Section
3.10 ). Tubes and holes, for instance, can double the inter-
face area between the water and the sediment. These
structures transport oxygen to deeper sediment layers,
producing a three-dimensional web of oxygenated and
sulfuric microhabitats, where each species can find the
most appropriate microhabitat (Reise 1981, Wetzel et al.
1995, Tita et al. 2000).
In intertidal areas, nematode vertical distribution may
also be controlled by the interstitial water drainage and
the abrupt changes in abiotic conditions during low tides.
Many nematodes are sensitive to low water content in the
sediment (Jansson 1968) and migrate to deeper layers
during low tide. As the tide comes in and the conditions
are reestablished, they return to the surface (McLachlan
et al. 1977, Steyaert et al. 2001). Yet, other species migrate
upward during low tide and downward during submer-
sion (Steyaert et al. 2001). There are several reasons why
this behavior may be advantageous: increased diatom
production and biomass build-up at the sediment surface
during tidal exposure (Guarini et al. 1997) may offer high
food availability to grazers. At the same time, by making
an inverse vertical migration relative to other nematodes,
including predacious species (e.g., Enoploides longispi-culosus ), predation risk may be reduced (Gallucci et al.
2005). Such inverse behaviors of different nematode
species may ultimately allow their coexistence. Finally,
temporary factors may induce nematode vertical migra-
tions in the sediment. For instance, heavy rainfall on tidal
flats may cause drastic changes in salinity, stimulating the
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112 3 Ecology of free-living marine nematodes
downward migration of more sensitive species (Steyaert
et al. 2001). Strong currents or waves may also trigger
the downward migration of species to avoid suspension.
However, the deposition of a phytoplankton bloom may
induce the upward migration of opportunistic nematode
species, such as Sabatieria sp. , to the surface (Franco
et al. 2008b).
3.3 Nematode abundance and diversity across marine habitats
Abundance, i.e., the number of individuals in a given area
(or volume), is widely used as an important characteristic
of biological communities to infer relationships between
the community and its environment. There is a close posi-
tive, often linear link between nematode abundance and
community biomass, governed by the size of individual
nematodes, which may vary across habitats in response
to resource availability. Shallow-water nematodes, for
instance, are generally much larger than their deep-sea
counterparts, owing to the generally higher food input
compared to the deep sea. Hence, nematode abundance is
often used as a proxy for community biomass and varies
from a few to several thousand individuals per 10 cm ² .
Exceptionally, > 10,000 individuals per 10 cm ² are obser-
ved in organically enriched habitats such as cold seeps
(Van Gaever et al. 2006), polar coastal areas (Vanhove
et al. 1999) or estuarine mudflats (see references in Heip
et al. 1985).
Nematodes represent one of the most diverse groups
of organisms in the marine realm, with species richness
estimates ranging from 10,000 up to > 1,000,000 species
(Mokievsky & Azovsky 2002, Lambshead & Boucher
2003). The latest estimation resulting from a globally con-
certed effort to assess diversity for all marine taxa showed
that only 14% of the estimated 50,000 free-living nema-
tode species are currently known (Appeltans et al. 2012).
Diversity can be measured at different spatial scales: from
local diversity ( α diversity), turnover diversity or diversity
between locations ( β diversity), to diversity over larger
regions, such as geographical areas or multi-ocean basin
areas ( γ diversity and higher). Nematode diversity has been
investigated at various spatial scales in several regions and
habitat types (e.g., Hodda 1990, Gambi & Danovaro 2006,
Fonseca et al. 2007, Schratzberger et al. 2008, Danovaro
et al. 2009a, Van Gaever et al. 2010). The discovery of dif-
ferent diversity patterns has instigated much debate about
which patterns are associated with which spatial scales
(see Section 3.2 ), and which processes are responsible
for the patterns observed (Fonseca et al. 2010, Ingels &
Vanreusel 2013). However, one concurrent result among
studies is that the scale of cm to m is the most important
source of variability. This small-scale variability is either
seen as a response to unmeasured microhabitat hetero-
geneity or strong species interactions, issues that have
been weakly explored in nematode ecology (see, e.g.,
Gallucci et al. 2005).
For nematodes, the most widely used diversity
descriptor is species or genus richness, as it gives a clear
and simple indication of how many species or genera
are present in a sample or area. One shortcoming of this
approach is that this measure is heavily dependent on the
sample size or area that is being investigated. Bigger sam-
pling cores will yield more species per sample, and more
samples result in more species collected. This positive
linear relationship levels off where additional material
does not add extra species to the total count. Nematode
ecological studies rarely reach that point and are gene-
rally dealing with incomplete species inventories. To over-
come this shortcoming, the expected number of species
(ES) or genera can be calculated based on a given number
of individuals. This diversity measure allows for the com-
parison of diversity among sets of samples of different
sizes, and among sites characterized by different samp-
ling efforts (Sanders 1968, Hurlbert 1971). Complementary
to species or genus richness, many other diversity indices
(e.g., Simpson, Shannon-Wiener, Pielou ́ s evenness) and
richness estimators (e.g., Chao, Ugland-Gray-Ellingsen)
have been proposed and are regularly used to describe
nematode assemblages (Clarke & Gorley 2006). The main
advantage of the diversity indices over richness is that they
give a better picture of the dominance and evenness of the
species by considering the relative abundance of each
taxon. Several reference works provide a comprehensive
overview with examples of nematode applications (Heip
et al. 1998, Boucher & Lambshead 1995, Lambshead et al.
2000, Warwick & Clarke 2001, Magurran 2004, Magurran
& McGill 2011).
Nematode abundance and diversity vary widely
among different habitats. This high variability is often
ascribed to the complex interactions among different
abiotic and biotic factors, such as food availability (quan-
tity and quality) and disturbance processes (physical,
chemical and biotic) ( Fig. 3.1 ). In addition, biological
interactions, physiological tolerance levels and adapta-
bility, life histories and dispersal processes may explain
abundance and diversity patterns at small spatial scales
within habitats. In both shallow- and deep-water environ-
ments, nematode abundances and diversity are associated
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3.3 Nematode abundance and diversity across marine habitats 113
with physical disturbance and food availability, with both
quality and quantity playing a role (e.g., Danovaro et al.
2002). For instance, enriched estuarine muddy sediments
are characterized by high densities ( > 3,000 ind. per 10 cm ² )
and few dominant species per sample (Heip et al. 1985),
whereas at oligotrophic sites (e.g., abyssal plains in the
eastern Mediterranean or sediments under permanent ice-
cover), nematode abundances may be severely depressed
with only a few species coexisting (Heip et al. 1985,
Netto et al. 1999, Vanreusel et al. 2000, Lampadariou &
Tselepides 2006, Fonseca & Soltwedel 2007, Danovaro
et al. 2008b). Species richness is usually high at the upper
slope (Boucher & Lambshead 1995, Vanaverbeke et al.
1997, Vanhove et al. 1999, Gallucci et al. 2008a, Fonseca &
Soltwedel 2009) and in deep-sea sediments with secondary
hard substrates, like manganese nodules and cold-water
corals (Vanreusel et al. 2010b). In these highly diverse
habitats, species richness is usually above 60 species per
sample (e.g., a corer 3.5 cm in diameter and 10 cm long).
In sandy coastal habitats, nematode abundances range
between 1000 – 3000 individuals per 10 cm ² , and species
richness at the sample scale (i.e., one corer) typically varies
between 30 and 40 (Gheskiere et al. 2004, 2005, Maria et al.
2012). Nematode abundances at continental shelves vary
from 500 to 2000 individuals per 10 cm ² (Muthumbi et al.
2004, Netto et al. 2005), whereas species richness ranges
between 30 – 50 (Vanhove et al. 1999). In the abyss, where
undisturbed muddy conditions prevail, faunal abun-
dance and species richness are tightly related to resource
availability. For example, abyssal sites under productive
water masses show higher species richness than sites
under oligotrophic waters (Lambshead et al. 2002,
Danovaro et al. 2008b). Contrasting to photosynthetic
production-based food webs are chemoautotrophically
driven ecosystems. Cold seeps, for instance, are fuelled
by chemical energy and are often characterized by very
high nematode densities (more than 11,000 individuals
per 10 cm ² ), due to the proliferation of one to a few suc-
cessful tolerant nematode species. Sometimes, however,
both densities and diversity may be depressed (Van Gaever
et al. 2006, 2009, Vanreusel et al. 2010a, Guilini et al. 2012)
despite the presence of abundant chemical energy. Although the response of nematode assemblages to
environmental and biological changes and habitat modi-
fication is highly complex and variable, some general
diversity and abundance patterns have been observed,
and several hypotheses or schematic models have been
applied to explain these patterns and understand the
underlying processes. For example, the Intermediate
Disturbance Hypothesis (IDH) postulates that maximum
diversity will be found at intermediate disturbance levels,
an environment where disturbances are not too strong
and frequent, allowing communities to diversify, but fre-
quent and strong enough to prevent competitive exclu-
sion (Connell 1978). Maximum diversity would therefore
be found at a state of non-equilibrium. The processes
governing disturbance-diversity relations are manifold,
and may act in the form of hydrodynamic or sediment
activity, organic enrichment, reduced oxygen availability
or high-impact organism interactions (see Section 3.6 ).
For nematodes, the validity of the IDH has been reported
for several marine habitats. For example, several authors
Fig. 3.1 : Major marine habitats arranged along hypothetical gradients of resource availability and physical disturbance.
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114 3 Ecology of free-living marine nematodes
observed mid-intertidal peaks in nematode diversity
consistent with the IDH (Armonies & Reise 2000, Gheskiere
et al. 2004, Gingold et al. 2010), and Schratzberger et al.
(2009) reported the validity of the IDH for various types
of sediment disturbance. Highest nematode diversity at
intermediate physical disturbance was also reported in
experimental setups (Austen et al. 1998, Schratzberger &
Warwick 1998). Finally, diversity or species richness peaks
at bathyal depths (Boucher & Lambshead 1995) ( Fig. 3.2 ),
a pattern comparable with that of macrofauna (Rex et al.
2005). The decrease of disturbance with increasing water
depth may support the hypothesis of a mid-water peak in
the framework of the IDH. In the same context, the IDH may be seen as com-
plementary to the Intermediate Productivity Model (IPM;
Grime 1973), for which food input plays an imperative
role. The combination of IDH and IPM led to another
influential disturbance-diversity theory in ecology, the
Dynamic Equilibrium Model (DEM; Huston 1979, 1994),
which predicts that the level of disturbance associated
with maximum diversity will depend on the level of pro-
ductivity (Svensson et al. 2012). Strong disturbance is thus
required to counteract competitive exclusion at high rates
of growth and productivity, whereas a relatively weak dis-
turbance is sufficient to prevent competitive exclusions at
lower growth rates. The DEM has repeatedly been applied
to explain nematode diversity patterns (e.g., Warwick &
Gee 1984, Austen & Widdicombe 2006, Ingels et al. 2011c).
Particularly, the effect of water depth on nematode
communities is often investigated in combination with
productivity, because food input (organic matter flux)
is reduced at greater depths. In contrast to the diver-
sity peak at bathyal depths (Boucher & Lambshead
1995), nematode abundance generally decreases with
Fig. 3.2 : Generalized trends in nematode abundance (straight line) and diversity (curved line) with increasing water depth.
increasing water depth (Mokievsky et al. 2007) ( Fig. 3.2 ).
This bathymetrical trend can be expected along any
slope, but exceptions occur when changes in producti-
vity or disturbance take place along the bathymetrical
transect. Trenches, canyons, marginal ice-zones and
oxygen minimum zones are examples of habitats where
such impacts are regularly observed. Oxygen minimum
zones, for instance, may show lower nematode abun-
dances (Muthumbi et al. 2004) and richness than expec-
ted (Guilini et al. 2012), although Cook et al. (2000)
observed that nematode abundance did not suffer from
an oxygen-limited environment. At marginal ice-zones,
abundance and species richness are significantly lower
under the ice pack than in ice-free sediments (Fonseca
& Soltwedel 2007). Geological faults like trenches and
canyons can be either species poor (Danovaro et al.
2009a, Ingels et al. 2009) or rich (Ingels et al. 2011c),
compared to adjacent slopes at the same depth, because
of the accumulation of food resources and the associated
biogeochemical changes or the impact of hydrodynamic
or sedimentary disturbance. These examples suggest
that abundance and diversity patterns change as soon
as the balance between disturbance and resource avai-
lability is altered.
Latitudinal and longitudinal patterns in nematode
abundance and species richness have received much
less attention compared to bathymetrical patterns (e.g.,
Lambshead et al. 2000, Rex et al. 2001). Along coastal
areas, no latitudinal pattern in nematode abundance
could be discerned, probably as a consequence of
high environmental variability among coastal habitats
(Mokievsky et al. 2007). However, a latitudinal pattern has
been detected in a regional dataset from sandy beaches
along the Chilean coast (18 ° S – 42 ° S). Sandy beach nema-
todes showed a constant decrease in species richness with
increasing latitude (Lee & Riveros 2012). It has been hypo-
thesized that the pattern along the Chilean coast is pro-
bably driven by sea-surface temperature, which decreases
with increasing latitude. For the deep sea, two different
trends have been observed. Based on a meta-analysis,
abundance of deep-sea nematodes showed a unimodal
pattern peaking at temperate regions (Mokievsky et al.
2007). However, regional datasets, one along the Pacific
abyssal plain (Lambshead et al. 2002) and the other
restricted to the North Atlantic (Lambshead et al. 2000),
suggest a bimodal pattern with abundance and diversity
peaking around the Equator and temperate latitudes. The
reasons for these two latitudinal patterns are unclear. For
instance they could be due to the difference in the geogra-
phical coverage of the datasets, differences regarding the
analytical methods or even differences in the treatment
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3.3 Nematode abundance and diversity across marine habitats 115
Fig. 3.3 : Unimodal relationship (middle line) between (A) nematode biomass (log10(1+Biomass)) and species richness (ES(51)) (R:0.613, p<0.0001) and (B) nematode abundance (log10(1+abundance)) and species richness (ES(51)) (R:0.625, p<0.0001) across deep-sea regions worldwide. Polynomial quadratic function fitted. Inner lines: 95% confidence limits; outer lines: 95% prediction limits. Data used from Leduc et al. (2012).
of the datasets. However, one concurrent result among
latitudinal and longitudinal regional-scale studies on
deep-sea nematodes is that patterns are usually associa-
ted with sea-surface productivity, i.e., less productive lati-
tudes and longitudes harbor fewer individuals and less
species than more productive latitudes and longitudes
(Lambshead et al. 2002, Danovaro et al. 2008b, Fonseca
et al. 2010). Whether this trend can be extrapolated for the
entire globe is still questionable.
Evidence so far suggests that abundance and richness
patterns are tightly linked. The shape of this relation is
conceptually unimodal; sites with extremely low abun-
dances are represented by few species, and an increment
in abundance entails an increase in the number of coexis-
ting species ( Figs. 3.3 and 3.4). The initial high increment
at relatively low abundances culminates where com-
petitive exclusion starts. High-density sites are usually
characterized by few species that tolerate the specific con-
ditions. For example, a large range of deep-sea samples
has been compared across a wide range of productivity
levels, resulting in a clear unimodal diversity-abundance
and diversity-biomass relation ( Fig. 3.3 ; data available in
Leduc et al. 2012). The conceptual model shown in Fig.
3.4 visualizes the same unimodal nematode abundance
and species richness pattern across different marine envi-
ronments. This model is based on the DEM proposed by
Huston (1994) and the literature cited in this section. It
gives a general overview about abundance/diversity pat-
terns across multiple habitats, in relation to productivity
and disturbance, as predicted by the DEM. Certain habi-
tats are displayed more than once as they may be charac-
terized by a variety of environmental variables that act in
concert ( Fig. 3.4 ). Although the predictions of IDH and DEM offer plau-
sible explanations for observed patterns, resource hete-
rogeneity (RH) and habitat connectivity (HC) are two
other mechanisms that may explain diversity patterns
(Leibold et al. 2004, Logue et al. 2011). The RH hypothe-
sis predicts that local richness increases with increasing
RH and, hence, is not necessarily a response to producti-
vity regimes and disturbances, but results from species-
specific niche adaptations. As a result, multiple species
coexist by niche segregation. In this context, the high
diversity observed at bathyal depths, for instance, would
be a consequence of higher RH. Alternatively, intense
competition for food in the resource-poor deep sea may
result in smaller realized niches and, hence, more species
per unit area compared to shallower waters (Mokievsky
& Azovsky 2002, Snelgrove & Smith 2002). However, the
few small-scale studies and manipulative experiments at
bathyal depths have not been conclusive (Gallucci et al.
2008a, Hasemann & Soltwedel 2011), and there is contro-
versy about the degree of resource selectivity vs. flexibility
in marine nematodes (see Section 3.8 ). As expected by the
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116 3 Ecology of free-living marine nematodes
RH hypothesis, the presence of biogenic structures in the
deep sea promotes habitat heterogeneity and enhances
the number of coexisting species (Levin 1991, Hasemann &
Soltwedel 2011). However, it has also been observed that
under experimental exclusion of physical disturbances
from megafauna, several species were favored rather than
few species achieving a high dominance (Gallucci et al.
2008a). This contradicts the predictions of the RH hypo-
thesis, but scale may be important to correctly interpret
the mechanisms generating diversity patterns.
Dispersion is another potentially important mecha-
nism driving diversity patterns of marine nematodes at
the local scale. Recruitment from adjacent habitats may
importantly contribute to extant local diversity (Logue
et al. 2011). Nematodes are poor swimmers, but they may
passively disperse over large distances through the water
column (e.g., Palmer 1988, treated in Section 7 ); even weak
currents can transport significant numbers of nematodes
(Boeckner et al. 2009, Thomas & Lana 2011). However,
to understand the effect of connectivity in shaping local
species richness, species range and turnover have to be
included into the analysis (Leibold et al. 2004). High tur-
nover, or low habitat connectivity (HC), indicates that
local diversity is principally shaped by local conditions
and species are not exploring all potentially suitable sites.
In this situation, each set of species at the local scale repre-
sents a small part of the total species pool. By contrast,
low turnover, or high HC, indicates that all species are
moving across all sites and are consequently temporally
present at sites exhibiting less suitable conditions. Such
movement across sites enhances local diversity in rela-
tion to the total species pool. The few studies on marine
nematodes that have attempted to analyze turnover rates
have shown that turnover was lower at lower latitudes
(Lee & Riveros 2012) or in organically enriched sediments
(Fonseca & Soltwedel 2009). Their conclusion was that
warmer temperatures and more food increased species
population sizes, which in turn increased the number
of common species between samples and promoted an
increase in the number of coexisting species. In contrast,
colder and impoverished regions were in general less
diverse and characterized by species with smaller popula-
tion sizes, large numbers of singletons and high turnover
between samples.
All the above-mentioned hypotheses explain different
underlying mechanisms; they are not mutually exclusive
and may operate simultaneously to generate diversity pat-
terns (Chase & Myers 2011). Moreover, an adequate under-
standing of local diversity patterns requires regional pat-
terns to be taken into account too (Gray 2002). Nematode
diversity at regional scales has been comparatively little
explored (Fonseca et al. 2010, Gambi et al. 2010, Vanreusel
et al. 2010b, Lee & Riveros 2012, Ingels & Vanreusel 2013),
and whether regional variations in species richness affect
local species coexistence is one of the unexplored topics
of marine nematode ecology.
Fig. 3.4 : Conceptual model of the relationship between nematode abundance and species richness/diversity in relation to habitat types, physical disturbance and resource availability. Disturbance and resources are parallel measures. The gradient indicates the hypothetical balance between them. Note that a habitat (e.g., abyss), showing distinct disturbance or productivity regimes, is placed several times along the gradient.
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3.4 Nematode biomass patterns 117
3.4 Nematode biomass patterns 3.4.1 Nematode individual biomass patterns
Much attention is given to the distribution patterns of
nematode individual biomass across habitats and along
gradients (Udalov et al. 2005, Soetaert et al. 2009).
Nematode individual biomass is fundamental for the
interpretation of important characteristics of nematode
communities: it is essential to assess standing stocks
(often calculated as the product of densities and average
individual biomass), production/biomass (P/B) ratios,
contribution to total sediment oxygen consumption, respi-
ration (Franco et al. 2010) or estimates of carbon demands
(Guilini et al. 2010, Ingels et al. 2010, Braeckman et al.
2011a). One of the largest gradients in the marine realm
is the transition from shelf seas to the deep-sea, along the
continental slope. Nematode individual biomass decre-
ases with depth, as revealed by meta-analyses based on
large datasets (Udalov et al. 2005, Soetaert et al. 2009).
Whereas Udalov et al. (2005) found a linear relationship
between individual biomass and bathymetric depth,
Soetaert et al. (2009) observed an exponential one: for
every doubling in water depth, nematode individual
biomass decreased 19% (Soetaert et al. 2009). However,
bathymetric depth co-varies with other factors, as both
authors also stress that (1) bathymetric depth is a proxy
for the flux of organic material (OM) reaching the seafloor,
and (2) other factors (e.g., grain size) are important struc-
turing variables as well.
OM supply to the seafloor has both direct (i.e.,
provision of food) and indirect (e.g., altering the oxic
conditions) effects on nematode individual biomass
(Soetaert et al. 2009). The direct effect of diminishing OM
input is a decrease in nematode individual body weight
(Udalov et al. 2005, Soetaert et al. 2009). The fact that
organic matter flux, rather than depth per se, structures
nematode individual biomass, is supported by the obser-
vation that nematode individual biomass is lower in oli-
gotrophic deep-sea sites compared to eutrophic deep-sea
sites at similar depths (Vanreusel et al. 1995, Sommer &
Pfannkuche 2000, Brown et al. 2001). Similarly, nematode
individual biomass is higher at the submarine Nazar é
Canyon (Western Iberian Margin) in comparison to adja-
cent continental slope stations at similar depths, again
reflecting the higher organic matter content in the canyon
sediments (Ingels et al. 2009).
The structuring role of grain size is not straightfor-
ward either, as grain size is correlated with bathymetric
depth as well (Udalov et al. 2005, Soetaert et al. 2009).
Higher variation in nematode individual biomass at the
shelf sea could be observed, related to a greater variety of
sediment composition (Udalov et al. 2005, Soetaert et al.
2009). The effect of grain size on nematode individual
biomass becomes apparent when comparing two stations
close to each other but with contrasting sediments, sub-
jected to the same primary production regime (Soetaert
et al. 2009): nematode individual biomass was investi-
gated during a seasonal sampling at both a fine (median
grain size: 185 μ m) and medium (median grain size:
329 – 361 μ m) sandy station. Nematode individual biomass
values assessed in medium sand represented only 43%
(October) to 70% (February) of the values encountered
in fine sand (Soetaert et al. 2009). However, grain size
structures nematode individual biomass only indirectly:
organic matter content in medium sand is low, because the
high permeability of the sediment promotes rapid organic
matter mineralization, whereas there is a build-up of
organic matter in fine, non-permeable sediments (Franco
et al. 2007). Also in muddy sediments, large variations
in nematode individual biomass occurred ( Schratzberger
et al. 2008). At two muddy locations in UK waters (Celtic
Deep and NW Irish Sea), threefold differences between
the lowest and highest mean individual biomass values
could be observed (Schratzberger et al. 2008). Again, local
differences (i.e., hydrodynamic disturbances, food avai-
lability) seemed to be reflected in nematode individual
biomass patterns. Unfortunately, general comparisons
of individual nematode biomass in muddy sediments are
hampered by the scarcity of extensive datasets and the
fact that data are often obtained using different methods
[i.e., different lower sieve sizes (63 μ m instead of 38 μ m),
no upper sieve, arithmetic instead of geometric means].
Although many studies treated bathymetric depth
and grain size related to nematode individual biomass,
seasonality has often been overlooked. However, sedi-
mentation of annual spring phytoplankton blooms provi-
des the sediment-inhabiting organisms with labile organic
matter. In coastal sediments at the Belgian part of the
North Sea (BPNS), nematode individual biomass increa-
sed up to 34% (medium sand) and 40% (fine sand) after
sedimentation of a spring phytoplankton bloom (Franco
et al. 2010). Although this increase is actually more than
one magnitude lower compared to the variation across the
bathymetric range (Soetaert et al. 2009), it bears impor-
tant consequences for local sediment metabolism (Franco
et al. 2010). The increase of nematode individual biomass
after a sudden food pulse may be the result of (1) many
juveniles growing to size at maturity, or (2) a switch in
species composition or (3) a combination of both. In the
coastal waters of the BPNS, the increase in nematode indi-
vidual biomass in medium sands seemed to be related to
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118 3 Ecology of free-living marine nematodes
a shift in species composition: densities of stout (short,
thick) nematodes increased fast after the sedimentation,
whereas this was not the case for the more slender nema-
todes (Vanaverbeke et al. 2004). However, it is not cur-
rently possible to make general conclusions based on this
observation, as more detailed data are still lacking.
3.4.2 How to calculate individual biomass
Estimates of mean individual nematode biomass should be
based on correct sampling, treatment of samples and cal-
culation methods. Although sampling gear and sampled
surface do not affect nematode individual biomass values,
sieve size and core penetration depth clearly do (Udalov
et al. 2005, Leduc et al. 2010). Sediment should be coll-
ected to a depth of at least 5 cm, and nematodes need to
be retained on the smallest sieve size possible to obtain
a nematode biomass distribution including small and
juvenile nematodes (Leduc et al. 2010). Apart from samp-
ling, calculation of mean biomass values is important as
well. Usually, distributions of nematode length, width and
the corresponding biomass are skewed toward smaller
values; therefore the presence of a few large nematodes
can heavily impact the traditionally calculated arithmetic
mean (Soetaert et al. 2009). To overcome this problem, it
is advised to calculate the geometric mean, which is based
on log-transformed data, and to use this geometric mean
for statistical analyses (Soetaert et al. 2009). However, sci-
entists are generally interested in the mean of untransfor-
med values, in order to calculate total biomass. However,
when back-transforming the geometric to the arithmetic
mean, the mentioned skewness to smaller sizes has to
be taken into account. The mean of the arithmetic distri-
bution ( μ a ) is estimated as μ
a = exp( μ
lny ) – exp(0.5s ²
lny ),
where μ lny
and s ² lny
are the estimated mean and variance
in logarithmic units (Finney 1941). The correction factor
exp(0.5s ² lny
) is, on average, 2.1 for nematode biomass, 1.15
for nematode length and 1.1 for nematode width (Soetaert
et al. 2009).
An alternative method to investigate nematode indivi-
dual biomass patterns is to construct nematode biomass
spectra describing the distribution of nematode indivi-
dual biomass values (Tita et al. 1999, Vanaverbeke et al.
2003). By doing so, measurements are not summarized
in a single average value and its associated variance, but
illustrated by the nematode biomass spectra. Therefore,
the presence of a few large individuals in a sample other-
wise populated by small nematodes does not necessarily
lead to a strongly increased mean individual biomass
value (Tita et al. 1999).
3.4.3 Nematode total biomass patterns
Nematode total biomass can be calculated (1) as the sum
of all individual biomass values, or (2) as the product
of the mean individual biomass and nematode density.
Unfortunately, studies integrating data on total nema-
tode biomass are very scarce, but it can be assumed that
recently described trends on total meiobenthic biomass
(Gambi et al. 2010, Wei et al. 2010) are valid for nematodes
as well, based on the fact that nematodes are the domi-
nant meiobenthic taxon in terms of abundance (60 – 100%;
Gambi et al. 2010). As both total nematode densities and
nematode individual biomass decrease with bathymetric
depth (Vincx et al. 1993, Soetaert et al. 2009, Gambi et al.
2010), total nematode biomass patterns mirror the trends
for individual biomass described above; a decrease in
nematode total biomass of about 35% could be observed
with every doubling of water depth (Soetaert et al. 2009).
A global analysis of meiobenthic biomass data taken at
many different sites in the Mediterranean Sea (Gambi
et al. 2010) revealed that (1) depth and food sources are
the most important factors explaining total biomass pat-
terns when depth exceeds 2000 m, (2) between 1000 m
and 2000 m depth, food sources alone explain most of the
variance and (3) at depths shallower than 1000 m, habitat
type becomes more important. The increasing impor-
tance of habitat type at shallower depths reveals that the
local environment has an important effect on nematode
total biomass. This has been observed outside the Medi-
terranean Sea as well, in shallow subtidal sediments in
the BPNS (Franco et al. 2010) and when comparing total
nematode biomass values from canyon and adjacent open
slope sediments at similar depths.
3.5 Nematode community composition patterns across marine habitats
Studies describing nematode assemblage structure mostly
identify specimens to genus level or separate them into
putative species, and this for several reasons: first, iden-
tification to genus level using general pictorial keys (e.g.,
Warwick et al. 1998) is not very difficult; second, apart from
some well-studied geographical areas, nematode assemb-
lages often still comprise a substantial portion of unde-
scribed species; third and most importantly, genus-level
identification has been shown to be equally powerful in
detecting and describing significant ecological patterns as
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3.5 Nematode community composition patterns across marine habitats 119
species-level identification (Warwick 1988, Somerfield &
Clarke 1995, Vanaverbeke et al. 1997, Vanreusel et al. 2000,
Fonseca & Soltwedel 2007, Schratzberger et al. 2007). This
may in part be because, in an assemblage, many genera
are often represented by single or few species, although
there are many exceptions to this. Moreover, the use of
both genera and species has proven more powerful in
detecting patterns than either single or combinations of
functional groups (multiple trait analysis) (Somerfield &
Clarke 1995, Schratzberger et al. 2007). Although several
studies have investigated trends in the diversity of marine
nematodes (see Section 3.3 ), only two have attempted to
systematically compare the composition of assemblages
across marine habitats.
The first study reviewed the dominant species over
five major marine biotopes: estuaries and brackish water,
marine sandy beaches, shallow subtitdal, deep sea and
epiphyton (Heip et al. 1985). The second study compa-
red the fauna across ten deep-sea habitats: continental
shelf, slope, abyss, cold seep, thermal vent, cold water
coral, manganese nodule, canyon, seamount and trench
(Vanreusel et al. 2010b). Both studies evidenced that
despite a high environmental heterogeneity among and
within habitats, there are widespread taxa (e.g., the genus
Daptonema ) occurring in nearly all habitats on the one
hand, and taxa that are restricted to a particular habitat or
set of habitats on the other.
3.5.1 Coastal habitats
The families Comesomatidae, Linhomoeidae and Desmo-
doridae are more frequent and abundant in enriched estu-
arine sediments with low oxygen levels. Members of these
families inhabiting such reduced sediments are usually
long and slender, and possess short setae and (very) small
buccal cavities. Typical Linhomoeidae of estuarine areas
are Terschellingia, Metalinhomoeus and Paralinhomo-eus (Heip et al. 1985). In reduced sediments, the family
Desmodoridae is often represented by genera such as
Desmodora, Spirinia, Stilbonema and Catanema , and
Comesomatidae by the genus Sabatieria . Although
members of these families may be very tolerant to anoxic
conditions (Jensen 1987b, Steyaert et al. 2005, 2007,
Fonseca et al. 2011), these characteristics may be partly
species- and/or context-specific. As an example, Saba-tieria spp. may occur in permanently hypoxic or anoxic
sediments (Vanreusel et al. 2010a) and have been known
to survive for more than a year in unaerated Baltic Sea
sediment aquaria (Aleksander Drgas, personal communi-
cation), but abundances of Sabatieria pulchra decreased
ca. threefold during a 1-week incubation in hypoxic and
anoxic sediment cores (Steyaert et al. 2007). Whether such
differences depend on species identity or on specific envi-
ronmental characteristics remains unknown, and so do
the mechanisms to tolerate such stressful conditions. For
instance, long and slender taxa may have a higher effici-
ency of obtaining oxygen as a consequence of their com-
paratively large surface/volume ratio (Jensen 1987b).
In sandy beaches, the family Xyalidae is often among
the most frequent taxa; it is usually represented by more
than one genus, and some genera also by multiple species
(Heip et al. 1985, Gheskiere 2005). Characteristic sandy
beach genera of Xyalidae comprise Xyala, Omicronema, Steineria, Paramonhystera, Pseudosteineria, Rhyncho-nema, Daptonema, Theristus and Metadesmolaimus (Heip
et al. 1985, Nicholas & Hodda 1999, Lee & Riveros 2012).
Other commonly encountered genera in clean sands are
Chromadorita, Bathylaimus, Nudora, Odontophora, Para-canthonchus, Paracyatholaimus and Microlaimus (Gingold
et al. 2010, Lee & Riveros 2012, Fonseca & Fehrlauer-Ale
2012). Several of these genera may have developed adap-
tations to cope with physical disturbances (caused by,
e.g., wave actions) and/or with low resource availability,
even though several of the above-listed Xyalidae are also
common in organic-rich, silty sediments. A robust body,
such as observed for Paracyatholaimus and Bathylaimus ,
could facilitate movement through interstitial spaces. The
long somatic setae commonly observed in Xyalidae may
help attach to sediment grains, avoiding resuspension, or
facilitate a quick settlement after resuspension.
Fine sandy beach sediment is physically less
disturbed, richer in organic matter, microphytobenthos
and biomass. Such abundance in food items in general
favors nematode genera such as Ascolaimus, Axonolai-mus, Trissonchulus, Enoplolaimus and Oncholaimellus
(Gheskiere et al. 2005, Maria et al. 2012). The latter three
genera are predators or facultative predators (Moens &
Vincx 1997), feeding types that also tend to abound on
coarse sandy beaches. Coarse beaches are usually cha-
racterized by strong hydrodynamics and higher relative
abundances of other meiofaunal groups, such as polycha-
etes, oligochaetes, nemertines and mollusks (Giere 2009).
Among the nematodes, predators and genera capable of
adhering to sediment grains tend to be abundant, typical
representatives being Choniolaimus, Latronema, Oxyon-chus, Pomponema and “ aberrant ” forms such as Tricoma ,
Draconematidae and Epsilonematidae (Heip et al. 1985).
Draconematidae and Epsilonematidae not only possess
caudal glands but also several rows of ambulacral setae,
each connected to a secretory gland. Both structures allow
adherence to sediment particles and a caterpillar-like
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120 3 Ecology of free-living marine nematodes
creeping movement over sediment grains. Species belon-
ging to the genus Tricoma also have glands secreting
sticky mucus to aggregate sediment particles around the
body. This “ armature ” may protect them against predators
and increase their body weight and thereby their settling
velocity after erosion from sediments.
Several nematodes, particularly belonging to Chro-
madoridae and Oncholaimidae, are characteristic repre-
sentatives of “ surface ” assemblages. These may comprise
surficial muddy intertidal flat sediments covered with
microphytobenthos biofilms (where a genus like Ptycho-laimellus typically abounds; Steyaert et al. 2003, Van
Colen et al. 2009), but also secondary substrates, like
macroalgae and other hard substrates in general (Heip
et al. 1985). These same groups have also been reported to
be highly abundant on hard substrata (Atilla et al. 2003,
Gobin 2007) and as early colonizers of artificial plates
(Fons ê ca-Genevois et al. 2006). The close association of
Chromadorids with superficial sediments and secondary
substrates is probably related to their feeding on biofilms
(treated in Section 8 ). The often large-bodied Oncholai-
midae are omnivores or facultative predators, and several
representatives have been shown to be rapid dispersers
(Lorenzen et al. 1987, Prein 1988), which may perhaps
explain their prominence on exposed substrata. In any
case, the abundance of large-bodied, predatory or omni-
vorous nematodes on secondary substrata seems to be
a rather general phenomenon that deserves more atten-
tion. Enoplus, Rhabdocoma, Thoracostoma, Phanoderma
and Symplocostoma are some typical genera commonly
found on the surface of Spartina and kelp holdfasts (Heip
et al. 1985). Kelp and Spartina are known to support high
abundances of amphipods, Acari and other small crusta-
ceans (Rutledge & Fleeger 1993, Arroyo et al. 2004), which
in turn would serve as food items to these large nemato-
des. However, non-predatory large-bodied nematodes like
Anticoma are also common on secondary substrata (Heip
et al. 1985), suggesting that size rather than feeding type
may hold the key to explain why these large genera tend to
be so prominent in these habitats.
3.5.2 Deep-sea habitats
As observed for the coastal habitats, Vanreusel et al.
(2010b) showed that each deep-sea habitat could be dis-
tinguished by a different set of taxa, with exception of
canyon and seep systems where the genera composition
was highly variable. Slope and shelf, for instance, shared
several genera and differed mostly in the relative abun-
dance of the dominant taxa. Slope assemblages were
mainly characterized by higher relative abundances of
Thalassomonhystera, Acantholaimus, Halalaimus and
Daptonema , whereas the dominant taxa at shelf sites were
Sabatieria and Microlaimus . Deep-sea corals were cha-
racterized by taxa belonging to the family Epsilonemati-
dae, Draconematidae and the genus Desmoscolex , taxa
adapted to crawl over and attach to surfaces. Seamounts
were mainly characterized by the presence of Desmodora, Ceramonema and Richtersia . Nodule areas showed the
highest relative abundance of Theristus , whereas at the
abyss Acantholaimus, Thalassomonhystera and Halalai-mus accounted for nearly 45% of the assemblages. Vent
samples were also characterized by a very high dominance
of Thalassomonhystera, Halomonhystera and Anticoma .
Seeps and canyons also showed different assemblages
when compared to adjacent sediments; however, no con-
sistent composition over multiple seeps or canyons was
detected, given the lack of uniformity among the different
sites. The main conclusion of this study is that there is a
tight association between nematode genera composition
and habitat and that habitat type is more important than
any other large-scale structural factor, such as geographi-
cal region or latitude (Vanreusel et al. 2010b).
The above very brief overview suggests two broad
conclusions: (1) nematode genera and species composition
of marine nematodes is largely driven by habitat type and
local environmental conditions rather than by geographi-
cal area or latitude, and (2) parallel nematode assemblages
may thus occupy similar habitats around the globe. Both
these conclusions are in agreement with patterns for other
small organisms and partly support the “ everything is eve-
rywhere ” (EiE) hypothesis, i.e., that everything that is small
could be everywhere provided local environmental condi-
tions are suitable (Fenchel & Finlay 2004). However, it is
questionable to what extent this hypothesis explains nema-
tode species composition spatial patterns (Fontaneto 2006).
For example, although there is evidence for the existence of
cosmopolitan species (Bik et al. 2010), supporting the EiE
hypothesis, there is also evidence for high levels of ende-
mism (Ingels et al. 2006, Vermeeren et al. 2004, Fonseca et al.
2007, Lee & Riveros 2012), and part of the presumed cosmo-
politan morphospecies may in fact be complexes of cryptic
species (Derycke et al. 2007a, 2008a, 2010b; see Section 3.7 ).
Moreover, whereas empirical evidence for parallel nematode
assemblages exists for the upper beach zone, sandy beach
nematode assemblages from the swash and subtidal zones
of the Baltic and Mediterranean seas showed very little in
common (Gheskiere et al. 2005). To gain further insight into
how much local environmental conditions and habitat types
explain nematode assemblage composition and the presence
of particular species, a combination of manipulative
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3.6 Disturbance and pollution 121
field experiments, population level studies and meta-
analyses would be required. If nematode assemblages are
indeed closely linked to habitat type and environmen-
tal conditions (Heip et al. 1985, Vanreusel et al. 2010b),
and if physical disturbances and resource availability are
among the main relevant characteristics of habitats (see
Fig. 3.1 in Section 3.3 ), nematode species composition
could become as predictable as general diversity patterns
(see Section 3.3 ).
3.6 Disturbance and pollution 3.6.1 Disturbance
Disturbance plays an important role in structuring faunal
communities (Dayton 1971, Connell 1978, Petraitis et al.
1989). Disturbance stems from processes acting at a variety
of temporal and spatial scales, from the localized feeding
activities of a polychaete to the widespread impacts of a
turbidite, and may be linked to a diverse range of biotic
(e.g., bioturbation, predation) and abiotic factors (e.g.,
waves, tectonic activity). Human activities such as fishing
and mining are also becoming an increasingly pervasive
source of disturbance in marine benthic environments,
even in ecosystems previously considered beyond reach,
such as the deep sea (Puig et al. 2012).
Disturbance was defined by White and Pickett (1985)
as “ … any relatively discrete event in time that disrupts
ecosystem, community, or population structure and
changes resources, substrate availability or the physical
environment ” . Most studies on the impact of disturbance
on nematode communities focus on processes that affect
the physical structure of the sediment (e.g., physical dis-
turbance), food availability (e.g., food falls) or a combina-
tion of both (e.g., presence of macrofauna). The response
of nematodes to disturbance is highly variable among
species and communities, but, as a general rule, “ (nema-
tode) assemblages are most affected by the kinds of dis-
turbances that they do not normally experience naturally ”
(Schratzberger & Warwick 1999).
The effect of physical disturbance (i.e., the disruption
of sediment particles) on shallow-water nematode commu-
nities depends on the interaction of factors, such as type
and frequency of disturbance (Schratzberger et al. 2000)
and sediment grain size (Schratzberger & Warwick 1998a).
Nematode communities in relatively coarse sediments
exposed to strong hydrodynamic conditions, for example,
are more likely to be subject to natural disturbance than
communities in muddy sediments, and are therefore expec-
ted to be more resilient (Schratzberger & Warwick 1998a).
Species with thick and/or ornamented cuticles are usually
more common in sandy than in muddy sediments (Heip
et al. 1985, Leduc & Probert 2011), probably because ela-
borate cuticular ornamentation aids locomotion and helps
prevent mechanical damage in coarse, unstable sediments
(Ward 1975). Although some authors have found the highest
levels of diversity at intermediate levels of disturbance in
the field (Gheskiere et al. 2004, Gingold et al. 2010), others
have found that high levels of physical disturbance lead
to lower local species diversity relative to low-level distur-
bance and lead to shifts in nematode species composition
Fig. 3.5 : Hypothetical arrangement of the dominant nematode taxa along the gradients of resource availability and physical disturbance based on the habitats plotted in Fig. 3.1 (Section 3.3) and the associations observed by Heip et al. (1985) and Vanreusel et al. (2010b).
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122 3 Ecology of free-living marine nematodes
(e.g., Schratzberger et al. 2009). Shifts in nematode
community structure following disturbance often reflect
declines in the abundance of susceptible taxa (generally
epigrowth feeders, such as Desmodora and Spirinia ), as
well as increased dominance of opportunistic taxa such
as Sabatieria (e.g., Schratzberger et al. 2009). Species of
this genus appear to be tolerant of a wide range of envi-
ronmental conditions and are frequently found in distur-
bed environments (e.g., Heip et al. 1990, Somerfield et al.
1995). As for most nematode taxa, however, we still know
very little about the life history characteristics of Sabati-eria species, and more experimental evidence is needed
before we can better interpret species/genus distribution
data from the field.
The presence of macrofauna may influence nematode
communities through a variety of processes, such as phy-
sical disturbance, creation of microhabitats, alteration
of biogeochemical gradients, depletion of food sources
and predation (see Section 3.10 ). The effect of macro-
fauna on nematode community attributes varies widely
among studies, and depends on experimental set-up, the
identity and density of the macrofaunal species involved,
and sediment characteristics (see review by Ó lafsson
2003). Results of microcosm experiments suggest that the
effects of biologically induced disturbance may be less
pronounced than the effects of repeated physical distur-
bance (Schratzberger & Warwick 1999). The results of cage
experiments on the Arctic continental slope suggest that
disturbance by megafauna promotes nematode species
coexistence, which may help explain the high diversity
levels typical of this biotope (Gallucci et al. 2008a).
Several human activities such as sand extraction and
beach cleaning may directly affect nematode communities
in marine benthic systems (Gheskiere et al. 2006, Merckx
et al. 2009). Bottom trawling, however, is by far the most
severe and widespread form of anthropogenic disturbance
to the seabed (Watling & Norse 1998). Most studies have
focused on mega- and macrofauna, and relatively little is
known about the impact of bottom trawling on nematode
communities. The evidence available to date suggests that
trawling may have a positive (Pranovi et al. 2000), nega-
tive (Schratzberger & Jennings 2002, Hinz et al. 2008), or
only minor impact on nematode community attributes
(Schratzberger et al. 2002a, Lampadariou et al. 2005).
Nematodes are generally considered to be more resilient to
physical disturbance than the larger macro- or megafauna
because they are less likely to be killed and can recover
more quickly (Schratzberger et al. 2002a, Whomersley
et al. 2009). Nematodes can recolonize adjacent disturbed
patches by actively dispersing vertically and horizontally
through the sediments (Schratzberger et al. 2000, Gallucci
et al. 2008b). Their ability to actively disperse in the water
column is limited, but passive long-distance dispersal
through resuspension in the water column can promote
quick recolonization of more distant locations (Boeckner
et al. 2009; see Section 3.7 ).
Very little is known about the impacts of human acti-
vities on deep-sea nematode communities. Experiments
conducted on the impacts of nodule mining on abyssal
nematode communities in the Clarion-Clipperton Fracture
Zone (Tropical and Equatorial Pacific) showed a negative
impact on nematode abundance and diversity (Vopel and
Thiel 2001); in one case, impacts remained detectable
26 years following the initial disturbance (Miljutin et al.
2011). This lack of recovery may be related to the slow cur-
rents characteristic of abyssal ecosystems, slow reproduc-
tive rates, and/or the lack of opportunistic species able to
quickly recolonize disturbed areas. Clearly, the deep sea
is a far more quiescent environment than coastal systems,
and deep-sea nematode communities appear less resilient
to physical disturbance than their counterparts in shallow
waters (but see Leduc and Pilditch 2013).
Disturbance induced by food falls and carrion can
have pronounced impacts on nematode communities.
Several studies from shallow-water habitats have shown
that nematode communities associated with decaying
fauna are distinct from communities in nearby areas (e.g.,
Gerlach 1977, Ó lafsson et al. 1992, Fonseca et al. 2011). The
environmental conditions found near decomposing car-
casses (i.e., high dissolved organic matter and sulphide
concentrations, low oxygen levels) are generally associ-
ated with lower nematode standing stocks but appear to
favor a subset of taxa that are otherwise rare in adjacent
sediments. Examples of such taxa include the genera
Terschellingia, Metalinhomoeus, Sabatieria , and the
species Pontonema vulgare and Halomonhystera disjuncta
(Lorenzen et al. 1987, Ó lafsson 1992, Fonseca et al. 2011).
The presence of large food falls helps create spatial hete-
rogeneity in environmental conditions, thus promoting
the coexistence of species with different life-history traits.
Nematodes are considered more tolerant to low
oxygen conditions than macrofauna and other meiofaunal
taxa (see review by Levin et al. 2009). Nematode survival
to hypoxia, however, is highly species-specific, and most
species are negatively affected. Some species, such as
Sabatieria pulchra and Terschellingia communis , survive
well following exposure to hypoxia, although their activity
is greatly reduced (e.g., Hendelberg & Jensen 1993, Steya-
ert et al. 2007). The tolerance of nematodes to hypoxia is
perhaps most obvious in oxygen minimum zones, where
macrofauna becomes scarce, and nematodes strongly
dominate benthic standing stocks (e.g., Gutierrez et al.
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3.6 Disturbance and pollution 123
2008). High abundance of nematodes in these regions
is thought to reflect both the high availability of organic
matter and release from predation pressure from the larger
fauna (Neira et al. 2001). Seeps offer another example of a
highly disturbed habitat characterized by high food avai-
lability, high sulphide and low oxygen concentrations,
where a small number of nematode species occur at high
densities (see review by Vanreusel et al. 2010a).
Pulses of food to the benthos in the form of sinking
fresh algal bloom material or phytodetritus create
another type of disturbance that is often followed by
changes in nematode community attributes. In some
cases, the deposition of fresh microalgal material to the
seabed following algal blooms can have positive effects
on nematode abundance and diversity (Vanaverbeke
et al. 2004), but the opposite has also been observed
(Garcia & Johnstone 2006). The response of nematodes
is most likely dependent on whether hypoxic conditions
develop following the deposition of microalgal material;
as noted above, oxygen depletion is usually associated
with nematode assemblages dominated by relatively
few species (e.g., Armenteros et al. 2010, and references
therein). Nematode communities in coarse sediments
are also more likely to be affected by a sudden organic
enrichment (e.g., shifts in species composition and rela-
tive abundance) than nematodes living in muddy sedi-
ments naturally rich in organic matter (Schratzberger &
Warwick 1998b). Eutrophication in nearshore ecosystems
can lead to macroalgal blooms that may influence nema-
tode communities over large spatial scales. Dense mats
of decaying macroalgae have been associated with shifts
in sediment nematode community structure as well as
decreases in species richness (Villano & Warwick 1995,
Wetzel et al. 2002).
3.6.2 Pollution
Nematode communities (and other meiofauna) are ubi-
quitous and comprise a large number of species/taxa with
a wide range of sensitivities to environmental conditions.
Detailed analyses of community structure can therefore
provide a wealth of information on the state of benthic
ecosystems from intertidal to abyssal depths. Given the
increasing pressure put on coastal environments from
human activities, it is perhaps not surprising that a rapidly
growing body of literature ( > 600 peer-reviewed papers
since the 1970s) has been dedicated to the response of
meiofauna to human-induced stressors, such as pollu-
tion (see reviews by Coull & Chandler 1992 and Fleeger &
Carman 2011).
There are two main difficulties associated with
assessing the impacts of pollution on nematode commu-
nities in the field: (1) our limited knowledge of the basic
biology and ecology of most species and (2) the high vari-
ability in community attributes related to environmental
factors operating at various temporal and spatial scales.
Factors such as hydrodynamics, physical and chemical
characteristics of the sediments, quantity and quality of
food resources and the presence of macrofauna can all
influence nematode communities, but it is usually impos-
sible to take them all into account in field surveys. Never-
theless, pollution appears to have relatively consistent
impacts on nematode communities that can be detected in
studies that are designed appropriately (e.g., Underwood
1994, 1996, 1997, Clarke & Warwick 2001). For example,
the response of nematode standing stocks to organic pol-
lution (such as sewage) is highly variable, but field studies
generally report shifts in community structure and lower
diversity compared to pristine sites (Coull & Chandler
1992). Species of the genera Daptonema, Sabatieria, Pon-tonema , and of the family Linhomoeidae, for example,
occur at high densities in organically enriched locations
throughout the world (e.g., Warwick & Robinson 2000,
Armenteros et al. 2009, Nanajkar & Ingole 2010). This faci-
litates the use of nematodes as indicators of organic pollu-
tion (e.g., Somerfield et al. 2003).
Laboratory assays constitute another useful approach
to quantify the response of nematodes to pollutants such
as metals. Tolerance to metal pollutants has been shown
to vary widely among nematode species (e.g., Vranken
et al. 1991, Kammenga et al. 1994). For example, although
some species such as Enoplus communis show low tole-
rance to metals (Howell 1984), other species, such as Dip-lolaimella dievengatensis and Halomonhystera disjuncta ,
are highly tolerant (Vranken & Heip 1986a, Vranken et al.
1991). This laboratory-based evidence is corroborated by
field surveys describing high densities of the latter (or
closely related) species at polluted sites (Heip et al. 1985),
and even in toxic sediments of a deep-sea cold seep (Van
Gaever et al. 2006). Some intraspecific variation in pollu-
tant tolerance may also occur, and may reflect the degree
of exposure to toxic conditions of different populations in
the field (Howell 1984). This variation may be linked with
changes in genetic diversity induced by sublethal concen-
trations of metals (Derycke et al. 2007b). Sublethal effects
can be detected using a variety of life-history parameters,
such as fecundity and development times; the latter are
generally considered more sensitive toxicity indicators in
laboratory bioassays than mortality (Vranken et al. 1991).
Microcosm studies offer a good compromise between
the complexity of the real world and the often highly
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124 3 Ecology of free-living marine nematodes
artificial settings of laboratory experiments. Nematodes
are particularly well-suited to microcosm studies because
only small amounts of sediments are required; micro-
cosms holding less than one l of sediment typically
contain many thousands of individuals and up to several
dozen nematode species. This type of experiment is ideal
for identifying species sensitive or resistant to a particular
pollutant (i.e., indicator species), as well as assessing the
effects of stressors at the community level. Nevertheless,
microcosms cannot mimic a variety of important proces-
ses operating in natural settings (e.g., immigration, pre-
dation), and should therefore be used in combination
with field surveys to verify the applicability of their results
to natural communities (e.g., Austen & Somerfield 1997).
Microcosm studies (also known as community bioas-
says) have been used to good effect to assess the impact
of metals on nematodes. Both synergetic and antagoni-
stic effects of different metals on nematode abundance,
diversity and community structure have been demonst-
rated (e.g., Gyedu-Ababio & Baird 2006, Mahmoudi et al.
2007), and dose effects have also been observed (Austen &
Somerfield 1997). Toxicity appears to differ among metals,
and may be lowered by the presence of organic matter in the
sediments, which may bind metals and reduce their avai-
lability (Austen et al. 1994). Interestingly, offshore nema-
tode communities appear more susceptible to metals than
nearshore communities, presumably because they are less
exposed to this type of pollutant (Austen & McEvoy 1997).
The degree of tolerance of nematode communities to pollu-
tants can also vary among estuaries, depending on the level
of toxicant exposure in the field (Millward & Grant 2000).
In addition to the study of metals, microcosms have great
potential for the study of other pollutants, such as pesti-
cides (Boufahja et al. 2011), or combinations of toxicants,
such as hydrocarbons and metals (Beyrem et al. 2007).
The ability of monitoring studies to describe ecological
change in a cost-effective manner largely depends on the
appropriate choice of community metrics. It is therefore
worthwhile to briefly mention the different nematode com-
munity metrics most commonly used in environmental
monitoring studies. Nematode abundance, for instance, is
generally considered the least informative community attri-
bute. The lack of a consistent response is linked with the
often complex effects of environmental factors on nema-
tode abundance, high spatial heterogeneity (i.e., patchi-
ness), and the ability of some species to survive in relatively
high densities despite highly polluted conditions (Coull &
Chandler 1992). More reliable and informative results are
obtained from analyses of assemblages at the species or
genus level. Species and genus diversity often yield pre-
dictable results when pollution gradients are investigated
in the field or in microcosms (i.e., lowest diversity in most
impacted sediments). Diversity indices, however, are affec-
ted by sample size and natural environmental variability
and may not always change in the expected direction (Gray
2000, Magurran 2004). Taxonomic distinctness quantifies
phylogenetic diversity rather than richness of species and
differs from most other diversity indices in that it is largely
unaffected by sample size and sampling effort (Warwick &
Clarke 1998). The effectiveness of this metric for the
purpose of environmental assessment, however, has been
questioned by some authors (see Bevilacqua et al. 2012
and references therein). Analysis of nematode community
structure is probably among the most sensitive metrics
for detecting environmental change, although it is also
subject to the influence of multiple environmental factors.
However, as several genera have been identified as relia-
ble indicators of anthropogenic impacts, the description of
the nematode community structure to genus level is pro-
bably one of the most effective ways to detect and describe
environmental change. Although determining community
structure (and diversity) is relatively labor intensive, iden-
tification of nematodes is aided by the existence of picto-
rial keys (e.g., Warwick et al. 1998) and online taxonomic
resources (e.g., Nemys; Deprez et al. 2005). A somewhat
different approach for quantifying change in nematode
communities is based on the classification of individuals
into functional groups. The classification scheme esta-
blished by Wieser (1953) and modifications thereof (e.g.,
Moens & Vincx 1997), is the most widely used in marine
settings and consists of the classification of species into
feeding groups based on buccal morphology (see Section
3.8 ). The usefulness of this metric (or others derived the-
refrom) for environmental monitoring purposes, however,
remains to be established (Lambshead 1986, Danovaro
et al. 1995, Mirto et al. 2002). The Maturity Index (MI) is
another potentially useful metric that was originally deve-
loped to assess the conditions of soil and freshwater habi-
tats based on the classification of nematode families on a
colonizer-persister scale (Bongers 1990, Bongers & Ferris
1999). The use of this index was later extended to environ-
mental monitoring of pollution in marine habitats (Bongers
et al. 1991), but its application in this biome remains cont-
roversial (e.g., Moreno et al. 2011). More detailed informa-
tion on the life-history characteristics of common marine
taxa may help make the MI a more meaningful index for
marine environmental assessment in the future.
Nematodes and other meiofaunal organisms are
efficient and sensitive indicators of environmental stress
(Kennedy & Jacoby 1999). Analyses have shown that
meiofauna may require less time for sample collection
and processing than macro- and megafauna, and often
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3.7 Dispersal, colonization, population genetic structure and cryptic diversity of marine nematodes 125
require fewer samples for detecting meaningful ecologi-
cal changes in community attributes (Rogers et al. 2008).
Despite this, the analysis of nematode communities con-
tinues to be seen by many as time-consuming and costly
compared to other, larger taxa. It may, however, be more
constructive to view the use of different organisms as pro-
viding different but complimentary insights into the state
of sediment communities, as no single faunal group can
provide a complete picture of the ecological processes
occurring in marine benthic systems. It has been sugge-
sted, for example, that the structure of nematode and
macrofaunal communities is influenced by different envi-
ronmental factors, and that therefore both groups should
be investigated whenever possible (Somerfield et al. 1995,
Vanaverbeke et al. 2011, Patricio et al. 2012).
3.7 Dispersal, colonization, population genetic structure and cryptic diversity of marine nematodes
3.7.1 Dispersal of free-living marine nematodes
The movement of organisms ( = dispersal) is one of the
few traits that are shared amongst all animal and plant
species. Dispersal allows organisms to escape unsuitable
environmental conditions, to avoid competition and pre-
dation and to find food. Free-living marine nematodes
are assumed to have low dispersal capacities because
they do not have planktonic or pelagic larvae, they gene-
rally deposit their eggs in situ and their body size is typi-
cally smaller than 1 mm. Nevertheless, quite a number of
marine nematode species show a widespread geographic
distribution (Bhadury et al. 2008, Derycke et al. 2008b,
Bik et al. 2010), indicating that long-distance dispersal
can occur. Such long-distance dispersal may be the result
of nematodes being transported in the ballast water of
ships (Radziejewska et al. 2006), but hydrodynamic forces
are probably more important for passive dispersal (Palmer
1988, Boeckner et al. 2009). The presence of nematodes
in the water column is largely determined by their verti-
cal distribution and abundance in the sediment: species
that are abundant in the sediment (Eskin & Palmer 1985)
or live close to the sediment-water interface (such as epi-
growth feeders, which primarily rely on a photosynthesi-
zing food source) (Commito & Tita 2002, Thomas & Lana
2011) have a higher probability of being suspended in
the water column. Once suspended in the water column,
small nematodes can more easily overcome gravity with
undulating body movements than large nematodes
(Ullberg & Olafsson 2003); therefore, they remain in the
water column, thereby increasing their passive disper-
sal. Similar dispersal abilities have been observed in the
deep sea (Gallucci et al. 2008b, Guidi-Guilvard et al. 2009,
Guilini et al. 2011), but here nematodes are far less abun-
dant in the water column than in shallow-water habitats.
Passive dispersal can also be mediated through
rafting on floating substrata (Thiel & Gutow 2005). Nema-
todes have been observed on floating macro-algae, which
can drift over large geographical distances (Thiel & Gutow
2005). One example is the rhabditid nematode Litoditis marina , which lives on macro-algae (Sudhaus 1974), and
which has been observed on drifting algae in the North
Sea (Derycke et al. 2008b). Phylogeographic analyses
have revealed that even transoceanic dispersal in this
species has occurred, albeit at low frequency (Derycke
et al. 2008b). L. marina has a stress-resistant stage, named
the “ dauer stage ” , which is a non-feeding juvenile stage
that can survive unsuitable environmental conditions
for several months. Dauer larvae can therefore be a very
suitable dispersal stage for nematodes, also through their
association with invertebrates (Kuhne 1996). However,
with the exception of the rhabditid nematodes, marine
nematode species generally do not have dauer larvae, and
vector associations are largely unknown.
Next to passive dispersal, nematodes can actively
disperse in the sediment (Jacobs 1988, Schratzberger
et al. 2004). Larger nematodes colonize empty patches in
the sediment more often than small nematodes, sugges-
ting that they can move more easily in the sediment than
small nematodes (Schratzberger et al. 2004, Gallucci et al.
2008b). The triggers for horizontal dispersal are highly
species-specific: a laboratory experiment with four cryptic
(i.e., morphologically similar but genetically differentia-
ted) species of the Litoditis marina species complex (Pm I,
Pm II, Pm III and Pm IV) revealed that time until dispersal
differs among species and is influenced by food availability
(De Meester et al. 2012). When no food was available at the
inoculation plate, all four species dispersed around 4 days
to avoid these suboptimal conditions. When food was
available at the inoculation plate, Pm I, Pm II and Pm IV
dispersed at the same time and same densities, suggesting
density-dependent dispersal, whereas Pm III dispersed
at lower densities (De Meester et al. 2012). Similar to the
horizontal movement of nematodes in the sediment, their
vertical distribution can be highly species-specific (Steya-
ert et al. 2001) and is at least partially influenced by food
availability (Steyaert et al. 1999) (see Section 3.2.2 ).
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126 3 Ecology of free-living marine nematodes
Nematodes can actively emerge into and swim in the
water column (Jensen 1981). After suspension in the water
column, some nematode species ( Theristus, Chromado-rita and Cobbia ) are able to actively choose and swim
toward sediment spots where suitable food is available
(Ullberg & Olafsson 2003). Large-bodied nematodes of
the family Oncholaimidae rapidly colonize carcasses of
fish and macrofauna, probably at least in part by active
swimming (Lorenzen et al. 1987). Marine nematodes have
a strong chemosensory system, which they can use to
detect a variety of chemical cues, enabling them to direct
their movements toward particular patches (Huettel 1986,
Riemann et al. 1990). However, it remains unclear over
what distances such chemotaxis can occur. The complex
interactions between habitat, hydrodynamics and species-
specific traits lead to high variation in dispersal patterns
through space and time (Commito & Tita 2002, Bostrom
et al. 2009).
3.7.2 Colonization-extinction dynamics of nematode populations in ephemeral habitats
Litoditis marina typically frequents decaying and stan-
ding intertidal macro-algae, which form a rather epheme-
ral habitat with recurrent local extinctions when algae are
decomposed. In such temporary habitats, the ability to
disperse enables nematodes to survive the strong fluctu-
ations in habitat availability. Litoditis marina is an effici-
ent colonizer that can establish populations from only
one or a few gravid females due to its high reproductive
capacity [up to 600 eggs per female under optimal con-
ditions (Vranken & Heip 1983)], short generation time
[ < 3 days under optimal conditions (Vranken & Heip 1983,
Moens & Vincx 2000a)] and its ability to produce dauer
larvae. In an in situ experiment at two contrasting sites
in an intertidal salt marsh, the colonization dynamics
of L. marina were surveyed during 1 month. Defaunated
algae were deposited close to and at a 1 km distance from
permanent algal stands harboring potential source popu-
lations (Derycke et al. 2007c). Nematode abundance and
genetic diversity patterns were recorded at regular time
intervals. Algal deposits near the permanent algal stands
were already colonized after 2 days, reached a fivefold
higher density of nematodes and had a higher genetic
diversity than algal deposits approximately 1 km away
from the source population. Nevertheless, L. marina also
colonized the distant patches within 10 days, showing
that dispersal of this nematode species at this scale is sub-
stantial. However, the populations in the distant patches
were founded from a small number of nematodes, as only
few mtDNA haplotypes were encountered, and these hap-
lotypes were rare in the permanent algal stands. Further-
more, only few new haplotypes were added over time,
suggesting that the first colonizers showed strong popula-
tion development, hampering the establishment of newly
arriving individuals (Derycke et al. 2007c). Such priority
effects are likely to impact the genetic structure of popu-
lations as well as communities. Next to L. marina , other
nematodes (mainly bacterivores) and unicellular eukary-
otes colonized the algae, albeit in much lower densities
(Derycke et al. 2007c).
3.7.3 Population genetic structure of marine nematodes
Dispersal can also be estimated indirectly from genetic
data. The genetic diversity within and among populati-
ons is the result of the simultaneous action of evolutio-
nary processes (gene flow, genetic drift and selection)
across thousands of generations. The population genetic
structure can be investigated through the calculation of
F st
(Wright 1951) or, for highly variable markers, through
related statistics such as D or F ’ st
(Jost 2008, Meirmans &
Hedrick 2011). These statistics basically calculate the
expected genetic diversity within and among populati-
ons and compare it to the total diversity observed. When
selectively neutral markers are used, the genetic structure
is very often correlated with dispersal: high F st
values
typically imply strong genetic differentiation and thus low
dispersal among populations, whereas low F st
values are
indicative of strong exchange among populations (Wright
1951).
The genetic structure of marine organisms is mainly
influenced by life-history characteristics of the species,
geographical barriers, as well as climatic shifts and conti-
nental drifts in the past (Palumbi 1994). However, patterns
of genetic structure do not differ among marine nematode
species with substantially different generation times,
numbers of offspring and habitat preferences, suggesting
that life history is less important for structuring marine
nematode populations (Derycke et al. 2005, 2007a). For
example Halomonhystera disjuncta and Litoditis marina ,
both complexes of closely related cryptic species (Derycke
et al. 2005, 2007a), differ in several aspects of their habitat
preferences and life history: whereas L. marina is nearly
completely restricted to macro-algal substrates, H. dis-juncta also occurs abundantly in the surrounding sedi-
ment and on detritus of vascular plant origin (e.g., in
marshes). H. disjuncta does not produce dauer larvae, and
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3.7 Dispersal, colonization, population genetic structure and cryptic diversity of marine nematodes 127
its generation time under optimal conditions is twice as
long as that of L. marina . If species-specific traits domina-
ted the population genetic structure in both species, we
would expect populations of L. marina to show a higher
genetic differentiation than populations of H. disjuncta
due to the patchier distribution and shorter generation
time. Yet, the genetic structure of the dominant species
from the two species complexes was very similar, and
seasonal differences in genetic structure were observed
for both (Derycke et al. 2006, 2007a), which may reflect
the influence of the transient nature of the macro-algal
habitat. Furthermore, Thoracostoma trachygaster , a
nematode with only one or two generations per year and
few offspring, showed no significant genetic structuring
within the southern Californian Bight at a geographical
scale comparable to that sampled for H. disjuncta and
L. marina (Derycke et al. 2010a). Apparently, differences
in generation time and offspring do not result in different
population genetic structure in marine nematodes.
Litoditis marina, H. disjuncta and T. trachygaster are
associated with macro-algae, which may considerably
increase passive dispersal through rafting, leading to
higher genetic connectivity and therefore weak genetic
structure. By contrast, Bathylaimus assimilis lives in the
sediment and is less prone to suspension in the water
column. Yet, genetic structuring of B. assimilis within the
Westerschelde was also very weak (Derycke et al. 2013). It
thus seems that dispersal at geographical scales of 50 km
or less is substantial in marine nematodes, regardless of
generation time, offspring and habitat preference. By con-
trast, dispersal may decline with increasing geographical
distance ( = isolation by distance; Slatkin 1993): when
combining the Westerschelde data with genetic data from
nematode populations from two nearby coastal locations,
both L. marina and H. disjuncta exhibited strong genetic
structuring (Derycke et al. 2005, 2006, 2007a). As there
are no obvious barriers to gene flow between the Wes-
terschelde and coastal locations, the more pronounced
genetic structuring may be caused by geographical dis-
tance. However, no positive correlation was observed
between genetic and geographical distance for the domi-
nant species from each species complex. In several cases,
significant pairwise genetic differentiation was observed
between close populations, whereas no significant dif-
ferentiation was observed between distant populations.
This “ chaotic genetic patchiness ” pattern is quite common
for the marine environment (Selkoe et al. 2010) and can be
explained by the nonlinear movement of organisms due to
turbulent and nonlinear water currents.
Next to life history and habitat, past land mass drift,
sea-level rises and climatic shifts have influenced the
current distribution and population genetic structuring
of many marine invertebrates (Maggs et al. 2008), inclu-
ding marine nematodes (Derycke et al. 2008b). All species
of the L. marina species complex showed strong genetic
structuring on a pan-European scale (Derycke et al.
2008b). For the two most widespread species (Pm I, Pm II),
this structuring could be linked to past changes in geo-
graphic distributions related to sea-level changes during
the last Ice Age. A genetic break along the British Isles
was observed, and two possible postglacial recoloniza-
tion routes of northern areas were suggested, one around
the British Isles, and one through the English Channel
(Derycke et al. 2008b). In the Southern Bight of the North
Sea, both colonization routes met in a secondary contact
zone. Clearly, past large-scale processes have strongly
affected the genetic variation of marine nematode popu-
lations. As their evolutionary imprint is still detectable in
the present-day genetic composition of marine nemato-
des, gene flow in marine nematodes must be restricted at
such large geographical scales.
Biogeographical barriers often coincide with genetic
breaks between populations on either side of the barrier
(Avise 1994, Teske et al. 2006), and have also affec-
ted genetic structuring in marine nematodes (Derycke
et al. 2010a). For example, Thoracostoma trachygaster
was sampled along the Californian coast (Derycke et al.
2010a), where Point Conception (PC; Wares et al. 2001)
and the Los Angeles Region (LAR; Pelc et al. 2009) are
well-known biogeographical barriers. Thoracostoma tra-chygaster showed a strong genetic structuring along the
Californian coast, with a significant amount of this varia-
tion explained by differences between populations north
and south of PC and, within the Southern Californian
Bight, between populations north and south of the LAR
(Derycke et al. 2010a). This illustrates that well-known
barriers limiting dispersal for marine invertebrates in
general are also limiting connectivity among nematode
populations.
In conclusion, the genetic data available at present
suggest that dispersal in marine nematodes is substan-
tial at scales of 10 – 100 km, irrespective of life history and
habitat preference. Investigating the genetic structure
with more variable markers, such as microsatellites, may
reveal more subtle patterns of genetic structure at these
geographical scales. At larger geographical scales, disper-
sal is strongly limited. This is reflected by the presence of
strong genetic structuring between coastal and estuarine
locations (Derycke et al. 2005, 2007a), by genetic signals
related to past large-scale processes (Derycke et al. 2008b)
and by the occurrence of genetic breaks around biogeo-
graphical barriers (Derycke et al. 2010a).
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128 3 Ecology of free-living marine nematodes
3.7.4 Cryptic diversity prevalent in marine nematodes
The term “ cryptic species ” refers to taxa that are morpho-
logically similar, but belong to different gene pools. Such
cryptic diversity occurs in a variety of metazoan taxa and
biogeographical regions (Pfenninger & Schwenk 2007)
and is particularly abundant in the marine environment
(Knowlton 2000). As cryptic species can generally not be
distinguished based on morphological characters, other
methods need to be implemented. Molecular data may
be one option (Westheide & Hass-Cordes 2001, Nygren &
Pleijel 2011), but applying an integrative approach using
molecular and morphological data (Egge & Simons 2006,
Birky et al. 2010, Nygren & Pleijel 2011) or even biologi-
cal and/or ecological data (Sudhaus & Kiontke 2007)
improves species recognition and description. Population
genetic and phylogeographic studies have highlighted the
presence of substantial cryptic diversity in several marine
nematodes (Derycke et al. 2005, 2007a, 2010a). In-depth
morphometric analyses have revealed morphological
differences among cryptic species (Derycke et al. 2008a,
Fonseca et al. 2008), and in one case, cryptic species have
actually been described (De Oliveira et al. 2012). The inte-
grative approach has rendered possible the detection of
six, five and three cryptic species in L. marina (Derycke
et al. 2008a), H. disjuncta (Fonseca et al. 2008) and T. tra-chygaster (Derycke et al. 2010a, De Oliveira et al. 2012),
respectively. Two to three cryptic species were found in
L. marina and H. disjuncta per season within the Wester-
schelde estuary. These numbers are quite high conside-
ring a geographical scale of less than 50 km. Preliminary
results for the endobenthic monhysterid Theristus acer
in the Westerschelde show three deeply divergent clades
based on the mitochondrial cytochrome oxidase c subunit
1 (COI) gene, which may be indicative of three cryptic
species (Derycke, unpublished data). The prevalence of
cryptic diversity in species complexes exhibiting different
life histories and stemming from different areas suggests
that it is a common phenomenon for marine nematodes.
However, no indications of cryptic species could be detec-
ted in the endobenthic nematodes Bathylaimus assimi-lis and Adoncholaimus fuscus within the Westerschelde
(Derycke, unpublished data), indicating that such general
predictions have to be made with caution.
Despite the considerable increase of newly discovered
cryptic species over the last decade (Bickford et al. 2007,
de Leon & Nadler 2010), only little autecological infor-
mation is available for cryptic species. The field distribu-
tion of the cryptic nematode species shows that several
of them co-occur spatially (Derycke et al. 2005, 2007a,
2008b, 2010a), but that temporal fluctuations in species
abundances are pronounced (Derycke et al. 2006, 2007a).
This, together with the fact that the distribution of several
cryptic L. marina species is restricted at a larger geogra-
phical scale (Derycke et al. 2008b), may point to distinct
tolerance limits and preferences for abiotic factors. By
contrast, essential life-history parameters can be very
similar between cryptic species. Breeding experiments
with four Litoditis species (Pm I, Pm II, Pm III en Pm IV)
provided evidence that the four species are reproductively
isolated, but fertility, minimal development time and
generation time were not significantly different among the
four species (Derycke, unpublished data).
Fluctuations in abiotic factors may at least in part
drive the coexistence of cryptic nematode species at local
scales (De Meester et al. 2011). Laboratory experiments
have shown that two of the four cryptic L. marina species
(Pm I and Pm III) have a faster population development
at a salinity of 15 than at a salinity of 25 (De Meester et al.
2011). Furthermore, when the four L. marina species were
combined in a multi-species treatment, interspecific inter-
actions reduced the population development of Pm II and
even led to the total extinction of Pm IV. These interspeci-
fic interactions were also clearly affected by salinity. Inhi-
bitory interactions have also been observed among closely
related monhysterid species (De Mesel et al. 2006). Alt-
hough such interspecific interactions can be influenced
by food availability inducing resource competition (Dos
Santos et al. 2009), indirect effects such as chemical cues
may also be responsible for the observed inhibitory effects
(De Mesel et al. 2006). As mentioned earlier, the four
cryptic L. marina species also show differences in their
active dispersal (De Meester et al. 2012). These differences
in dispersal can lead to different responses under subop-
timal conditions and may help explain their coexistence.
Discerning cryptic species and investigating their ecologi-
cal characteristics provides the necessary information to
correctly interpret biogeographical distributions, species
interactions, the link between biodiversity and ecosystem
functioning and to identify indicator species for pollution
and other environmental stress factors.
3.8 Feeding ecology Despite their ubiquity, high abundance and presumed
involvement in a variety of important ecosystem functions
(Heip et al. 1985, Coull 1999, De Mesel et al. 2003, Hubas
et al. 2010), one of the basic prerequisites to better under-
pin the roles of nematodes in ecosystem functioning,
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3.8 Feeding ecology 129
i.e., a thorough understanding of their feeding ecology, is
still not met. Free-living aquatic nematodes may feed on a
diverse array of resources, such as bacteria and Archaea,
protists, fungi, particulate and dissolved organic matter,
and as predators prey on metazoans, including other
nematodes. However, at the species, genus and even
family level, available qualitative information is often
anecdotal and restricted to a limited set of “ experimental
conditions ” , thus precluding generalizations to other con-
ditions, let alone to other taxa. Quantitative information is
even far scantier and prone to methodological bias, which
may lead to considerable over- or underestimations of true
feeding rates and metabolic activities under natural con-
ditions (Montagna 1984, Moens et al. 1999b, Braeckman
et al. 2013). One of the consequences of this lack of empi-
rical information is that the role of resource selectivity as a
driver of nematode community composition and diversity
remains unclear. Several studies have provided examples
highlighting the capacity of nematodes to select between
even closely resembling food sources (Trotter & Webster
1984, Moens et al. 1999a, 2000), but whether and to what
extent this capacity translates into real selective feeding
behavior is not understood. By contrast, one might expect
that a more generalist or at least flexible feeding beha-
vior is beneficial in unstable and fluctuating environ-
ments, and that most free-living nematodes are therefore
not highly specialized feeders (Moens et al. 2006). This
contributes to the question as to whether closely related
nematodes, or nematodes with highly similar stoma
morphologies, share very similar resources and feeding
strategies, and may thus be mutually redundant from a
functional perspective, or whether, alternatively, species
have unique behaviors and roles (Moens et al. 1999a, De
Mesel et al. 2004).
For lack of adequate empirical information on actual
feeding behaviors and resources of the vast majority of
species, marine nematodes have traditionally been assi-
gned to feeding types or guilds based on the morphology
of their stoma and, to a lesser extent, pharyngeal muscu-
lature. This firm link between morphology and feeding
behavior was first materialized by Wieser (1953), who pro-
posed a classification with four feeding types as detailed
below. Several modifications and alternative classifica-
tions have later been proposed, but the one by Wieser
remains the most frequently applied. It has the advantage
of being easy to use, in that an identification of the nema-
tode is not strictly required, as the morphology of the
stoma holds all relevant information to assign a nematode
to a feeding category. Moreover, newly published data
are more easily compared with older studies when the
same groupings are used. However, like all subsequently
proposed classifications, it has the implicit disadvantage
that the high marine nematode species diversity is stre-
amlined into a very limited trophic diversity. Moreover,
the link between morphology and feeding, although infor-
mative, is neither as absolute nor as straightforward as
suggested by Wieser ’ s classification (Moens et al. 2004).
Below, we briefly present Wieser ’ s (1953) scheme and the
most important modifications that have subsequently
been proposed.
3.8.1 The four feeding types according to Wieser (1953)
Wieser (1953) distinguished four feeding types, with a
primary subdivision between nematodes with and without
“ buccal armature ” , each of these two groups then being
further subdivided into two. Buccal armature refers to the
presence of a tooth or teeth, onchia, denticles, mandibles
or other sclerotised structures.
1A and 1B nematodes have no buccal armature. They
are both called deposit feeders, but distinguished from
each other based on the size of the buccal cavity. 1A are
referred to as selective deposit feeders, characterized
by small to minute mouth openings, which only allow
ingestion of very small, bacteria-sized food particles.
Non- selective deposit feeders (1B) have more spacious
buccal cavities, enabling them to exploit a wider array of
differently sized particles, occasionally including other
metazoans (Moens & Vincx 1997). As mentioned above,
the issue of selective feeding in nematodes remains
largely unresolved. The distinction between selective and
non-selective as proposed by Wieser (1953) was based on
the general assumption that in a sediment matrix, where
there are far more inedible than suitable food particles,
nematodes with very small buccal cavities can only survive
when they optimize consumption of edible particles while
avoiding uptake of non-nutritious particles. In contrast,
nematodes with a more spacious mouth may mostly invest
in finding feeding spots where suitable food is plentiful,
and may then benefit from a less selective feeding strategy
once inside such a patch (Moens et al. 2006). Although
this mouth-size-based distinction between selective and
non-selective deposit feeders looks arbitrary, the relative
abundances of these two groups indeed often behave
differently. Non-selective deposit feeders, for instance,
typically comprise a considerable share of the nematode
assemblages in silty sediments with high organic loading,
whereas selective deposit-feeders tend to be more promi-
nent in sediments that are comparatively poor in organic
matter (Vincx 1989, Smol et al. 1991). However, there are
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130 3 Ecology of free-living marine nematodes
many exceptions to this “ rule ” . Romeyn & Bouwman
(1983) linked cephalic setation to feeding selectivity of
marine nematodes, but no empirical support has been
added since to back up their hypothesis.
Epistratum feeders (2A) are characterized by the pre-
sence of a tooth, denticles or other sclerotized structures
in the stoma. These mouthparts can be used to either
scrape off bacteria or microalgae from a substratum, such
as a sand grain, or to damage the target food cell to suck it
empty. The latter can be done by piercing (the nematode
sucks the food particle to its mouth and then partly everts
its tooth to puncture it), or by cracking (the food particle is
partly taken into the mouth, opened with a tooth, emptied
and subsequently discarded) (Jensen 1982, Moens &
Vincx 1997). Based on observations on nematodes from
coastal habitats, many epistratum feeders are assumed
to predominantly graze on diatoms and other microalgae.
However, they can be equally prominent in deep-sea sedi-
ments where inputs of fresh microalgal cells are absent or
very limited (Vanreusel et al. 2010b). It is plausible that
they obtain part of their energy from other strategies than
herbivory, perhaps including grazing on bacteria and/or
fungi (Iken et al. 2001).
Predators (feeding type 2B) are often fairly large
nematodes with spacious mouth openings, equipped
with sclerotized structures like teeth, onchia and mandi-
bles. Feeding mechanisms include piercing and emptying
of a prey, tearing a prey open or ingesting the entire prey
(Moens & Vincx 1997, Fonseca & Gallucci 2008). Depending
on the size ratio between prey and predator, some species
(for instance, Oncholaimidae) may shift from one strategy
to another. Some predators use a largely hollow dorsal
tooth, on the top of which opens a glandular outlet, and
observations suggest such nematodes pierce their prey to
inject paralyzing or lethal secretions (Moens & Vincx 1997).
Wieser (1960) changed the name of the predator guild to
“ predators/omnivores ” because of indications that these
nematodes may have additional feeding strategies such as
herbivory, bacterivory or even forms of deposit-feeding.
Incidentally, stylet-like mouth structures, which are
prominent in a variety of soil nematodes, where they
serve feeding strategies as different as plant-feeding, fun-
gal-feeding and predation, are lacking in marine benthic
nematode assemblages, with an exception made for a few
marine algae or vascular-plant-associated species that
are essentially halotolerant representatives of terrestrial
nematode families. Indeed, a trophic link between marine
nematodes and fungi has not yet been established, apart
from some anecdotal observations on nematophagous
fungi preying on nematodes (Moens, unpublished data).
In addition, Iken et al. (2001) suggested fungi as a potential
major food source for nematodes from deep-sea sedi-
ments, but direct evidence to support such a claim has not
yet been provided.
3.8.2 Modifications of Wieser ’ s feeding type classification
Jensen (1987a) proposed two fundamental changes to the
scheme by Wieser (1953). For lack of empirical evidence
that the feeding selectivity between selective and non-
selective deposit feeders differs, both groups were pooled
into a single category of deposit feeders. This grouping has
also been adopted by Traunspurger (1997) for fresh water
nematodes. Among the predators/omnivores, Jensen
(1987a) discriminated between real predators and sca-
vengers, the latter relying mostly on dead faunal remains.
Although scavenging behavior certainly ranks among the
foraging strategies of, e.g., several Oncholaimidae (Jensen
1987a, Moens & Vincx 1997), it may be difficult to precisely
discriminate from the aggregation and active feeding of
bacterivores (for instance L. marina and H. disjuncta (Heip
et al. 1985, Moens unpublished data)) on cadavers. They
probably graze on the associated bacteria, but the possi-
bility that they also scavenge on the cadaver or absorb dis-
solved carbon cannot be discarded. Vice versa, scavengers
sensu Jensen (1987a) may equally benefit from dissolved
carbon and bacteria (Chia & Warwick 1969, Riemann et al.
1990, Moens et al. 1999c). More generally, the possibility
that marine nematodes obtain a significant part of their
carbon from dissolved organic matter remains to be tested.
Moens & Vincx (1997) proposed a modified feeding-
type classification based on dedicated observations of
the feeding behavior of a variety of estuarine nematodes,
covering all feeding types proposed by Wieser (1953) and
Jensen (1987a). Moens & Vincx (1997) re-instated the basi-
cally mouth-size based division among deposit feeders,
but did not link it to a different level of selectivity, as
knowledge on selectivity in most nematode feeding types
is direly lacking. Wieser ’ s (1953) selective deposit feeders
were now labeled microvores, and the non-selective
deposit feeders simply became deposit feeders. A small
subgroup (genera like Tripyloides and Bathylaimus ) was
separated from the latter group based on repeated obser-
vations of Tripyloides ingesting large amounts of cili-
ates. Also, recognizable diatom frustules were lacking
in these nematodes ’ guts, in contrast to many other
deposit feeders like Xyalidae, which often have their
guts filled with diatoms. Epistratum feeders were retai-
ned as a feeding group, but were added to several genera
previously categorized as predators/omnivores, such as
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3.8 Feeding ecology 131
B C
D
A
J
E
H IG
F
Fig. 3.6 : Compound picture zooming in on mouth structures of representatives of all major marine nematode feeding types. Position in the feeding-type classifications of Wieser (1953), Moens & Vincx (1997) and Moens et al. (2004) is given in Tab. 3.1.
Metachromadora, Hypodontolaimus and Ptycholaimellus .
The presence of a prominent tooth and pharyngeal mus-
culature does not inherently imply a predatory feeding
mode, but may equally serve microalgal piercing or cra-
cking. In the cases of Metachromadora and Ptycholaimel-lus , their position as microalgal grazers has meanwhile
been confirmed by both stable isotope data and laboratory
culture trials (Moens et al. 2005a, Moens unpublished
data). This is but one example that highlights that a
strict adherence to stoma morphology does not always
offer a reliable basis to accurately assign nematodes to
feeding types. Much like Jensen (1987a), Moens & Vincx
(1997) divided Wieser ’ s 2B group of predators/omnivo-
res in two: “ strict ” predators and facultative predators.
The latter largely conformed to Jensen ’ s scavengers,
but focused on the consistent ability of these nemato-
des to actively capture live prey, a behavior that may be
supplemented with various other feeding behaviors,
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132 3 Ecology of free-living marine nematodes
including scavenging. Initially, the facultative preda-
tors mainly encompassed Oncholaimidae and Enoplus
(Hellwig-Armonies et al. 1991), but recent evidence sug-
gests that some nematodes previously considered strictly
predatory exhibit more generalist feeding behavior, as
appears to be the case for Enoploides (Franco et al. 2008a,
Moens et al. in press).
Some marine nematodes lack a mouth (for instance
the genus Astomonema ), or a connection between mouth
and gut (males of Calyptronema). Astomonema and
related genera possess endosymbiotic bacteria; uptake of
low-molecular weight dissolved compounds through the
nematode cuticle may provide their symbionts with the
necessary nutrients for their growth, and the endosymbi-
onts in turn fuel the nematode through the secretion of ext-
racellular metabolites (Ott et al. 2004). Whether this also
holds for other mouthless nematodes is not clear. In classi-
cal feeding-type classifications, mouthless nematodes have
been classified under selective deposit feeders or micro-
vores, but given that they do not ingest any particulate
food, it may be better to assign them to a separate category.
Each of the above feeding type classifications has
the implicit disadvantage of assigning nematode species
to fixed categories. However, some nematode species
may be life-history omnivores, shifting diet with deve-
lopmental stage. This has been illustrated for Enoplus brevis (Hellwig-Armonies et al. 1991), but not for another
large predatory nematode, Pontonema sp. (Fonseca &
Gallucci 2008). Moreover, nematodes may be deposit
feeders but also predators at the same time (see example
of Daptonema in Moens & Vincx 1997). The latter is but
one of several issues that arise from the fact that most
feeding-type classifications classify on the basis of a mix
of feeding mechanisms and presumed food sources. What
unifies deposit-feeding nematodes, for instance, is not so
much a shared food source, but rather the way in which
food particles are taken up. Similarly, epistratum feeders
may obtain a variety of food sources, but their feeding
mechanism is relatively uniform. As a consequence, there
is strong overlap in the main resources of, for instance,
deposit feeders and epistratum feeders: in intertidal sedi-
ments many of them may feed predominantly on microal-
gae (Moens & Vincx 1997, Moens et al. 2005a). The feeding
type classification by Yeates et al. (1993) for soil nematodes
partly solves this confusion by identifying trophic guilds
based on presumed principal food sources, yielding guilds
such as bacterivores, unicellular eukaryote feeders and
carnivores. However, the feeding types “ substrate inges-
ters ” and “ omnivores ” have also been established based
on feeding mode rather than food source. Yet, Yeates et al.
(1993) implicitly allow the possibility of assigning a nema-
tode to more than one guild. As such, a nematode can at
the same time be a bacterivore and a unicellular eukaryote
feeder, or a substrate ingester that, through its mode of
feeding, aims mostly at bacteria associated with sediment
grains, and is therefore also a bacterivore. Based on their
own observations of nematode feeding behaviors, Moens &
Vincx (1997) also emphasized the flexibility in feeding
modes and food sources of marine nematodes. Moens
et al. (2004) demonstrated that an only slightly modified
feeding guild classification of Yeates et al. (1993) can be
readily applied to marine nematode assemblages.
3.8.3 Some examples of methods (and pitfalls) in determining nematode food sources
Observations, even though usually anecdotal, on
the foraging of living nematodes under laboratory
conditions, or of gut contents in preserved specimens,
remain very useful in pinpointing potential feeding
Tab. 3.1: Genus of names and allocations to feeding types of the nematodes depicted in Fig. 3.6.
Genus Wieser (1953) Moens & Vincx (1997) Moens et al. (2004)
a – Enoplolaimus 2B predator carnivore, unicellular eukaryote feeder b – Sphaerolaimus 2B predator carnivore c – Synonchiella 2B predator carnivore d – Spilophorella 2A epistrate feeder unicellular eukaryote feeder e – Gomphionema 2A epistrate feeder unicellular eukaryote feeder f – Adoncholaimus 2B facultative predator carnivore, substrate ingester, perhaps partly bacterivore g – Daptonema 1B deposit feeder substrate ingester, unicellular eukaryote feeder, bacterivore (?),
occasionally carnivore h – Bathylaimus 1B ciliate feeder unicellular eukaryote feeder, carnivore (?), substrate ingester (?) i – Antomicron 1A microvore bacterivore j – Haliplectus 1A microvore bacterivore
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3.8 Feeding ecology 133
interactions. However, caution is due when interpreting,
or generalizing from, such observations. The following
two examples should illustrate this. Members of the genus
Enoploides have been shown to be voracious predators of
other nematodes, other small benthic invertebrates, and
ciliates (Moens & Vincx 1997, Moens et al. 1999c, Hamels
et al. 2001), but specimens are often found with their guts
filled with diatoms. This may illustrate that they are also
capable of grazing on microphytobenthos [which has
indeed been confirmed by Franco et al. (2008a) and Moens
et al. (in press)], but the diatom cells could equally derive
from the gut contents of the preys of Enoploides (Moens
et al. 1999c). Second, the trophic guild of ciliate feeders
has been established largely based upon observations of
Tripyloides gracilis feeding intensively on a ciliate bloom
on the surface of laboratory agar slants. But it is not at
all clear whether Tripyloides consistently feeds on cilia-
tes in the field or rather has a flexible feeding behavior
aiming at different types of food, depending on their
availability.
According to the “ you are what you eat ” principle,
appropriately corrected for isotopic fractionation, the
ratios of the stable isotopes of carbon and nitrogen may
help to elucidate resources as well as trophic levels
of nematodes in their natural habitat, in so far as the
principal resources have sufficiently distinct isotopic
ratios (Carman & Fry 2002, Moens et al. 2005a, Rzeznik-
Orignac et al. 2008) (see Box 3.1), and the pathways
of carbon flow can be traced (Middelburg et al. 2000,
Moens et al. 2002). For instance, bacteria often have
nearly identical carbon and nitrogen isotope ratios as
their organic resources, so natural isotope ratios may
not allow discrimination between direct grazing on
microphytobenthos and grazing on bacteria that utilize
microphytobenthic exopolymeric secretions (EPS) or
dead cells. They normally do allow discrimination
between direct utilization of microphytobenthos (MPB)
and predation on eukaryotes that have been grazing on
MPB. In the latter case, carbon isotopic ratios of MPB,
herbivores and the predators of herbivores tend to be
nearly identical, but nitrogen isotopes fractionate suf-
ficiently to assign different trophic levels; unfortuna-
tely, the fractionation factor is not constant (Vander
Zanden & Rasmussen 2001, McCutchan et al. 2003) (see
Box 3.1). A major drawback with most current isotope
ratio mass spectrometers is their biomass require-
ments: typically on the order of 5 μ g of the element of
interest, although slightly smaller amounts may suffice
if measurement conditions are optimized (Carman
& Fry 2002). For carbon, a single adult Thoracostoma
or Adoncholaimus may already fit that requirement,
but for most assemblages from coastal environments,
10 – 100 specimens will have to be pooled to attain this
amount of carbon, and for, e.g., small-sized deep-sea
nematodes, these numbers may even be considerably
higher. Nitrogen is much less abundant in nematodes
than carbon, and one would therefore typically need
at least five times more nematode biomass for a single
measurement. A logical consequence is that most pio-
neering studies on nematode stable isotopes have ana-
lyzed whole assemblages rather than particular taxa
or functional groups (e.g., Couch 1989, Riera & Hubas
Box 3.1 Based on Fry (2008). Stable isotopes are naturally occurring, non- radioactive isotopes of an element. One is usually much more abundant than the other(s). Examples are C, with the 12 C and 13 C isotopes, and N, with the 14 N and 15 N isotopes. The former isotope in each of these two pairs comprises well over 95% of the naturally occurring elements, the latter being relatively “ rare ” .
The ratios of the stable isotopes of an element can differ among different types of organic matter as a result of fractionation. Isotopic fractionation is mostly caused by two phenomena: 1) In kinetic reactions, lighter isotopes and molecules tend to react
faster than heavier ones. As an example, assuming all oxygen is present as 16 O, CO 2 has a molecular weight of 44 or 45, depen-ding on whether the C-isotope is 12 C or 13 C, respectively. Diffu-sion rates for the lighter 12 CO 2 are slightly faster than those of the heavier 13 CO 2 . Depending on the environment and on the “ physiology ” of the organism utilizing this CO 2 , different photo-synthetically active organisms may have more or less difficulty obtaining the heavier 13 CO 2 , resulting in lower 13 C/ 12 C ratios. As a result, different resources at the basis of the food web may end up having measurable differences in their carbon isotopic ratios. Vice versa, when heterotrophs metabolize organic carbon compounds, they release CO 2 through respiration. Here too, lighter 12 CO 2 will diffuse slightly faster. As a result, the consumer will retain comparatively (a very little bit) more of the heavier than of the lighter isotope than was present in its food.
2) In exchange reactions, heavy isotopes tend to concentrate around the strongest chemical bonds, which further emphasizes the effect of 1.
According to the “ you are what you eat ” principle,consumers have very similar isotopic ratios as their resources. In the case of carbon, the similarity is such that one cannot reliably differentiate consumer and resource based on the carbon isotopic signature. In the case of nitrogen, however, the difference is substantial and consistent enough to provide an indication of trophic level . Hence, a predacious nematode feeding on herbivorous nematodes, which in turn feed on microphytobenthos, all have nearly identical carbon isotope ratios; thus, the carbon isotopes elucidate the basal resour-ces but not the trophic level. Nitrogen isotopic ratios will differenti-ate these three trophic levels. Unfortunately, the magnitude of the fractionation between consumer and resource is not constant, which may complicate interpretation of food web relations.
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134 3 Ecology of free-living marine nematodes
2003). Given that most nematode assemblages comprise
representatives of different feeding types as well as
trophic levels, the usefulness of such assemblage-level
analyses is doubtful. Properly replicated, genus-level
analysis of both carbon and nitrogen stable isotopes is
feasible (but time-consuming) for the more abundant
and/or larger genera in assemblages with considerable
dominance. However, it is much less so in highly diverse
and even assemblages and/or in assemblages domina-
ted by (very) small taxa. NanoSIMS (SIMS = secondary
ion mass spectrometry) offers the technological facilities
to measure isotopic ratios at the level of (even very tiny)
individual organisms, but is currently too expensive and
too seldom available to most meiobenthic ecologists.
Stable isotope enrichment experiments, in combi-
nation with assumptions on absorption and production
efficiencies (see Section 9) may allow quantification
of food ingestion (e.g., Moens et al. 2002, Franco et al.
2008a). In contrast to radioactive tracers, which were
commonly used for this purpose in the 1980s and early
1990s, they do not require special precautionary measures
for handling, nor costly waste disposal. Here too, the main
bottleneck for application to nematodes is in the biomass
requirements.
3.9 Marine nematodes and energy flow
Assessing the importance of marine nematodes in
benthic carbon flows or other benthic ecosystem func-
tions requires the assessment of carbon production
and turnover in nematode assemblages. Merely judging
from extant biomass, it seems unlikely that nematodes
would have a significant direct contribution to carbon
flows (Heip et al. 1985, Somerfield et al. 2005). However,
meiofaunal carbon turnover is generally assumed to
be much higher than that of macrobenthos, which may
compensate for their lower extant biomass (Warwick
1984). Measuring all parameters necessary to construct
energy budgets, in particular under (near-) natural con-
ditions, is usually not possible. Therefore, estimates of
nematode production tend to be indirect and are based
on either feeding or respiration experiments. Given that
the amount of carbon consumed by an organism, under
a classical static energy budget, equals the sum of its
absorption and losses, and that absorption in turn equals
the sum of production and respiration, both consump-
tion and respiration may be used to derive production
(see Box 3.2). For example, a feeding experiment using
Box 3.2
A static energy budget for a heterotrophic, multicellular organism can be written in the form of
C(onsumption) = A(bsorption) + L(osses)A = P(roduction) + R(espiration)
Losses are mostly in the form of feces but also different secretory and excretory products.Production comprises both somatic growth and reproduction.Absorption efficiency (AE) = (Absorption/Consumption) * 100Production efficiency (PE) = (Production/(Production + Respiration)) * 100Estimates of AE in nematodes are scanty and span a range of 9%–60%. The higher value, however, is from a single study that, judging by the description of methods, likely confused consump-tion and absorption because of too long an incubation in relation to the nematode’s short gut passage time. Omitting this single study leaves a range of values from 9%–25%.
Estimates of PE vary from 57%–96%. The latter seems implau-sible, but the available data do suggest a generally high PE of 60% or more.
Static energy budgets have many limitations and shortcomings (Kooijman 2000, Van der Meer et al. 2005), but offer the advantage that most parameters can be readily measured. Dynamic energy budget models (Kooijman 2000) offer a more conceptual approach and recognize, for instance, that not all energy budget terms draw upon the entire carbon pool of an animal’s body, or have the same body-mass dependence. Their main disadvantage is that their state variables and various fluxes cannot be measured directly. There have nevertheless been some applications of DEB models to free-living nematodes (albeit not marine) (e.g., Jager et al. 2005).
stable-isotope tracers will reveal information on con-
sumption or absorption rates, depending on incubation
time. The distinction between the two is crucial but far
from evident, because even at short incubations of less
than 1 h, the amount of labeled carbon in a nematode
may better reflect what has accumulated in tissues than
in the gut (Moens et al. 1999b). Given proper estimates of
absorption and production efficiencies (see Box 3.2), the
results of a feeding experiment can thus be translated
into estimates of carbon production. Vice versa, when
measuring respiration (oxygen consumption) as a proxy
for oxic metabolic activity, an estimate of production
efficiency alone is sufficient to translate respiration into
production.
Given that there is a fairly constant exponent (~0.75)
for the allometric relationship between body mass and
respiration in nematodes (Heip et al. 1985), one may even
consider omitting the often tedious respiration or feeding
experiments and use available allometric relations to
predict respiration based on extant nematode biomass.
For example Franco et al. (2010) used a respiration-
biomass relationship originally conceived for deep-sea
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3.9 Marine nematodes and energy flow 135
benthos (Mahaut et al. 1995). Alternatively, when respi-
ration data are available, yet other allometric relations
may be used to derive production directly from respiration
(e.g., McNeil & Lawton 1970, Humphreys 1979). However,
these relationships between respiration and production
have been proposed across a variety of invertebrate taxa,
and there is very little data to assess their adequacy for
nematodes.
Extant biomass is often the easiest variable to obtain
that may bear relevance for assessing nematode contri-
bution to carbon flow. Based on a laboratory study of two
nematode species, an annual production/biomass ratio
of 9 was proposed for marine nematodes (and meiofauna)
in general (Gerlach 1971). This value is derived from a life-
cycle turnover of 3 (Waters 1969) and an average number
of 3 generations per year. Although the former has recei-
ved at least some empirical support (but see Herman
et al. 1984, Vranken et al. 1986 for caveats), the latter is
an extreme oversimplification. Under field conditions,
nematodes may have from less than one to more than 20
generations annually (Vranken & Heip 1986b). The lower
end of this range can be derived from time-series field
sampling, but these do not provide useful information
on the majority of species because generations overlap
(there may be continuous reproduction, although this is
again far less evident than it used to be considered) and
vary in number (Vranken & Heip 1986b). The higher end
of this range is an extrapolation to real field conditions
from lab cultures of a monhysterid nematode at different
temperatures (Vranken & Heip 1986b). However,
although lab cultures provide detailed and highly useful
information on nematode life cycles, such extrapolation
to field conditions remains tricky. As an example, for this
same monhysterid nematode under very similar clima-
tic conditions, Moens (1999) found the lowest frequency
of occurrence and lowest abundance in a year-round
field sampling when temperature conditions in the field
matched the optimal temperature derived from the lab
experiments of Vranken & Heip (1986), suggesting other
environmental factors to be more important drivers than
temperature. But for the vast majority of marine nema-
tode species, there are no data from lab cultures and no
clearly distinguishable cohorts in temporal field sam-
plings (Vranken & Heip 1986b, Somerfield et al. 2005).
Nevertheless, a P/B ratio of 9 has often been used as a
“ quick-and-dirty ” method to estimate carbon produc-
tion rates in marine nematode assemblages from extant
community biomass.
The foregoing may unintentionally create the
impression that obtaining estimates of nematode “ meta-
bolic activity ” is fairly easy and straightforward. This
is certainly not the case. Both feeding and respiration
experiments, even when performed under controlled
laboratory conditions, suffer from methodological
shortcomings and inherent uncertainties. Having said
that, ex situ feeding experiments are feasible, and cont-
rols for indirect label uptake are possible, whereas deve-
lopments in polarographic electrode and particularly
optode technology now allow accurate measurements
of respiration on batches of only a small number of spe-
cimens (Moens et al. 1996, Moodley et al. 2008). Most
respiration measurements on marine nematodes have
measured respiration under conditions of oxygen satu-
ration. In many marine sediments, however, oxygen con-
centrations are well below saturation, and hypoxia may
already occur at very shallow sediment depths (mms to
cms). Based on controlled lab respiration experiments at
various oxygen concentrations, Braeckman et al. (2013)
conclude that respiration-based estimates of metabolic
activity under conditions of oxygen saturation tend to
be strongly overestimated and poorly representative of
field conditions.
Another important concern throughout the above- listed
approaches to estimate nematode carbon production rates,
is that much or most of the available information on life his-
tories, energy budgets, respiration rates and production and
absorption efficiencies stems from laboratory studies on
fast-growing, opportunistic, tolerant, bacterivorous species
kept under optimal conditions. When supplied with suf-
ficient food, a monhysterid nematode may take less than
two weeks to develop from adult in one generation to adult
in the next, produce a few hundred eggs per female and
do so at typically high production efficiencies (PE) but low
absorption efficiencies (AE) (Vranken et al. 1988, Herman
& Vranken 1988, Moens & Vincx 2000a, b). The influence
of environmental factors, such as oxygen and temperature
on all these parameters is poorly known, and so are effects
of food quantity and particularly quality. The rhabditid
L. marina unlimitedly increases its ingestion rate with increa-
sing food availability, but above a certain food density, its AE
decreases. This implies that AE fluctuates with food availabi-
lity (Moens et al. 2006). Moreover, although the effect of food
availability on respiration rates in bacterivorous nematodes
is moderate and basically linear, its effect on production is
pronounced and hyperbolic, suggesting a dependence of
PE on food availability as well (Schiemer 1982, 1985, 1987).
There is little doubt that the food quality of carnivores tends
to be higher than that of bacterivores, and carnivorous
nematodes tend to have much slower development and
reproduction rates (Heip et al. 1985). It is therefore proba-
ble that feeding types other than bacterivores have different
AEs and PEs. Hence, AEs and PEs are likely species-specific
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136 3 Ecology of free-living marine nematodes
and context-dependent, and cautious interpretation is due
when applying any of these indirect approaches to estimate
carbon production in marine nematode assemblages.
Given the methodological and conceptual problems
described above, there is not yet any consensus about the
importance of nematodes in benthic carbon flows. Several
authors have argued that nematodes are important in
view of their high numbers and fast turnover (Kuipers
et al. 1981, Coull 1999), or based on tracer experiments
(see Montagna 1995, for review) or more indirect estimates
of grazing rates (Rzeznik-Orignac et al. 2003). By contrast,
several more recent stable-isotope tracer experiments
suggest that nematodes process only tiny fractions of
labile organic matter that either reaches, or grows on, the
sediment surface (Middelburg et al. 2000, Van Oevelen
et al. 2006, Urban-Malinga & Moens 2006, Franco et al.
2008a, Ingels et al. 2010). There is clearly an important
challenge in reconciling these conflicting results and in
improving approaches for obtaining reliable estimates of
nematode metabolic activity under field conditions.
3.10 Trophic and non-trophic interactions with macrofauna
Meiofauna are influenced by often larger benthic
organisms. Every interaction that alters meiofaunal
abundance or behavior potentially affects ecosystem
dynamics and stability as meiofaunal organisms influ-
ence ecosystem processes, such as sediment- and solute
transport, the mineralization of organic matter and
concomitant nutrient regeneration (see Section 3.11 ). Bio-
logically mediated changes in meiobenthic community
structure, diversity and population abundance result
from both direct and indirect interactions, as demonst-
rated by surveys and experiments in a wide variety of
marine benthic soft-bottom habitats along the intertidal-
deep sea gradient, covering temperate, (sub-) tropical
and polar environments. Most studies of the mechanisms
of the interactions between meiofauna and other benthic
organisms have been undertaken in intertidal habi-
tats, including sand- and mudflats, sandy beaches, salt
marshes and mangroves. This likely relates to the easier
logistics for sampling, manipulation and monitoring of
specific processes, and the high taxonomic resolution
of meiobenthic communities that is available for these
habitats. A long history of caging experiments in inter-
tidal habitats that include or exclude particular benthic
groups has shed light on the biotic interactions with
meiobenthic communities (e.g., Bell 1980, Reise 1985,
Schrijvers & Vincx 1997), whereas the use of, e.g., stable
isotopes, computed tomography (CT) scans and experi-
mental community manipulations and disturbances in
situ or in mesocosm experiments has recently further
unraveled the underlying mechanisms (Schratzberger &
Warwick 1998a, b, Bouchet et al. 2009, Van Colen et al.
2009, Maria et al. 2011).
Meiofauna are potential prey to infaunal, epi- and
hyperbenthic predating polychaetes, crabs, mysids,
shrimps, fish and wading birds, as well as suspension
feeders that filter (re-) suspended meiofauna from the
water column but may also consume it as “ bycatch ” of
other preys (see, e.g., Coull 1999 for a review). Conse-
quently, predation is the predominantly reported direct
interaction that affects meiobenthic communities. For
example, Li et al. (1996) demonstrated that in a brackish
tidal flat, predation by deposit-feeding macrobenthos was
more important in controlling the variation in nematode
biomass than variability in food availability.
Indirect interactions include mainly facilitation and
competition. Ecosystem engineering (Jones et al. 1994) is
a key pathway by which meiofauna is affected by other
organisms. For example, macrobenthic organisms alter
the distribution of high-quality organic matter (Graf 1989,
Levin et al. 1997), as well as oxygen and toxic metaboli-
tes in the sediment (Kristensen & Kostka 2005) through
bioturbation and bio-irrigation activities (Meysman et al.
2006), which subsequently may influence meiofaunal
distribution, abundance and diversity. These activi-
ties do not only directly affect the transport of solids
and solutes, but also stimulate biogeochemical proces-
ses along the burrow walls (Mermillod-Blondin et al.
2004), which may alter the microbial community (Kris-
tensen & Kostka 2005) and hence diversify the menu
for meiofauna. Moreover, macrobenthic fecal casts sti-
mulate bacterial activity due to a higher concentration
of organically enriched fine particles (Reise 1985). In
addition, macrobenthos may affect meiobenthic com-
munities by (1) the construction of physical structures
(e.g., polychaete tubes) that provide shelter from pre-
dation (Z ü hlke et al. 1998), (2) the depletion of shared
food resources ( Ó lafsson et al. 1993) and (3) direct phy-
sical disturbance resulting from bioturbation (Austen &
Widdicombe 1998, Schratzberger & Warwick 1999).
Despite predation- and disturbance-related mortality or
avoidance due to exploitative competition, studies often
report enhanced meiofaunal diversity in the presence of
macrofauna. In this respect, the IDH (Connell 1978) has
been frequently used to explain increased meiofauna
abundances and diversity close to macrofaunal feeding
or moving tracks (Warwick et al. 1986, Varon & Thistle
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3.11 Nematodes and ecosystem functioning 137
1988, Reidenauer 1989, Ó lafsson et al. 1990, Austen et al.
1998).
The outcome of biological interactions between
macro- and meiobenthic communities depends on the
environmental and temporal context. For example, bio-
logical control on meiobenthic communities may be more
pronounced in low-energy, muddy sediments with strong
biogeochemical gradients compared to exposed tidal flats
and permeable subtidal sandy sediments, where strong
physical forces control benthic communities (Warwick
et al. 1997, Vanaverbeke et al. 2010). There is no clear diffe-
rence in the extent or magnitude of meiofaunal responses
to macrobenthos between intertidal and subtidal habitats
(reviewed in Ó lafsson 2003). In shallow habitats, macro-
fauna has been found to reduce the abundance of meio-
fauna through predation and disturbance (e.g., Reidenauer
1989, Hedqvist-Johnson & Andre 1991, Aarnio et al. 1998)
or through competition for food (e.g., Ó l afsson et al. 1993,
Braeckman et al. 2011a, b). Warwick et al. (1997) described
reductions in meiofauna diversity related to deteriorating
oxygen conditions in the neighborhood of bivalve biode-
posits. By contrast, where macrobenthos activities affect
even the strong biogeochemical gradients in the sediment,
food availability and hence meiofauna abundance, diver-
sity and downward migration may increase (Warwick et al.
1986, Austen & Widdicombe 1998; et al. 1998, Dashfield
et al. 2008, Braeckman et al. 2011a, b). Finally, some
studies did not detect any biological effect on meiofauna
at all (Aarnio et al. 1991, Nilsson et al. 1993, Ó lafsson et al.
1993, Austen & Thrush 2001).
The amount of studies investigating interactions
between meiofauna and other benthic organisms in deep-
sea habitats is considerably lower than for intertidal and
shallow subtidal habitats. Experimental investigation of
biotic interactions in deep-sea habitats is extremely chal-
lenging due to logistic issues associated with the remote-
ness of this habitat. Nevertheless, empirical evidence of
biologically mediated changes of meiobenthic communi-
ties in deep-sea habitats has been gathered since the mid-
1980s. For example, Gallucci et al. (2008a) demonstrated
that the experimental removal of megafauna resulted in
increased abundances of certain species over a 4-year
period, most likely as a consequence of the lack of bio-
genic disturbance. However, biogenic structures, such as
relict burrows, may well stimulate meiofaunal diversity
(Levin et al. 1991, Soltwedel & Vopel 2001), as they can
act as traps for organic matter, providing an extraordi-
nary localized energy source in a relatively food-depleted
environment (Aller & Aller 1986). Moreover, they provide
efficient refuges from predation (Thistle & Eckman 1990)
and may enhance vertical transport of solutes, resulting
in altered meiofaunal abundances explained by species-
specific attraction or avoidance behavior (Eckman &
Thistle 1991). As the rate of physical and biological distur-
bance decreases with depth, benthic organism-induced
habitat heterogeneity persists over long time periods,
which may stimulate niche diversification. In addition,
low production, sedimentation and population growth
rates may enhance competitive similarity among deep-
sea species and is therefore thought to contribute to
competitive exclusion in benthic deep-sea communities
(Hasemann & Soltwedel 2011).
In summary, the variety of responses of meiobenthic
communities to the presence of other benthic organisms
indicates that (1) biologically mediated changes in meio-
benthic communities are a universal ecological process in
the marine realm and (2) that responses relate to species-
specific life history traits of the meiofaunal organisms and
the species that interact with them (Austen & Widdicombe
1998, Braeckman et al. 2011b). To enhance our under-
standing of biological interactions between marine soft-
bottom meio- and macro- and megabenthic communities,
future research requires a high taxonomic resolution as
well as insights in the functional traits of the meiobenthic
community on the one hand, and those organisms influ-
encing the meiofauna on the other.
3.11 Nematodes and ecosystem functioning
Ecosystem functioning involves several processes such
as primary and secondary production, consumption and
decomposition of organic matter, the regeneration of
nutrients and their transfer through different, eventually
higher trophic levels. These processes are sustained and
shaped by intra- and interspecific interactions as well
as the interplay between organisms and their physical
environment. Essential goods and services (not only for
humans), such as food or clean water, highly depend on
an integer, well-functioning ecosystem.
The number and composition of species play a crucial
role in the functioning of a system (e.g., Hooper et al.
2005). Several theoretical biodiversity-ecosystem func-
tioning (BEF) relationships have been proposed. The null
model predicts no effect of species diversity on ecosystem
functioning, whereas the Rivets Hypothesis supposes a
linear improvement of ecosystem functioning as species
are added to the system (Ehrlich & Ehrlich 1981). By cont-
rast, the redundancy hypothesis describes an asymptoti-
cal relationship where ecosystem function improves until
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138 3 Ecology of free-living marine nematodes
a certain diversity threshold, but after that, species ’ func-
tions are redundant and induce no functional improvement
(Walker 1992). For the deep sea, an exponential relation-
ship between nematode diversity and ecosystem function
has been proposed, suggesting that associated ecosystem
functions exhibit greater increases as species are added
(Danovaro et al. 2008a, Danovaro 2012; but see Leduc
et al. 2013). Free-living marine nematodes can be assig-
ned to different functional or trophic groups, such as, e.g.,
bacteria feeders or predators/scavengers (see Section 3.8 ).
Although theoretically many species apparently share the
same function, empirical evidence suggests only limited
functional overlap (De Mesel et al. 2006, Dos Santos 2009,
Gingold et al. 2013). Finally, the idiosyncrasy hypothesis
posits that diversity alterations affect ecosystem functio-
ning in an unpredictable manner, as single “ high-impact
species ” may have a substantially more important effect on
a given process than others (Lawton 1994).
The functions of nematodes in intertidal habitats
such as sandy beaches, salt marshes, mud flats and estu-
aries, are manifold yet sometimes still poorly understood.
Trophic structure is but one of the many characteristics
that drive the functioning of nematode communities in
marine ecosystems. Structural diversity is often used as a
surrogate of functioning under the premise that an empi-
rical relation between diversity and functioning exists.
While nematodes often represent the dominant taxon in
terms of abundance and diversity (50 or more species and
up to several (ten-) thousand individuals 10 cm –2 (Heip
et al. 1985), experiments often involve only one to several
single species obviating the methodological difficulties
that would arise from treating entire communities as
experimental units. However, through these experiments,
fundamental knowledge about many functional aspects
of nematodes has been gained.
Nematodes in general, and bacterivore nematodes in
particular, may play a crucial role in the decomposition
of organic matter (Findlay & Tenore 1982, Alkemade et al.
1992a, Lilleb ø et al. 1999). Nematode diversity may enhance
microbial activity (De Mesel et al. 2006) and enhance det-
ritus processing, digestion and reworking, resulting in
higher rates of organic matter re- mineralization. Parts of
tidal flats and marshes are characterized by salt-tolerant
vegetation often dominated by cordgrass species of the
genus Spartina . Bacterivorous nematodes such as Mon-
hysteridae, in particular the genera Diplolaimelloides
and Diplolaimella , can generally be found in association
with the decaying leaves of S. anglica , where they feed on
the bacterial assemblage on the leaves. Laboratory expe-
riments revealed that the mineralization rate of dead
S. anglica leaves significantly improves and may increase up
to 300% in the presence of bacterivore nematodes (Findlay
& Tenore 1982, Alkemade et al. 1992a). The effect depends,
among other factors, on the leaf condition (e.g., whether it is
fresh or senescent) and on the nematode population density.
The stimulation of bacterial decomposition on plant leaves
through nematodes takes place through mechanisms, such
as: 1) higher predation on bacteria, which maintains higher
bacterial growth rates (Traunspurger et al. 1997), 2) biotur-
bation, which enhances oxygen and nutrient fluxes, which,
in turn, stimulates microbial growth rates (Alkemade et al.
1992b) and 3) mucus secretion by nematodes that influences
bacterial colonization and population development (Moens
et al. 2005b).
Bacterivore nematodes may have a significant top-
down effect on the bacterial community structure, even at
low grazing pressure (De Mesel et al. 2004). Their grazing
activities significantly shape the bacterial community and
influence the relative importance of the different commu-
nity members, as shown by two microcosm experiments
involving four bacterivore nematode species singly and
in combination (De Mesel et al. 2004, 2006). The effects
are species-specific on the one hand, possibly depen-
ding on the food preferences of the single species (i.e.,
selective vs. unselective; De Mesel et al. 2004) and diver-
sity-dependent on the other hand, with strong support
for the idiosyncrasy hypothesis (De Mesel et al. 2006).
The species- specific effect is most pronounced with the
species representing the most extreme colonizer, stron-
gest grazer and fastest reproducer of the species tested
(i.e., Panagrolaimus paetzoldi ), which indicates that the
effect may, in fact, be more density- than species-specific
(De Mesel et al. 2004). The idiosyncratic diversity effect,
on the other hand, may be due to unexpected inhibitory
interactions between two closely related monhysterid
species (De Mesel et al. 2006). Complex species interac-
tions, such as inhibition or facilitation, may render pre-
dictions on nematode BEF relationships difficult or even
impossible (Dos Santos et al. 2009).
Besides the direct top-down effect on the bacterial
community and hence the decomposition of organic
matter, nematodes contribute to bioturbation, which
indirectly enhances detritus mineralization. Members of
the macrofauna are generally the more important sedi-
ment bioturbators (e.g., Biles et al. 2002). Bioturbation
by macrobenthos may intensify with increasing diver-
sity levels, with consequent increases in benthic fluxes
to the benefit of the benthic ecosystem (Lohrer et al.
2004, Meysman et al. 2006). In the case of nematodes,
the term cryptobioturbation may be applied because of
their large numbers in small amounts of sediment (e.g.,
Giere 2009). Micro-scale biogenic activities have already
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3.11 Nematodes and ecosystem functioning 139
been observed when the marine nematode ecology was
still in its infancy (Cullen 1973). Meiofaunal bioturbation
is now well recognized as an important function with
consequences for, e.g., bacterial population develop-
ment through promotion of oxygen and nutrient cycling,
thereby enhancing mineralization of detritus (Alkemade
et al. 1992b). Mixing activities of nematodes more than
double transport rates of solutes in sediments (Aller
& Aller 1992) and promote reaction rates, particularly
aerobic decomposition and associated processes, such as
nitrification in the oxic zones of marine sediments (e.g.,
Rysgaard et al. 2000). Bioturbation activity of the bacteri-
vore nematode Diplolaimella dievengatensis significantly
enhances oxygen diffusion into the sediment and conse-
quently leads to increased Spartina detritus decomposi-
tion (Alkemade et al. 1992b). The movements enhance the
sediment porosity on the one hand, and the feeding, bur-
rowing and other activities lead to particle fragmentation
and exposure on the other (Aller & Aller 1992).
In addition to their microbioturbating activities,
aquatic nematodes can produce sticky mucus by means
of their caudal glands and can also release large amounts
of mucus from their mouths (Riemann & Schrage 1978).
The mucus serves for attachment to the sediment (mucus
is released upon contact with the substratum; Riemann &
Schrage 1978), to stabilize burrows (Nehring et al. 1990) = ,
or to attach eggs to the ground (Riemann & Schrage 1978).
Microbioturbation and mucus-supported burrows may
enhance but also reduce porosity and permeability of the
sediments, and hence affect the efficiency with which nut-
rient exchanges take place (Netto et al. 2008). Moreover,
the mucus may serve as a trap for bacteria and detritus
(mucus-trap-hypothesis; Riemann & Schrage 1978). Labo-
ratory experiments affirmed that nematode tracks covered
with mucus (in contrast to artificial tracks) induce bacte-
rial growth and allow the establishment and maintenance
of dominant strains over time (Moens et al. 2005b). The
presence of nematodes may also enhance the bacterial and
microphytobenthic production of extracellular polymeric
substances (EPS; colloidal carbohydrates and proteins)
by stimulating bacterial and diatom population growth
(Hubas et al. 2010). The stimulation effect may arise from
increased nitrogen (ammonium) excretion relieving nut-
rient limitation for bacteria and diatoms, among other
reasons (Hubas et al. 2010).
Given their relatively higher mobility, nematodes may
act as “ taxis ” for bacteria, taking them to new spots of
freshly deposited organic matter ( “ founder effect ” ; Moens
et al. 2005b), a vectoring function that has even evolved very
specialized forms leading to symbiosis in some cases. Stilbo-nema sp. , for example, transfers ectosymbiotic bacteria from
and to sulfidic and oxidized sediment layers (Schiemer et al.
1990). Prokaryotic symbioses with nematodes are sometimes
even established within the nematode habitus, as is the case
for several nematodes from the family Siphonolaimidae.
Both in shallow waters and in the deep sea, Parastomonema
and Astomonema species have been found with endosym-
biotic prokaryotes identified as sulphide oxidizers. Owing
to the lack of any mouth opening of the nematodes, this
implies that the prokaryotes are able to provide chemosyn-
thetically harnessed energy to the nematode host (Ott et al.
1982, Austen et al. 1993, Giere et al. 1995, Musat et al. 2007,
Tchesunov et al. 2012). This association enables nematodes
to exploit otherwise toxic (micro-) habitats and increases
the functional complexity of the communities present. The
close association between prokaryotes and nematodes as
observed in shallow-water environments may be even more
pronounced in deep-sea environments. Benthic prokaryotes
(Bacteria and Archaea) become quantitatively more impor-
tant relative to other living components with increasing
water depth (Rex et al. 2006). The discovery of high metabo-
lic activities and specific functional characteristics in deep-
sea prokaryotes has led to the conclusion that prokaryotes
play a pivotal role in deep-sea food webs, carbon and nut-
rient cycling, and overall deep-sea ecosystem functioning
(Boetius et al. 2000, Danovaro et al. 2009b) and contribute to
the observed exponential relation between nematode diver-
sity and deep-sea ecosystem function.
Free-living marine nematodes are highly diverse and
nematode assemblages often include many different
species within each of several functional (trophic) groups.
Nematode interactions add to the complexity of functio-
ning, e.g., through predator-prey relations and subse-
quent regulation of the trophic complexity of nematode
communities. Are they redundant in their function? So far,
experiments indicate that they may be only to a limited
extent: They are capable of specialist feeding (Moens
et al. 1999a; see Section 8 ), and single species contribute
idiosyncratically to ecosystem functioning (e.g., De Mesel
et al. 2006). However, experiments are usually conduc-
ted with a limited number of species. A new approach in
BEF studies involves microcosm experiments with free-
living marine nematode communities at close-to-natural
diversity levels, especially to address the two related fun-
damental questions, whether 1) diversity plays a crucial
role in ecosystem functioning, resistance and resilience
and 2) species of the same trophic/functional group are
redundant or complementary in their function. Pionee-
ring microcosm experiments on that subject revealed
that nematode species richness seems to have a posi-
tive influence on the functioning of a system, measured
as, e.g., microbial activity (Dos Santos 2009). However,
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140 3 Ecology of free-living marine nematodes
stress resistance seems to be influenced idiosyncratically,
depending on the community origin rather than species
richness (Gingold et al. 2013).
For deep-sea environments, nematode research has
only started to explore nematode functioning by means
of experimental setups because of the inaccessibility and
extreme conditions that make experimental manipula-
tion difficult compared to intertidal and shallow-water
environments. However, technological advances have
been instigating innovative research in recent years. So
far, results remain mostly based on natural observations,
correlative approaches, and what has been learned from
shallow-water studies. Compared to shallow waters, the
deep sea is assumed to be relatively stable, like an envi-
ronmental calm, with little fluctuations in terms of hyd-
rodynamic activity and biogeochemical characteristics
(Thistle 2003). Deep-sea environments are (except for
chemosynthetic systems) dependent on euphotic produc-
tion that escapes the upper water column and sinks to
the seafloor, as well as terrestrial and freshwater inputs
that are channeled to the deep sea via topographical fea-
tures, such as submarine canyons. Deep-sea nematode
functioning therefore reflects their activities in exploiting
and recycling the inputs of materials from the photic zone
(Danovaro 2012), as well as their interactions with sedi-
ments and other organisms (e.g., Leduc & Probert 2009,
Leduc et al. 2012). The dependency on phytodetritus is
reflected in the variability of nematode trophic diversity
observed in different deep-sea environments receiving
different amounts and types of input (e.g., Ingels et al.
2011a, b) and in chemosynthetic environments (Vanreusel
et al. 2010a). It hints at the sensitivity and selectivity of
different feeding types in exploiting deep-sea food resour-
ces (Guilini et al. 2010, Ingels et al. 2010, 2011c), although
results are not consistent (Guilini et al. 2011). Nematode
biomass as an ecosystem function shows a positive linear
relation with food availability (particulate organic carbon
flux as a measure of food becoming available to the deep-
sea benthos) at abyssal depths, and the same trend is
observed in terms of nematode diversity in the deep
equatorial Pacific (Smith et al. 2008; see Section 4 ). Most
notable, however, is the observation that nematode diver-
sity is exponentially linked with ecosystem functioning
(measured in terms of prokaryotic activity and biomass,
as well as total faunal biomass) and ecosystem efficiency
(Danovaro et al. 2008a, Danovaro 2012). This suggests that
mutually positive functional interactions may exist that
are enhanced with greater diversity levels in the deep sea.
One possible explanation for the high deep-sea
nematode diversity and the great sensitivity of ecosys-
tem functioning to a decline in diversity may be found
in the stability-time hypothesis (Sanders 1968, 1969). The
stability-time hypothesis implies that in very stable envi-
ronments, such as the deep sea, species become highly
specialized within narrow niches, and therefore many
species are able to co-exist at a competitive equilibrium
(Snelgrove & Smith 2002). The constant deep-sea envi-
ronment has enabled species to adapt to each other rather
than needing to adapt to the rigors of the environment, as
is the case, for instance, in intertidal areas. The seasonal
character of the phytodetrital food fluxes to the deep sea
may intensify the associated processes; it creates a type
of temporally recurring disturbance that gives rise to the
appearance or success of species before actual compe-
titive exclusion occurs. These deep-sea characteristics
may thus explain the exponential nature of the nema-
tode diversity-function relationship there, in contrast to
the other models applicable to shallow-water environ-
ments. In this context, productivity plays an important
role in driving the observed biological deep-sea patterns.
Whether maximum function (nematode biomass) will be
obtained at highest (Danovaro et al. 2008) or rather at
intermediate nematode diversity levels (Leduc et al. 2012,
and Fig. 3.3 in this chapter) remains a matter of debate.
Nematodes play an essential role in nutrient rege-
neration, biogeochemical fluxes and ecological stability
through numerous trophic and other interactions with
multiple benthic organisms in shallow-water as well
as deep-sea environments. They eat, clean, stir, take,
bring, attach, assemble and decompose, unremittingly,
irreplaceably and peerlessly. Barely visible to the naked
eye, science has gained fundamental knowledge of global
relevance through their study. Yet, many aspects remain
to be discovered, and in a world where biodiversity loss
is one of the most pressing issues, the understanding of
species richness for the functioning of ecosystems, and
thus the sustainability of ecological goods and services, is
of primordial importance and may provide an important
subject for future studies involving marine nematodes.
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