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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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).

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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 ).

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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).

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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,

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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,

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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,

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

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.

Literature Aarnio, K., Sandberg, E. & Bonsdorff, E. (1991): Benthic predation on

shallow-water macrofauna and meiofauna in the Baltic Sea - an experimental comparison between Pomatoschistus minutus (Pisces) and Saduria entomon (Crustacea). Ann. Zool. Fennici 28: 41 – 48.

Aarnio, K., Bonsdorff, E. & Norkko, A. (1998): Role of Halicryptus spinulosus (Priapulida) in structuring meiofauna and settling macrofauna. Mar. Ecol. Prog. Ser. 163: 145 – 153.

Alkemade, R., Wielemaker, A. & Hemminga, M. A. (1992a): Stimulation of decomposition of Spartina anglica leaves by

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   141

the bacterivorous marine nematode Diplolaimelloides bruciei (Monhysteridae). J. Exp. Mar. Biol. Ecol. 159: 267 – 278.

Alkemade, R., Wielemaker, A., de Jong, S. A. & Sandee, A. J. J. (1992b): Experimental evidence for the role of bioturbation by the marine nematode Diplolaimella dievengatensis in stimulating the mineralization of Spartina anglica detritus. Mar. Ecol. Prog. Ser. 90: 149 – 155.

Aller, J. Y. & Aller, R. C. (1986): Evidence for localized enhancement of biological activity associated with tube and burrow structures in deep-sea sediments at the Hebble Site, Western North-Atlantic. Deep Sea Res. Part A 33: 755 – 790.

Aller, R. C. & Aller, J. Y. (1992): Meiofauna and solute transport in marine muds. Limnol. Oceanogr. 37: 1018 – 1033.

Appeltans, W., Ahyong, S. T., Anderson, G., Angel, M.V., Artois, T., Bailly, N., Bamber, R., Barber, A., Bartsch, I., Berta, A., Blazewicz-Paszkowycz, M., Bock, P., Boxshall, G., Boyko, C. B., Brand ã o, S. N., Bray, R. A., Bruce, N. L., Cairns, S. D., Chan, T. Y., Cheng, L., Collins, A. G., Cribb, T., Curini-Galletti, M., Dahdouh-Guebas, F., Davie, P. J., Dawson, M. N., De Clerck, O., Decock, W., De Grave, S., de Voogd, N. J., Domning, D. P., Emig, C. C., Ers é us, C., Eschmeyer, W., Fauchald, K., Fautin, D. G., Feist, S. W., Fransen, C. H., Furuya, H., Garcia-Alvarez, O., Gerken, S., Gibson, D., Gittenberger, A., Gofas, S., G ó mez-Daglio, L., Gordon, D. P., Guiry, M. D., Hernandez, F., Hoeksema, B. W., Hopcroft, R. R., Jaume, D., Kirk, P., Koedam, N., Koenemann, S., Kolb, J. B., Kristensen, R. M., Kroh, A., Lambert, G., Lazarus, D. B., Lemaitre, R., Longshaw, M., Lowry, J., Macpherson, E., Madin, L. P., Mah, C., Mapstone, G., McLaughlin, P. A., Mees, J., Meland, K., Messing, C. G., Mills, C. E., Molodtsova, T. N., Mooi, R., Neuhaus, B., Ng, P. K., Nielsen, C., Norenburg, J., Opresko, D. M., Osawa, M., Paulay, G., Perrin, W., Pilger, J. F., Poore, G. C., Pugh, P., Read, G. B., Reimer, J. D., Rius, M., Rocha, R. M., Saiz-Salinas, J. I., Scarabino, V., Schierwater, B., Schmidt-Rhaesa, A., Schnabel, K. E., Schotte, M., Schuchert, P., Schwabe, E., Segers, H., Self-Sullivan, C., Shenkar, N., Siegel, V., Sterrer, W., St ö hr, S., Swalla, B., Tasker, M. L.,Thuesen, E. V., Timm, T., Todaro, M. A., Turon, X., Tyler, S., Uetz, P., van der Land, J., Vanhoorne, B., van Ofwegen, L. P., van Soest, R. W., Vanaverbeke, J., Walker-Smith, G., Walter, T. C., Warren, A., Williams, G. C., Wilson, S. P. & Costello, M. J. (2012): The magnitude of global marine species diversity. Curr. Biol. 22: 2189 – 2202.

Armenteros, M., Ruiz-Abierno, A., Fernandez-Gracez, R., Perez-Garcia, J. A., Diaz-Asencio, L., Vincx, M. & Decraemer, W. (2009): Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Carribean Sea. Estuarine Coastal Shelf Sci. 85: 179 – 189.

Armenteros, M., Perez-Garcia, J. A., Tuiz-Abierno, A., Diaz-Asencio, L., Helguera, Y., Vincx, M. & Decraemer, W. (2010): Effects of organic enrichment on nematode assemblages in a microcosm experiment. Mar. Environ. Res. 70: 374 – 382.

Armonies, W. & Reise, K. (2000): Faunal diversity across a sandy shore. Mar. Ecol. Prog. Ser. 196: 49 – 57.

Arroyo, N. L., Maldonado, M., Perez-Portela, R. & Benito, B. (2004): Distribution patterns of meiofauna associated with a sublittoral Laminaria bed in the Cantabrian Sea (northeastern Atlantic). Mar. Biol. 144: 231 – 242.

Atilla, N., Wetzel, M. A. & Fleeger, J. W. (2003): Abundance and colonization potential of artificial hard substrate associated meiofauna. J. Exp. Mar. Biol. Ecol. 287: 273 – 287.

Austen, M. C., Warwick, R. M. & Ryan, K. P. (1993): Astomonema southwardorum sp. nov. a gutless nematode dominant in a methane seep area in the North Sea. J. Mar. Biol. Assoc. U. K. 73: 627 – 634.

Austen, M. C., McEvoy, A. J. & Warwick, R. M. (1994): The specificity of meiobenthic community responses to different pollutants: results from microcosm experiments. Mar. Pollut. Bull. 28: 557 – 563.

Austen, M. C. & McEvoy, A. J. (1997): The use of offshore meiobenthic communities in laboratory microcosm experiments: response to heavy metal contamination. J. Exp. Mar. Biol. Ecol. 211: 247 – 261.

Austen, M. C. & Somerfield, P. J. (1997): A community level sediment bioassay applied to an estuarine heavy metal gradient. Mar. Environ. Res. 43: 315 – 328.

Austen, M. C. & Widdicombe, S. (1998): Experimental evidence of effects of the heart urchin Brissopsis lyrifera on associated subtidal meiobenthic nematode communities. J. Exp. Mar. Biol. Ecol. 222: 219 – 238.

Austen, M. C., Widdicombe, S. & Villano-Pitacco, N. (1998): Effects of biological disturbance on diversity and structure of meiobenthic nematode communities. Mar. Ecol. Prog. Ser. 174: 233 – 246.

Austen, M. C. & Thrush, S. F. (2001): Experimental evidence suggesting slow or weak response of nematode community structure to a large suspension-feeder. J. Sea Res. 46: 69 – 84.

Austen, M. C. & Widdicombe, S. (2006): Comparison of the response of meio- and macrobenthos to disturbance and organic enrichment. J. Exp. Mar. Biol. Ecol. 330: 96 – 104.

Avise, J. (1994): Molecular markers: natural history and evolution, Second edition . Sinauer Associates, Sunderland.

Bell, S. S., Watzin, M. C. & Coull, B. C. (1978): Biogenic structure and its effects on the spatial heterogeneity of meiofauna in a salt marsh. J. Exp. Mar. Biol. Ecol. 35: 99 – 107.

Bell, S. S. (1980): Meiofauna-macrofauna interactions in a high salt-marsh habitat. Ecol. Monographs 50: 487 – 505.

Bevilacqua, S., Sandulli, R., Plicanti, A. & Terlizzi, A. (2012): Taxonomic distinctness in Mediterranean marine nematodes and its relevance for environmental impact assessment. Mar. Pollut. Bull. 64: 1409 – 1416.

Beyrem, H., Mahmoudi, E., Essid, N., Hedfi, A., Boufahja, F. & Aissa, P. (2007): Individual and combined effects of cadmium and diesel on a nematode community in a laboratory microcosm experiment. Ecotoxicol. Environ. Saf. 68: 412 – 418.

Bhadury, P., Austen, M. C., Bilton, D. T., Lambshead, P. J. D., Rogers, A. D. & Smerdon, G. R. (2008): Evaluation of combined morphological and molecular techniques for marine nematode ( Terschellingia spp.) identification. Mar. Biol. 154: 509 – 518.

Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. & Das, I. (2007): Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148 – 155.

Bik, H. M., Thomas, W. K., Lunt, D. H. & Lambshead, P. J. D. (2010): Low endemism, continued deep-shallow interchanges, and evidence for cosmopolitan distributions in free-living marine nematodes (order Enoplida). BMC Evol. Biol. 10: 389.

Biles, C. L., Paterson, D. M., Ford, R. B., Solan, M. & Raffaelli, D. G. (2002): Bioturbation, ecosystem functioning and community structure. Hydro. Earth Syst. Sci. 6: 999 – 1005.

Birky, C. W., Ricci, C., Melone, G. & Fontaneto, D. (2010): Integrating DNA and morphological taxonomy to describe diversity in poorly studied microscopic animals: new species of the genus Abrochtha Bryce, 1910 (Rotifera: Bdelloidea: Philodinavidae). Zool. J. Linn. Soc. 161: 723 – 734.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

142   3 Ecology of free-living marine nematodes

Blanchard, G. F. (1990): Overlapping microscale dispersion patterns of meiofauna and microphytobenthos. Mar. Ecol. Prog. Ser. 68: 101 – 111.

Boeckner, M. J., Sharma, J. & Proctor, H. C. (2009): Revisiting the meiofauna paradox: dispersal and colonization of nematodes and other meiofaunal organisms in low- and high-energy environments. Hydrobiologia 624: 91 – 106.

Boetius, A., Ferdelman, T. & Lochte, K. (2000): Bacterial activity in sediments of the deep Arabian Sea in relation to vertical flux. Deep Sea Res. Part II 47: 2835 – 2875.

Bongers, T. (1990): The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14 – 19.

Bongers, T., Alkemade, R. & Yeates, G. W. (1991): Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the Maturity Index. Mar. Ecol. Prog. Ser. 76: 135 – 142.

Bongers, T. & Ferris, H. (1999): Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol. Evol. 14: 224 – 228.

Bostrom, C., Tornroos, A. & Bonsdorff, E. (2009): Invertebrate dispersal and habitat heterogeneity: expression of biological traits in a seagrass landscape. J. Exp. Mar. Biol. Ecol. 390: 106 – 117.

Boucher, G. & Lambshead, P. J. D. (1995): Ecological biodiversity of marine nematodes in samples from temperate, tropical and deep-sea regions. Conserv. Biol. 9: 1594 – 1604.

Bouchet, V. M. P., Sauriau, P. G., Debenay, J. P., Mermillod-Blondin, F., Schmidt, S., Amiard, J. C. & Dupas, B. (2009): Influence of the mode of macrofauna-mediated bioturbation on the vertical distribution of living benthic foraminifera: first insight from axial tomodensitometry. J. Exp. Mar. Biol. Ecol. 371: 20 – 33.

Boufahja, F., Sellami, B., Dellali, M., Aissa, P., Mahmoudi, E. & Beyrem, H. (2011): A microcosm experiment on the effects of permethrin on a free-living nematode assemblage. Nematology 13: 901 – 909.

Braeckman, U., Provoost, P., Moens, T., Soetaert, K., Middelburg, J. J., Vincx, M. & Vanaverbeke, J. (2011a): Biological vs. physical mixing effects on benthic food web dynamics. PLoS One 6: e18078.

Braeckman, U., Van Colen, C., Soetaert, K., Vincx, M., Vanaverbeke, J. (2011b): Contrasting macrobenthic activities differentially affect nematode density and diversity in a shallow subtidal marine sediment. Mar. Ecol. Prog. Ser. 422: 179 – 191.

Braeckman, U., Vanaverbeke, J., Vincx, M., Van Oevelen, D. & Soetaert, K. (2013): Meiofauna metabolism in suboxic sediments: currently overestimated. PLoS One 8: e59289.

Brown, C. J., Lambshead, P. J. D., Smith, C. R., Hawkins, L. E. & Farley, R. (2001): Phytodetritus and the abundance and biomass of abyssal nematodes in the central, equatorial Pacific. Deep Sea Res. Part I 48: 555 – 565.

Callaway, R. (2006): Tube worms promote community change. Mar. Ecol. Prog. Ser. 308: 49 – 60.

Carman, K. R. & Fry, B. (2002): Small-sample methods for δ 13 C and δ 15 N analysis of the diets of marsh meiofaunal species using natural-abundance and tracer-addition isotope techniques. Mar. Ecol. Prog. Ser. 240: 85 – 92.

Chase, J. M. & Myers, J. A. (2011): Disentangling the importance of ecological niches from stochastic processes across scales. Phil. Trans. R. Soc. London, Ser. B 366: 2351 – 2363.

Chia, F. S. & Warwick, R. M. (1969): Assimilation of labelled glucose from seawater by marine nematodes. Nature 224: 720 – 721.

Clarke, K. R. & Warwick, R. M. (2001): Change in marine communities: an approach to statistical analysis and interpretation, Second edition . PRIMER-E, Plymouth.

Clarke, K. R. & Gorley, R. N. (2006): PRIMER v6: User Manual/Tutorial . PRIMER-E, Plymouth.

Commito, J. A. & Tita, G. (2002): Differential dispersal rates in an intertidal meiofauna assemblage. J. Exp. Mar. Biol. Ecol. 268: 237 – 256.

Connell, J. H. (1978): Diversity in tropical rain forests and coral reefs – high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199: 1302 – 1310.

Cook, A. A., Lambshead, P. J. D., Hawkins, L. E., Mitchell, N. & Levin, L. A. (2000): Nematode abundance at the oxygen mini mum zone in the Arabian Sea. Deep Sea Res. Part II 47: 75 – 78.

Coomans, A. (2002): Present status and future of nematode systematics. Nematology 4: 573 – 582.

Couch, C. A. (1989): Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuarine Coastal Shelf Sci. 28: 433 – 441.

Coull, B. C. & Chandler, G. T. (1992): Pollution and meiofauna: field, laboratory, and mesocosm studies. Oceanograph. Mar. Biol. Ann. Rev. 30: 191 – 271.

Coull, B. C. (1999): Role of meiofauna in estuarine soft-bottom habitats. Aus. J. Ecol. 24: 327 – 343.

Cullen, D. J. (1973): Bioturbation of superficial marine sediments by interstitial meiobenthos. Nature 242: 323 – 324.

Danovaro, R., Fabiano, M. & Vincx, M. (1995): Meiofauna response to the Agip Abruzzo oil spill in subtidal sediments of the Ligurian Sea. Mar. Pollut. Bull. 30: 133 – 145.

Danovaro, R., Gambi, C. & Della Croce, N. (2002): Meiofauna hotspot in the Atacama Trench (Southern Pacific Ocean). Deep Sea Res. Part I 49: 843 – 857.

Danovaro, R., Scopa, M., Gambi, C. & Fraschetti, S. (2007): Trophic importance of subtidal metazoan meiofauna: evidence from in situ exclusion experiments on soft and rocky substrates. Mar. Biol. 152: 339 – 350.

Danovaro, R., Gambi, C., Dell ’ Anno, A., Corinaidesi, C., Fraschetti, S., Vanreusel, A., Vincx, M. & Gooday, A. J. (2008a): Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Curr. Biol. 18: 1 – 8.

Danovaro, R., Gambi, C., Lampadariou, N. & Tselepides, A. (2008b): Deep-sea nematode biodiversity in the Mediterranean basin: testing for longitudinal, bathymetric and energetic gradients. Ecography 3: 231 – 244.

Danovaro, R., Bianchelli, S., Gambi, C., Mea, M. & Zeppilli, D. (2009a): α -, β -, γ -, δ - and ε -diversity of deep-sea nematodes in canyons and open slopes of Northeast Atlantic and Mediterranean margins. Mar. Ecol. Prog. Ser. 396: 197 – 209.

Danovaro, R., Corinaldesi, C., Luna, G. M., Magagnini, M., Manini, E. & Pusceddu, A. (2009b): Prokaryote diversity and viral production in deep-sea sediments and seamounts. Deep Sea Res. Part II 56: 738 – 747.

Danovaro, R. (2012): Extending the approaches of biodiversity and ecosystem functioning to the deep ocean. In: Solan, M., Aspden, R. J. & Paterson, D. M. (eds.) Marine Biodiversity and Ecosystem Functioning: Frameworks, Methodologies, and Integration, pp 115 – 126. Oxford University Press, Oxford.

Dashfield, S. L., Somerfield, P. J., Widdicombe, S., Austen, M. C. & Nimmo, M. (2008): Impacts of ocean acidification and

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   143

burrowing urchins on within-sediment pH profiles and subtidal nematode communities. J. Exp. Mar. Biol. Ecol. 365: 46 – 52.

Dayton, P. K. (1971): Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monograph 41: 351 – 388.

de Leon, G. P. P. & Nadler, S. A. (2010): What we don ’ t recognize can hurt us: a plea for awareness about cryptic species. J. Parasitol. 96: 453 – 464.

De Meester, N., Derycke, S., Bonte, D. & Moens, T. (2011): Salinity effects on the coexistence of cryptic species: a case study on marine nematodes. Mar. Biol. 158: 2717 – 2726.

De Meester, N., Derycke, S. & Moens, T. (2012): Differences in time until dispersal between cryptic species of a marine nematode species complex. PLoS One 7: e42674.

De Mesel, I., Derycke, S., Swings, J., Vincx, M. & Moens, T. (2003): Influence of bacterivorous nematodes on the decomposition of cordgrass. J. Exp. Mar. Biol. Ecol. 296: 227 – 242.

De Mesel, I., Derycke, S., Moens, T., Van der Gucht, K., Vincx, M. & Swings, J. (2004): Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ. Microbiol. 6: 733 – 744.

De Mesel, I., Derycke, S., Swings, J., Vincx, M. & Moens, T. (2006): Role of nematodes in decomposition processes: Does within-trophic group diversity matter? Mar. Ecol. Prog. Ser. 321: 157 – 166.

De Oliveira, D. A. S., Decraemer, W., Holovachov, O., Burr, J., De Ley, I. T., De Ley, P., Moens, T. & Derycke, S. (2012): An integrative approach to characterize cryptic species in the Thoracostoma trachygaster Hope, 1967 complex (Nematode: Leptosomatidae). Zool. J. Linn. Soc. 164: 18 – 35.

Decho, A. W. & Fleeger, J. W. (1988): Microscale dispersion of mei-obenthic copepods in response to food-resource patchiness. J. Exp. Mar. Biol. Ecol. 118: 229 – 243.

DePatra, K. D. & Levin, L. A. (1989): Evidence of the passive deposition of meiofauna into fiddler crab burrows. J. Exp. Mar. Biol. Ecol. 125: 173 – 192.

Deprez, T., Steyaert, M., Vanaverbeke, J., Speybroeck, J. & Raes, M. (2005): NeMys. Generic Biological Information Service (online). Available at: nemys.ugent.be.

Derycke, S., Remerie, T., Vierstraete, A., Backeljau, T., Vanfleteren, J., Vincx, M. & Moens, T. (2005): Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar. Ecol. Prog. Ser. 300: 91 – 103.

Derycke, S., Backeljau, T., Vlaeminck, C., Vierstraete, A., Vanfleteren, J., Vincx, M. & Moens, T. (2006): Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida). Genetica 128: 307 – 321.

Derycke, S., Backeljau, T., Vlaeminck, C., Vierstraete, A., Vanfleteren, J., Vincx, M. & Moens, T. (2007a): Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar. Biol. 151: 1799 – 1812.

Derycke, S., Hendrickx, F., Backeljau, T., D ’ Hondt, S., Camphijn, L., Vincx, M. & Moens, T. (2007b): Effects of sublethal abiotic stressors on population growth and genetic diversity of Pellioditis marina (Nematoda) from the Westerschelde estuary. Aquat. Toxicol. 82: 110 – 119.

Derycke, S., Van Vynckt, R., Vanaverbeke, J., Vincx, M. & Moens, T. (2007c): Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and

genetic structure of the dominant species Pellioditis marina. Limnol. Oceanogr. 52: 992 – 1001.

Derycke, S., Fonseca, G., Vierstraete, A., Vanfleteren, J., Vincx, M. & Moens, T. (2008a): Disentangling taxonomy within the Rhabditis (Pellioditis) marina (Nematoda, Rhabditidae) species complex using molecular and morphological tools. Zool. J. Linn. Soc. 152: 1 – 15.

Derycke, S., Remerie, T., Backeljau, T., Vierstraete, A., Vanfleteren, J., Vincx, M. & Moens, T. (2008b): Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Mol. Ecol. 17: 3306 – 3322.

Derycke, S., De Ley, P., De Ley, I. T., Holovachov, O., Rigaux, A. & Moens, T. (2010a): Linking DNA sequences to morphology: cryptic diversity and population genetic structure in the marine nematode Thoracostoma trachygaster (Nematoda, Leptosomatidae). Zool. Scripta 39: 276 – 289.

Derycke, S., Vanaverbeke, J., Rigaux, A., Backeljau, T. & Moens, T. (2010b): Exploring the use of cytochromoe oxydase c subunit I (COI) for DNA barcoding of free-living marine nematodes. PLoS One 5: e13716.

Derycke, S., Backeljau, T. & Moens, T. (2013): Dispersal and gene flow in free living marine nematodes. Front. Zool. 10: 1.

Dittmann, S. (1996): Effects of macrobenthic burrows on infaunal communities in tropical tidal flats. Mar. Ecol. Prog. Ser. 134: 119 – 130.

Dos Santos, G. A. P., Derycke, S., Fons ê ca-Genevois, V. G., Coelho, L. C. B. B., Correia, M. T. S. & Moens, T. (2008): Differential effects of food availability on population growth and fitness of three species of estuarine, bacterial-feeding nematodes. J. Exp. Mar. Biol. Ecol. 355: 27 – 40.

Dos Santos, G. A. P. (2009): Top-Down and Bottom-Up Controls on Populations and Assemblages of Marine Nematodes, and their Effects on Benthic Ecosystem Functioning: an Experimental Approach . Ph.D. thesis. Ghent University, Belgium.

Dos Santos, G. A. P., Derycke, S., Fons ê ca-Genevois, V. G., Coelho, L., Correia, M. T. S. & Moens, T. (2009): Interactions among bacterial-feeding nematode species at different levels of food availability. Mar. Biol. 156: 629 – 640.

Eckman, J. & Thistle, D. (1988): Small-scale spatial pattern in meiobenthos in the San Diego Trough. Deep Sea Res. Part A 35: 1565 – 1578.

Eckman, J. E. & Thistle, D. (1991): Effects of flow about a biologically produced structure on harpacticoid copepods in San-Diego Trough. Deep Sea Res. Part A 38: 1397 – 1416.

Egge, J. J. D. & Simons, A. M. (2006): The challenge of truly cryptic diversity: diagnosis and description of a new madtom catfish (Ictaluridae: Noturus). Zool. Scripta 35: 581 – 595.

Ehrlich, P. R. & Ehrlich, A. H. (1981): Extinction: The Causes and Consequences of the Disappearance of Species . Random House, New York.

Eskin, R. A. & Palmer, M. A. (1985): Suspension of marine nematodes in a turbulent tidal creek - species patterns. Biol. Bull. 169: 615 – 623.

Fenchel, T. & Riedl, R. J. (1970): The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar. Biol. 7: 255 – 268.

Fenchel, T. & Finlay, B. J. (2004): The ubiquity of small species: patterns of local and global diversity. BioScience 54: 777 – 784.

Findlay, S. E. G. (1981): Small-scale spatial distribution of meiofauna on a mud- and sandflat. Estuarine Coastal Shelf Sci. 12: 471 – 484.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

144   3 Ecology of free-living marine nematodes

Findlay, S. & Tenore, K. R. (1982): Effect of a free-living marine nematode ( Diplolaimella chitwoodi ) on detrital carbon mineralization. Mar. Ecol. Prog. Ser. 8: 161 – 166.

Finney, D. (1941): On the distribution of a variate whose logarithm is normally distributed. J. Roy. Stat. Soc. 7, Suppl.: 155 – 161.

Fleeger, J. W. & Carman, K. R. (2011): Experimental and genetic studies of meiofauna assess environmental quality and reveal mechanisms of pollution fate and effects. Vie et Milieu 61: 1 – 26.

Fonseca, G. & Soltwedel, T. (2007): Deep-sea meiobenthic communities underneath the marginal ice zone off Eastern Greenland. Polar Biol. 30: 607 – 618.

Fonseca, G. & Muthumbi, A. & Vanreusel, A. (2007): Species richness of the genus Molgolaimus (Nematoda) from local to ocean scale along continental slopes. Mar. Ecol. 28: 446 – 459.

Fonseca, G, Gallucci, F. (2008): Direct evidence of predation in deep-sea nematodes: the case of Pontonema sp. Cah. Biol. Mar. 49: 295 – 297.

Fonseca, G., Derycke, S. & Moens, T. (2008): Integrative taxonomy in two free-living nematode species complexes. Biol. J. Linnean Soc. 94: 737 – 753.

Fonseca, G. & Soltwedel, T. (2009): Regional patterns of nematode assemblages in the Arctic deep seas. Polar Biol. 32: 1345 – 1357.

Fonseca, G., Soltwedel, T., Vanreusel, A. & Lindegarth, M. (2010): Variation in nematode assemblages over multiple spatial scales and environmental conditions in Arctic deep seas. Prog. Oceanogr. 84: 174 – 184.

Fonseca, G., Hutchings, P., Vieira, D. C. & Gallucci, F. (2011): Meiobenthic community underneath the carcass of a stingray: a snapshot after natural death. Aquat. Biol. 13: 27 – 33.

Fonseca, G. & Fehrlauer-Ale, K. (2012): Three in one: fixing marine nematodes for ecological, molecular and morphological studies. Limnol. Oceanogr.: Methods 10: 516 – 523.

Fons ê ca-Genevois, V., Somerfield, P. J., Neves, M. H. B., Coutinho, R. & Moens, T. (2006): Colonization and early succession on artificial hard substrata by meiofauna. Mar. Biol. 148: 1039 – 1050.

Fontaneto, D. (2006): Biogeography of Microscopic Organisms: Is Everything Small Everywhere? Cambridge University Press, Cambridge.

Franco, M. A., Soetaert, K., Costa, M. J., Vincx, M. & Vanaverbeke, J. (2008a): Uptake of phytodetritus by meiobenthos using C-13 labelled diatoms and Phaeocystis in two contrasting sediments from the North Sea. J. Exp. Mar. Biol. Ecol. 362: 1 – 8.

Franco, M. A., Soetaert, K., Van Oevelen, D., Van Gansbeke, D., Costa, M. J., Vincx, M. & Vanaverbeke, J. (2008b): Density, vertical distribution and trophic responses of metazoan meiobenthos to phytoplankton deposition in contrasting sediment types. Mar. Ecol. Prog. Ser. 358: 51 – 62.

Franco, M. A., Vanaverbeke, J., Van Oevelen, D., Soetaert, K., Costa, M. J., Vincx, M. & Moens, T. (2010): Respiration partitioning in contrasting subtidal sediments: seasonality and response to a spring phytoplankton deposition. Mar. Ecol. 31: 276 – 290.

Fry, B. (2008): Stable Isotope Ecology, Third edition . Springer, New York. Gallucci, F., Steyaert, M. & Moens, T. (2005): Can field distributions

of marine predacious nematodes be explained by sediment constraints on their foraging success? Mar. Ecol. Prog. Ser. 304: 167 – 178.

Gallucci, F., Fonseca, G. & Soltwedel, T. (2008a): Effects of megafauna exclusion on nematode assemblages at a deep-sea site. Deep Sea Res. Part I 55: 332 – 349.

Gallucci, F., Moens, T., Vanreusel, A. & Fonseca, G. (2008b): Active colonization of disturbed sediments by deep-sea nematodes:

evidence for the patch mosaic model. Mar. Ecol. Prog. Ser. 367: 173 – 183.

Gallucci, F., Moens, T. & Fonseca, G. (2009): Small-scale spatial patterns of meiobenthos in the Arctic deep sea. Mar. Biodiversity 39: 9 – 25.

Gambi, C. & Danovaro, R. (2006): A multiple-scale analysis of metazoan meiofaunal distribution in the deep Mediterranean Sea. Deep Sea Res. Part I 53: 1117 – 1134.

Gambi, C., Lampadariou, N. & Danovaro, R. (2010): Latitudinal, longitudinal and bathymetric patterns of abundance, biomass of metazoan meiofauna: importance of the rare taxa and anomalies in the deep Mediterranean Sea. Adv. Oceanogr. Limnol. 1: 167 – 197.

Garcia, R. & Johnstone, R. W. (2006): Effects of Lyngbya majuscula (Cyanophycea) blooms on sediment nutrients and meiofaunal assemblages in seagrass beds in Moreton Bay, Australia. Mar. Freshwater Res. 57: 155 – 165.

Gerlach, S. A. (1971): On the importance of marine meiofauna for benthos communities. Oecologia 6: 176 – 190.

Gerlach, S. (1977): Attraction to decaying organisms as a possible cause for patchy distribution of nematodes in Bermuda beach. Ophelia 16: 151 – 165.

Gheskiere, T., Hoste, E., Vanaverbeke, J., Vincx, M. & Degraer, S. (2004): Horizontal zonation patterns and feeding structure of marine nematode assemblages on a macrotidal, ultra-dissipative sandy beach (De Panne, Belgium). J. Sea Res. 52: 221 – 226.

Gheskiere, T. (2005): Nematode Assemblages from European Sandy Beaches: Diversity, Zonation Patterns and Tourist Impact . Ph.D. thesis. Ghent University, Belgium.

Gheskiere, T., Vincx, M., Urban-Malinga, B., Rossano, C., Scapini, F. & Degraer, S. (2005): Nematodes from wave-dominated sandy beaches: diversity, zonation patterns and testing of the isocommunities concept. Estuarine Coastal Shelf Sci. 62: 365 – 375.

Gheskiere, T., Vincx, M., Pison, G. & Degraer, S. (2006): Are strandline meiofaunal assemblages affected by a once-only mechanical beach cleaning? Experimental findings. Mar. Environ. Res. 61: 245 – 264.

Giere, O., Windoffer, R. & Southward, E. C. (1995): The bacterial endosymbiosis of the gutless nematode, Astomonema southwardorum — ultrastructural aspects. J. Mar. Biol. Assoc. U. K. 75: 153 – 164.

Giere, O. (2009): Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments, Second edition. Springer-Verlag, Berlin.

Gingold, R., Mundo-Ocampo, M., Holovachov, O. & Rocha-Olivares, A. (2010): The role of habitat heterogeneity in structuring the community of intertidal free-living marine nematodes. Mar. Biol. 157: 1741 – 1753.

Gingold, R., Moens, T. & Rocha Olivares, A. (2013): Assessing the response of nematode communities to climate change driven warming: a microcosm experiment. PLoS One 8: e66653.

Gobin, J. F. (2007): Free-living marine nematodes of hard bottom substrates in Trinidad and Tobago, West Indies. Bull. Mar. Sci. 81: 73 – 84.

Graf, G. (1989): Benthic pelagic coupling in a deep-sea benthic community. Nature 341: 437 – 439.

Gray, J. S. (1981): The Ecology of Marine Sediments. An Introduction to the Structure and Function of Benthic Communities. Cambridge Studies in Modern Biology, Vol. 2. Cambridge University Press, Cambridge.

Gray, J. S. (2000): The measurement of marine species diversity with an application to the benthic fauna of the Norwegian continental shelf. J. Exp. Mar. Biol. Ecol. 250: 23 – 49.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   145

Gray, J. S. (2002): Species richness of marine soft sediments. Mar. Ecol. Prog. Ser. 244: 285 – 297.

Grime, J. P. (1973): Competitive exclusion in herbaceous vegetation. Nature 242: 344 – 347.

Guarini, J. M., Blanchard, G. F., Gros, P. & Harrison, S. J. (1997): Model ling the mud surface temperature on intertidal flats to investigate the spatio-temporal dynamics of the benthic microalgal photosynthetic capacity. Mar. Ecol. Prog. Ser. 153: 25 – 36.

Guidi-Guilvard, L. D., Thistle, D., Khripounoff, A. & Gasparini, S. (2009): Dynamics of benthic copepods and other meiofauna in the benthic boundary layer of the deep NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 396: 181 – 195.

Guilini, K., Van Oevelen, D., Soetaert, K., Middelburg, J. J. & Vanreusel, A. (2010): Nutritional importance of benthic bacteria for deep-sea nematodes from the Arctic ice margin: results of an isotope tracer experiment. Limnol. Oceanogr. 55: 1977.

Guilini, K., Soltwedel, T., van Oevelen, D. & Vanreusel, A. (2011): Deep-sea nematodes actively colonise sediments, irrespective of the presence of a pulse of organic matter: results from an in-situ experiment. PLoS One 6: e18912.

Guilini, K., Levin, L. A. & Vanreusel, A. (2012): Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Paci fi c Ocean). Prog. Oceanogr. 96: 77 – 92.

Gutierrez, D., Enriquez, E., Purca, S., Quipuzcoa, L., Marquina, R., Flores, G. & Graco, M. (2008): Oxygenation episodes on the continental shelf of central Peru: remote forcing and benthic ecosystem response. Prog. Oceanogr. 79: 177 – 189.

Gyedu-Ababio, T. K. & Baird, D. (2006): Response of meiofauna and nematode communities to increased levels of contaminants in a laboratory microcosm experiment. Ecotoxicol. Environ. Saf. 63: 443 – 450.

Hamels, I., Moens, T., Muylaert, K. & Vyverman, W. (2001): Trophic interactions between ciliates and nematodes from an intertidal flat. Aquat. Microb. Ecol. 26: 61 – 72.

Hasemann, C. & Soltwedel, T. (2011): Small-scale heterogeneity in deep-sea nematode communities around biogenic structures. PLoS One 6: e29152.

Hedqvist-Johnson, K. & Andre, C. (1991): The impact of the brown shrimp Crangon crangon L on soft-bottom meiofauna - an experimental approach. Ophelia 34: 41 – 49.

Heip, C., Vincx, M. & Vranken, G. (1985): The ecology of marine nematodes. Oceanogr. Mar. Biol. Ann. Rev. 23: 399 – 489.

Heip, C., Huys, R., Vincx, M., Vanreusel, A., Smol, N., Herman, R. & Herman, P. M. J. (1990): Composition, distribution, biomass and production of North Sea meiofauna. Neth. J. Sea Res. 26: 333 – 342.

Heip, C., Herman, P. & Soetaert, K. (1998): Indices of diversity and evenness. Oceanis 24: 61 – 87.

Hellwig-Armonies, M., Armonies, W. & Lorenzen, S. (1991): The diet of Enoplus brevis (Nematoda) in a supralittoral salt-marsh of the North Sea. Helgol ä nder Meeresuntersuchungen 45: 357 – 372.

Hendelberg, M. & Jensen, P. (1993): Vertical distribution of the nematode fauna in a coastal sediment influenced by seasonal hypoxia in the bottom water. Ophelia 37: 83 – 94.

Herman, P. M. J., Vranken, G. & Heip, C. (1984): Problems in meiofauna energy-flow studies. Hydrobiologia 118: 21 – 28.

Herman, P. M. J. & Vranken, G. (1988): Studies of the life-history and energetics of marine and brackish-water nematodes. I. Production, respiration and food uptake by Monhystera disjuncta. Oecologia 77: 457 – 463.

Hinz, H., Hiddink, J. G., Forde, J. & Kaiser, M. (2008): Large-scale responses of nematode communities to chronic otter-trawl disturbance. Can. J. Fish. Aqaut. Sci. 65: 723 – 732.

Hodda, M. (1990): Variation in estuarine littoral nematode populations over three spatial scales. Estuarine Coastal Shelf Sci. 30: 325 – 340.

Hogue, E. W. & Miller, C. B. (1981): Effects of sediment microto-pography on small-scale spatial distributions of meiobenthic nematodes. J. Exp. Mar. Biol. Ecol. 53: 181 – 191.

Hogue, E. W. (1982): Sediment disturbance and the spatial distributions of shallow water meiobenthic nematodes on the open Oregon coast. J. Mar. Res. 40: 551 – 573.

Hooper, D. U., Chapin III, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Set ä l ä , H., Symstad, A. J., Vandermeer, J. & Wardle, D. A. (2005): Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monograph 75: 3 – 35.

Howell, R. (1984): Acute toxicity of heavy metals to two species of marine nematodes. Mar. Environ. Res. 11: 153 – 161.

Hugot, J. P., Baujard, P. & Morand, S. (2001): Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3: 199 – 208.

Hubas, C., Sachidhanandam, C., Rybarczyk, H., Lubarsky, H. V., Rigaux, A., Moens, T. & Paterson, D. M. (2010): Bacterivorous nematodes stimulate microbial growth and exopolymer production in marine sediment microcosms. Mar. Ecol. Prog. Ser. 419: 85 – 94.

Huettel, R. N. (1986): Chemical communicators in nematodes. J Nematol. 18: 3 – 8.

Humphreys, W. F. (1979): Production and respiration in animal populations. J. Anim. Ecol. 48: 427 – 453.

Hurlbert, S. H. (1971): The nonconcept of species diversity: a critique and alternative parameters. Ecology 52: 577 – 586.

Huston, M. (1979): General hypothesis of species diversity. Am. Nat. 113: 81 – 101.

Huston, M. (1994): Biological Diversity: The Coexistence of Species on Changing Landscapes . Cambridge University Press, Cambridge.

Iken, K., Brey, T., Wand, U., Voigt, J. & Junghans, P. (2001): Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog. Oceanogr. 50: 383 – 405.

Ingels, J., Vanhove, S., De Mesel, I. & Vanreusel, A. (2006): The biodiversity and biogeography of the free-living nematode genera Desmodora and Desmodorella (family Desmodoridae) at both sides of the Scotia Arc. Polar Biol. 29: 936 – 949.

Ingels, J., Kiriakoulakis, K., Wolff, G. A., Vanreusel, A. (2009): Nematode diversity and its relation to the quantity and quality of sedimentary organic matter in the deep Nazar é Canyon, Western Iberian Margin. Deep Sea Res. Part I 56: 1521 – 1539.

Ingels, J., Van den Driessche, P., De Mesel, I., Vanhove, S., Moens, T. & Vanreusel, A. (2010): Preferred use of bacteria over phytoplankton by deep-sea nematodes in polar regions. Mar. Ecol. Prog. Ser. 406: 121 – 133.

Ingels, J., Billett, D. S. M., Kiriakoulakis, K., Wolff, G. A. & Vanreusel, A. (2011a): Structural and functional diversity of Nematoda in relation with environmental variables in the Set ú bal and Cascais canyons, Western Iberian Margin. Deep Sea Res. Part II 58: 2354 – 2368.

Ingels, J., Billett, D. S. M. & Vanreusel, A. (2011b): An insight into the feeding ecology of deep-sea canyon nematodes - Results from field observations and the first in-situ 13 C feeding experiment in the Nazar é Canyon. J. Exp. Mar. Biol. Ecol. 396: 185 – 193.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

146   3 Ecology of free-living marine nematodes

Ingels, J., Tchesunov, A. & Vanreusel, A. (2011c): Meiofauna in the Gollum Channels and the Whittard Canyon, Celtic Margin - how local environmental conditions shape nematode structure and function. PLoS One 6: e20094.

Ingels, J. & Vanreusel, A. (2013): The importance of different spatial scales in determining structure and function of deep-sea infauna communities. Biogeosci. Discuss. 10: 195 – 232.

Jacobs, L. J. (1988): Monografische studie van de Monhysteridae de Man, 1876 (Nematoda) . Ph.D. dissertation, Ghent University, Ghent.

Jager, T., Alvarez, O. A., Kammenga, J. E. & Kooijman, S. A. L. M. (2005): Modeling nematode life cycles using dynamic energy budgets. Funct. Ecol. 19: 136 – 144.

Jansson, B. O. (1968): Quantitative and experimental studies of the interstitial fauna in four Swedish sandy beaches. Ophelia 5: 1 – 71.

Jensen, P. (1981): Phyto-chemical sensitivity and swimming behavior of the free-living marine nematode Chromadorita tenuis. Mar. Ecol. Prog. Ser. 4: 203 – 206.

Jensen, P. (1982): Diatom-feeding behaviour of the free-living marine nematode Chromadorita tenuis. Nematologica 28: 71 – 76.

Jensen, P. (1986): Nematode fauna in the sulphide-rich brine seep and adjacent bottoms of the East Flower Garden, NW Gulf of Mexico. Mar. Biol. 92: 489 – 503.

Jensen, P. (1987a): Feeding ecology of free-living aquatic nematodes. Mar. Ecol. Prog. Ser.s 35: 187 – 196.

Jensen, P. (1987b): Differences in microhabitat, abundance, biomass and body size between oxybiotic and thiobiotic freeliving marine nematodes. Oecologia 71: 1432 – 1939.

Jones, C. G., Lawton, J. H. & Shachak, M. (1994): Organisms as ecosystem engineers. Oikos 69: 373 – 386.

Jost, L. (2008): GST and its relatives do not measure differentiation. Mol. Ecol. 17: 4015 – 4026.

Kammenga, J. E., Van Gestel, C. A. M. & Bakker, J. (1994): Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Arch. Environ. Contam. Toxicol. 27: 88 – 94.

Kennedy, A. D. & Jacoby, C. A. (1999): Biological indicators of marine environmental health: meiofauna- a neglected component? Environ. Monit. Assess. 54: 47 – 68.

Knowlton, N. (2000): Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420: 73 – 90.

Kooijman, S. A. L. M. (2000): Dynamic Energy and Mass Budgets in Biological Systems, Second edition . Cambridge University Press, Cambridge.

Kristensen, E. & Kostka, J. E. (2005): Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In: Kristensen, E., Haese, R. R. & Kostka, J. E. (eds.) Interactions between Macro- and Microorganisms in Marine Sediments, Coastal and Estuarine Studies , pp 125 – 157. American Geophysical Union, New York.

Kuhne, R. (1996): Relations between free-living nematodes and dung-burying Geotrupes spp (Coleoptera: Geotrupini). Fundam. Appl. Nematol. 19: 263 – 271.

Kuipers, B. R., de Wilde, P. A. W. J. & Creutzberg, F. (1981): Energy flow in a tidal flat ecosystem. Mar. Ecol. Prog. Ser. 5: 215 – 221.

Lambshead, P. J. D. (1986): Sub-catastrophic sewage and industrial waste contamination as revealed by marine nematode faunal analysis. Mar. Ecol. Prog. Ser. 29: 247 – 260.

Lambshead, P. J. D. (1993): Recent developments in marine benthic biodiversity research. Oceanis 19: 5 – 24.

Lambshead, P. J. D., Tietjen, J., Ferrero, T. & Jensen, P. (2000): Latitudinal diversity gradients in the deep sea with special reference to North Atlantic nematodes. Mar. Ecol. Prog. Ser. 194: 159 – 167.

Lambshead, P. J. D., Brown, C. J., Ferrero, T. J., Mitchell, N. J., Smith, C. R., Hawkins, L. E. & Tietjen, J. (2002): Latitudinal diversity patterns of deep-sea marine nematodes and organic fluxes: a test from the central equatorial Pacific. Mar. Ecol. Prog. Ser. 236: 129 – 135.

Lambshead, P. J. D. & Boucher, G. (2003): Marine nematode deep-sea biodiversity - hyperdiverse or hype? J. Biogeogr. 30: 475 – 485.

Lampadariou, N., Hatziyanni, E. & Tselepides, A. (2005): Meiofaunal community structure in Thermaikos Gulf: response to intense trawling pressure. Cont. Shelf Res. 25: 2554 – 2569.

Lampadariou, N. & Tselepides, A. (2006): Spatial variability of meiofaunal communities at areas of contrasting depth and productivity in the Aegean Sea (NE Mediterranean). Prog. Oceanogr. 69: 19 – 36.

Lawton, J. H. (1994): What do species do in ecosystems? Oikos 71: 367 – 374.

Leduc, D. & Probert, P. K. (2009): The effect of bacterivorous nematodes on detritus incorporation by macrofaunal detritivores: a study using stable isotope and fatty acid analyses. J. Exp. Mar. Biol. Ecol. 371: 130 – 139.

Leduc, D., Probert, P. & Nodder, S. (2010): Influence of mesh size and core penetration on estimates of deep-sea nematode abundance, biomass, and diversity. Deep Sea Res. Part I 57: 1354 – 1362.

Leduc, D. & Probert, P. K. (2011): Small-scale effect of intertidal seagrass ( Zostera muelleri ) on meiofaunal abundance, biomass, and nematode community structure. J. Mar. Biol. Assoc. U. K. 91: 579 – 591.

Leduc, D., Rowden, A. A., Bowden, D. A., Probert, P. K., Pilditch, C. A. & Nodder, S. D. (2012): Unimodal relationship between biomass and species richness of deep-sea nematodes: implications for the link between productivity and diversity. Mar. Ecol. Prog. Ser. 454: 53 – 64.

Leduc, D. & Pilditch, C. A. (2013): Effect of a physical disturbance event on deep-sea nematode community structure and ecosystem function. J. Exp. Mar. Biol. Ecol. 440: 35 – 41.

Leduc, D., Rowden, A. A., Pilditch, C. A., Maas, E. W. & Probert, P. K. (2013): Is there a link between deep-sea biodiversity and ecosystem function? Mar Ecol 34: 334–344.

Lee, J. J., Tietjen, J. H., Mastropaolo, C. & Rubin, H. (1977): Food quality and the heterogeneous spatial distribution of meiofauna. Helgol ä nder wissenschaftliche Meeresuntersuchungen 30: 272 – 282.

Lee, M. & Riveros, M. (2012): Latitudinal trends in the species richness of free-living marine nematode assemblages from exposed sandy beaches along the coast of Chile (18 – 42 ° S). Mar. Ecol. 33: 317 – 325.

Leibold, M. A., Holyoak, M., Mouquet, N., Amrasekare, P., Chase, J. M., Hooper, M. F., Holt, R. D., Shurin, J. B., Law, R., Tilman, D., Loreau, M. & Gonzalez, A. (2004): The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7: 601 – 613.

Levin, L., Blair, N., DeMaster, D., Plaia, G., Fornes, W., Martin, C. & Thomas, C. (1997): Rapid subduction of organic matter by maldanid polychaetes on the North Carolina slope. J Mar. Res. 55: 595 – 611.

Levin, L. A. (1991): Interactions between metazoans and large agglutinating protozoans: implications for the community structure of deep-sea benthos. Integr. Comp. Biol. 31: 886 – 900.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   147

Levin, L. A., Huggett, C. L. & Wishner, K. F. (1991): Control of deep-sea benthic community structure by oxygen and organic-matter gradients in the eastern Pacific Ocean. J. Mar. Res. 49: 763 – 800.

Levin, L. A., Ekau, W., Gooday, A. J., Jorissen, F., Middelburg, J. J., Naqvi, S. W. A., Neira, C., Rabalais, N. N. & Zhang, J. (2009): Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6: 2063 – 2098.

Li, J., Vincx, M. & Herman, P. M. J. (1996): A model of nematode dynamics in the Westerschelde estuary. Ecol. Modell. 90: 271 – 284.

Li, J., Vincx, M., Herman, P. M. J. & Heip, C. (1997): Monitoring meiobenthos using cm-, m- and km-scales in the Southern Bight of the North Sea. Mar. Environ. Res. 43: 265 – 278.

Lilleb ø , A. I., Flindt, M. R., Pardal, M. Â . & Marques, J. C. (1999): The effect of macrofauna, meiofauna and microfauna on the degradation of Spartina maritima detritus from a salt marsh area. Acta Oecologica 20: 249 – 258.

Logue, J. B., Mouquet, N., Peter, H. & Hillebrand, H. (2011): Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol. Evol. 26: 482 – 491.

Lohrer, A. M., Thrush, S. F. & Gibbs, M. M. (2004): Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431: 1092 – 1095.

Lorenzen, S., Prein, M. & Valentin, C. (1987): Mass aggregations of the free-living marine nematode Pontonema vulgare (Oncholaimidae) in organically polluted fjords. Mar. Ecol. Prog. Ser. 37: 27 – 34.

Maggs, C. A., Castilho, R., Foltz, D., Henzler, C., Jolly, M. T., Kelly, J., Olsen, J., Perez, K. E., Stam, W., Vainola, R., Viard, F. & Wares, J. (2008): Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89: S108 – S122.

Magurran, A. E. (2004): Measuring Biological Diversity . Blackwell Science, Oxford.

Magurran, A. E. & McGill, B. J. (2011): Biological Diversity: Frontiers in Measurement and Assessment. Oxford University Press, Oxford.

Mahaut, M. L., Sibuet, M. & Shirayama, Y. (1995): Weight-dependent respiration rates in deep-sea organisms. Deep Sea Research Part I 42: 1575 – 1582.

Mahmoudi, E., Essid, N., Beyrem, H., Hedfi, A., Boufahja, F., Vitiello, P. & Aissa, P. (2007): Individual and combined effects of lead and zinc on a free-living marine nematode community: results from microcosm experiments. J. Exp. Mar. Biol. Ecol. 343: 217 – 226.

Maria, T. F., Esteves, A. M., Vanaverbeke, J. & Vanreusel, A. (2011): The effect of the dominant polychaete Scolelepis squamata on nematode colonisation in sandy beach sediments: an experimental approach. Estuarine Coastal Shelf Sci. 94: 272 – 280.

Maria, T. F., Vanaverbeke, J., Esteves, A. M., De Troch, M. & Vanreusel, A. (2012): The importance of biological interactions for the vertical distribution of nematodes in a temperate ultra-dissipative sandy beach. Estuarine Coastal Shelf Sci. 97: 114 – 126.

McCutchan Jr, J. H., Lewis, W. M., Kendall, C. & McGrath, C. C. (2003): Variation in trophic shift for carbon, nitrogen, and sulfur. Oikos 102: 378 – 390.

McLachlan, A., Erasmus, T. & Furstenberg, J. P. (1977): Migration of sandy beach meiofauna. Afr. Zool. 12:257 – 277.

McNeil, S. & Lawton, J. H. (1970): Annual production and respiration in animal populations. Nature 225: 472 – 474.

Meirmans, P. G. & Hedrick, P. W. (2011): Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11: 5 – 18.

Merckx, B., Goethals, P., Steyaert, M., Vanreusel, A., Vincx, M. & Vanaverbeke, J. (2009): Predictability of marine nematode biodiversity. Ecol. Modell. 220: 1449 – 1458.

Mermillod-Blondin, F., Rosenberg, R., Francois-Carcaillet, F., Norling, K. & Mauclaire, L. (2004): Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. Aquat. Microb. Ecol. 36: 271 – 284.

Meysman, F. J. R., Middelburg, J. J. & Heip, C. H. R. (2006): Bioturbation: a fresh look at Darwin ’ s last idea. Trends Ecol. Evol. 21: 688 – 695.

Middelburg, J. J., Barranguet, C., Boschker, H. T. S., Herman, P. M. J.,Moens, T. & Heip, C. H. R. (2000): The fate of intertidal microphytobenthos carbon: an in situ 13 C labelling study. Limnol. Oceanogr. 45: 1224 – 1234.

Miljutin, D. M., Gad, G., Miljutina, M. A., Mokievsky, V. O., Fons ê ca-Genevois, V. & Esteves, A. M. (2010): The state of knowledge on deep-sea nematode taxonomy: how many valid species are known down there? Mar. Biodivers. 40: 143 – 159.

Miljutin, D. M., Miljutina, M. A., Arbizu, P. M. & Galeron, J. (2011): Deep-sea nematode assemblage has not recovered 26 years after experimental mining of polymetallic nodules (Clarion-Clipperton Fracture Zone, Tropical Eastern Pacific). Deep Sea Res. Part I 58: 885 – 897.

Millward, R. N. & Grant, A. (2000): Pollution-induced tolerance to copper of nematode communities in the severely contaminated Restronguet Creek and adjacent estuaries, Cornwall, United Kingdom. Environ. Toxicol. Chem. 19: 454 – 461.

Mirto, S., La Rosa, T., Gambi, C., Danovaro, R. & Mazzola, A. (2002): Nematode community response to fish-farm impact in the western Mediterranean. Environ. Pollut. 116: 203 – 214.

Moens, T., Vierstraete, A., Vanhove, S., Verbeke, M. & Vincx, M. (1996): A handy method for measuring meiofaunal respiration. J. Exp. Mar. Biol. Ecol. 197: 177 – 190.

Moens, T. & Vincx, M. (1997): Observations on the feeding ecology of estuarine nematodes. J. Mar. Biol. Assoc. U. K. 77: 211 – 227.

Moens, T. (1999): Feeding Ecology of Free-Living Estuarine Nematodes. An Experimental Approach . Ph.D. dissertation. Ghent University, Ghent.

Moens, T., Verbeeck, L., de Maeyer, A., Swings, J. & Vincx, M. (1999a): Selective attraction of marine bacterivorous nematodes to their bacterial food. Mar. Ecol. Prog. Ser. 176: 165 – 178.

Moens, T., Verbeeck, L. & Vincx, M. (1999b): Preservation- and incubation-time induced bias in tracer-aided grazing studies on meiofauna. Mar. Biol. 133: 69 – 77.

Moens, T., Verbeeck, L. & Vincx, M. (1999c): Feeding biology of a predatory and a facultatively predatory nematode ( Enoploides longispiculosus and Adoncholaimus fuscus). Mar. Biol. 134: 585 – 593.

Moens, T. & Vincx, M. (2000a): Temperature and salinity constraints on the life cycle of two brackish-water nematode species. J. Exp. Mar. Biol. Ecol. 243: 115 – 135.

Moens, T. & Vincx, M. (2000b): Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments. J. Exp. Mar. Biol. Ecol. 243: 137 – 154.

Moens, T., Herman, P. M. J., Verbeeck, L., Steyaert, M. & Vincx, M. (2000): Predation rates and prey selectivity in two predacious estuarine nematodes. Mar. Ecol. Prog. Ser. 205: 185 – 193.

Moens, T., Luyten, C., Middelburg, J. J., Herman, P. M. J. & Vincx, M. (2002): Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Mar. Ecol. Prog. Ser. 234: 127 – 137.

Moens, T., Yeates, G. W. & De Ley, P. (2004): Use of carbon and energy sources by nematodes. Nematol. Monogr. Perspect. 2: 529 – 545.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

148   3 Ecology of free-living marine nematodes

Moens, T., Bouillon, S. & Gallucci, F. (2005a): Dual stable isotope abundances unravel trophic position of estuarine nematodes. J. Mar. Biol. Assoc. U. K. 85: 1401 – 1407.

Moens, T., dos Santos, G. A. P., Thompson, F., Swings, J., Fons ê ca-Genevois, V., Vincx, M. & De Mesel, I. (2005b): Do nematode mucus secretions affect bacterial growth? Aquat. Microb. Ecol. 40: 77 – 83.

Moens, T., Bergtold, M. & Traunspurger, W. (2006): Feeding ecology of free-living benthic nematodes. In: Eyualem, A., Andr á ssy, I. & Traunspurger, W. (eds.) Freshwater Nematodes: Ecology and Taxonomy , pp 105 – 131. CABI, Wallingford.

Moens, T., Vafeiadou, A. M., De Geyter, E., Vanormelingen, P., Sabbe, K. & De Troch, M. (2013). Diatom feeding across trophic guilds in tidal flat nematodes, and the importance of diatom cell size. J. Sea Res. In press, available online.

Mokievsky, V. & Azovsky, A. (2002): Re-evaluation of species diversity patterns of free-living marine nematodes. Mar. Ecol. Prog. Ser. 238: 101 – 108.

Mokievsky, V. O., Udalov, A. A. & Azovsky, A. I. (2007): Quantitative distribution of meiobenthos in deep-water zones of the World Ocean. Oceanology 47: 797 – 813.

Montagna, P. A., Coull, B. C., Herring, T. L. & Dudley, B. W. (1983): The relationship between abundances of meiofauna and their suspected microbial food (diatoms and bacteria). Estuarine Coastal Shelf Sci. 17: 381 – 394.

Montagna, P. A. (1984): In situ measurement of meiobenthic grazing rates on sediment bacteria and edaphic diatoms. Mar. Ecol. Prog. Ser. 18: 119 – 130.

Montagna, P. A. (1995): Rates of metazoan meiofaunal microbivory: a review. Vie et Milieu 45: 1 – 9.

Moodley, L., Steyaert, M., Epping, E., Middelburg, J. J., Vincx, M., van Avesaath P., Moens, T. & Soetaert, K. (2008): Respiration rates of benthic meiofauna: a novel oxygen micro-respiration system. J. Exp. Mar. Biol. Ecol. 357: 41 – 47.

Moreno, M., Semprucci, F., Vezzulli, L., Balsamo, M., Fabiano, M. & Albertelli, G. (2011): The use of nematodes in assessing ecological quality status in the Mediterranean coastal systems. Ecol. Indic. 11: 328 – 336.

Musat, N., Giere, O., Gieseke, A., Thiermann, F., Amann, R. & Dubilier, N. (2007): Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environ. Microbiol. 9: 1345 – 1353.

Muthumbi, A. W. & Vincx, M. (1997): Acantholaimus (Chromadoridae: Nematoda) from the Indian Ocean: description of seven species. Hydrobiologia 346: 59 – 76.

Muthumbi, A. W., Vanreusel, A., Duineveld, G., Soetaert, K. & Vincx, M. (2004): Nematode community structure along the continental slope off the Kenyan coast, Western Indian Ocean. Int. Rev. Hydrobiol. 89: 188 – 205.

Nanajkar, M. & Ingole, B. (2010): Impact of sewage disposal on a nematode community of a tropical sandy beach. J. Environ. Biol. 31: 819 – 826.

Nehring, S., Jensen, P. & Lorenzen, S. (1990): Tube-dwelling nematodes: tube construction and possible ecological effects on sediment-water interfaces. Mar. Ecol. Prog. Ser. 64: 123 – 128.

Neira, C., Sellanes, J., Levin, L. A. & Arntz, W. E. (2001): Meiofaunal distributions on the Peru margin: relationships to oxygen and organic matter availability. Deep Sea Res. Part I 48: 2453 – 2472.

Netto, S. A., Attrill, M. J. & Warwick, R. M. (1999): Sublittoral meiofauna and macrofauna of Rocas Atoll (NE, Brazil): indirect evidences of a topographically controlled front. Mar. Ecol. Prog. Ser. 179: 175 – 186.

Netto, S. A., Gallucci, F. & Fonseca, G. (2005): Meiofauna communities of continental slope and deep-sea sites off SE Brazil. Deep Sea Res. Part I 52: 845 – 859.

Netto, R. G., Tognoli, F. M. W., Buatois, L. A. & Mangano, M. G. (2008): Reduction in reservoir potential by cryptobioturbation. A case study in upper paleozoic shallow-marine sandstones (Rio Bonito/Palermo sedimentary succession, Paran á Basin, south Brazil). 2008 Joint Meeting of The Geological Society of America, Soil Science Society of America, American Society of Agronomy, Crop Science Society of America, Gulf Coast Association of Geological Societies with the Gulf Coast Section of SEPM.

Nicholas, W. L. & Hodda, M. (1999): Free-living nematodes of a temperate, high-energy sandy beach: faunal composition and variation over space and time. Hydrobiologia 394: 113 – 127.

Nilsson, P., Sundback, K. & Jonsson, B. (1993): Effect of the brown shrimp Crangon crangon L on endobenthic macrofauna, meiofauna and meiofaunal grazing rates. Neth. J. Sea Res. 31: 95 – 106.

Nygren, A. & Pleijel, F. (2011): From one to ten in a single stroke - resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex. Mol. Phylogenet. Evol. 58: 132 – 141.

Ó lafsson, E., Moore, G. C. & Bett, B. J. (1990): The impact of Melinna palmata Grube, a tube-building polychaete, on meiofaunal community structure in a soft-bottom subtidal habitat. Estuarine Coastal Shelf Sci. 31: 883 – 893.

Ó lafsson, E. & Elmgren, R. (1991): Effects of biological disturbance by benthic amphipods Monoporeia affinis on meiobenthic community structure: a laboratory approach. Mar. Ecol. Prog. Ser. 74: 99 – 107.

Ó lafsson, E. (1992): Small scale spatial distribution of marine meiobenthos: the effects of decaying macrofauna. Oecologia 90: 37 – 42.

Ó lafsson, E., Elmgren, R. & Papakosta, O. (1993): Effects of the deposit-feeding benthic bivalve Macoma balthica on meiobenthos. Oecologia 93: 457 – 462.

Ó lafsson, E. (2003): Do macrofauna structure meiofauna assemblages in marine soft-bottoms? A review of experimental studies. Vie et Milieu 53: 249 – 265.

Ott, J. A. & Schiemer, F. (1973): Respiration and anaerobiosis of free living nematodes from marine and limnic sediments. Neth. J. Sea Res. 7: 233 – 243.

Ott, J., Rieger, G., Rieger, R. & Enderes, F. (1982): New mouthless interstitial worms from the sulfide system: symbiosis with prokaryotes. Mar. Ecol. 3: 313 – 333.

Ott, J., Bright, M. & Bulgheresi, S. (2004): Symbioses between marine nematodes and sulfur-oxidizing chemoautotrophic bacteria. Symbiosis 36: 103 – 126.

Palmer, M. A. (1988): Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implications for recruitment. Mar. Ecol. Prog. Ser. 48: 81 – 91.

Palumbi, S. R. (1994): Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Evol. Syst. 25: 547 – 572.

Patricio, J., Adao, H., Neto, J. M., Alves, A. S., Traunspurger, W. & Marques, J. C. (2012): Do nematodes and macrofauna assemblages provide similar ecological assessment information? Ecol. Indic. 14: 124 – 137.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   149

Pelc, R. A., Warner, R. R. & Gaines, S. D. (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J. Biogeogr. 36: 1881 – 1890.

Petraitis, P. S., Latham, R. E. & Niesenbaum, R. A. (1989): The maintenance of species diversity by disturbance. Q. Rev. Biol. 64: 393 – 418.

Pfenninger, M. & Schwenk, K. (2007): Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol. Biol. 7: 121.

Pranovi, F., Raicevich, S., Franceschini, G., Farrace, M. G. & Giovanardi, O. (2000): Rapido trawling in the northern Adriatic Sea: effects on benthic communities in an experimental area. ICES J. Mar. Sci. 57: 517 – 524.

Prein, M. (1988): Evidence for a scavenging life-style in the free-living nematode Pontonema vulgare (Enoplida: Oncholaimidae). Kieler Meeresforschung Sonderheft 6: 389 – 394.

Puig, P., Canals, M., Company, J. B., Martin, J., Amblas, D., Lastras, G., Palanques, A. & Calafat, A. M. (2012): Ploughing the deep-sea floor. Nature 489: 286 – 290.

Radziejewska, T., Gruszka, P. & Rokicka-Praxmajer, J. (2006): A home away from home: a meiobenthic assemblage in a ship ’ s ballast water tank sediment. Oceanologia 48: 259 – 265.

Reidenauer, J. A. (1989): Sand-dollar Mellita quinquiesperforata (Leske) burrow trails - sites of harpacticoid disturbance and nematode attraction. J. Exp. Mar. Biol. Ecol. 130: 223 – 235.

Reise, K. (1981): High abundance of small zoobenthos around biogenic structures in tidal sediments of the Wadden Sea. Helgol ä nder wissenschaftliche Meeresuntersuchungen 34: 413 – 425.

Reise, K. (1985): Macrofauna promotes meiofauna. Tidal flat ecology. An experimental approach to species interactions. In: Billings, W. D., Golley, F., Lange, O. L., Olson, J. S. & Remmert, H. (eds.) Ecological Studies: Analysis and Synthesis , pp 119 – 145. Springer-Verlag, Berlin.

Reise, K. (2002): Sediment mediated species interactions in coastal waters. J. Sea Res. 48: 127 – 141.

Renaud-Debyser, J. (1963): Recherches é cologiques sur la faune interstitielle des sables. Bassin d ’ Arcachon, î le de Bimini, Bahamas. Vie et Milieu, Supplement 15: 1 – 157.

Rex, M. A., Stuart, C. T. & Etter, R. J. (2001): Do deep-sea nematodes show a positive latitudinal gradient of species diversity? The potential role of depth. Mar. Ecol. Prog. Ser. 210: 297 – 298.

Rex, M. A., Crame, J. A., Stuart, C. T. & Clarke, A. (2005): Large-scale biogeographic patterns in marine molluscs: a confluence of history and productivity? Ecology 86: 2288 – 2297.

Rex, M. A., Etter, R. J., Morris, J. S., Crouse, J., McClain, C. R., Johnson, N. A., Stuart, C. T., Deming, J. W., Thies, R. & Avery, R. (2006): Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Mar. Ecol. Prog. Ser. 317: 1 – 8.

Rice, A. L. & Lambshead, P. J. D. (1994): Patch dynamics in the deep-sea benthos: the role of a heterogeneous supply of organic matter. In: Giller, P. S., Hildrew, A. G. & Raffaelli, D. G. (eds.) Aquatic Ecology: Scale, Pattern and Process. 34 th Symposium of the British Ecological Society , pp 469 – 499. Blackwell Scientific Publications, Oxford.

Riemann, F. & Schrage, M. (1978): The mucus-trap hypothesis on feeding of aquatic nematodes and implications for biodegradation and sediment texture. Oecologia 34: 75 – 88.

Riemann, F., Ernst, W. & Ernst, R. (1990): Acetate uptake from ambient water by the free-living marine nematode Adoncholaimus thalassophygas. Mar. Biol. 104: 453 – 457.

Riera, P. & Hubas, C. (2003): Trophic ecology of nematodes from various microhabitats of the Roscoff Aber Bay (France): importance of stranded macroalgae evidenced through δ 13 C and δ 15 N. Mar. Ecol. Prog. Ser. 260: 151 – 159.

Rogers, S. I., Somerfield, P. J., Schratzberger, M., Warwick, R. M., Maxwell, T. A. D. & Ellis, J. R. (2008): Sampling strategies to evaluate the status of offshore soft sediment assemblages. Mar. Pollut. Bull. 56: 880 – 894.

Romeyn, K. & Bouwman, L. A. (1983): Food selection and consumption by estuarine nematodes. Hydrobiological Bulletin 17: 103 – 109.

Rutledge, P. A. & Fleeger, J. W. (1993): Abudance and seasonality of meifoauna, incuding harpacticoid copepod species, associated to stems of the salt-marsh cord-grass, Spartina alterniflora. Estuaries 16: 760 – 768.

Rysgaard, S., Christensen, P. B., S ø rensen, M. V., Funch, P. & Berg, P. (2000): Marine meiofauna, carbon and nitrogen minera-lization in sandy and soft sediments of Disko Bay, West Greenland. Aquat. Microb. Ecol. 21: 59 – 71.

Rzeznik-Orignac, J., Fichet, D. & Boucher, G. (2003): Spatio-temporal structure of the nematode assemblages of the Brouage mudflat (Marennes-Oleron, France). Estuarine Coastal Shelf Sci. 58: 77 – 88.

Rzeznik-Orignac, J., Boucher, G., Fichet, D. & Richard, P. (2008): Stable isotope analysis of food source and trophic position of intertidal nematodes and copepods. Mar. Ecol. Prog. Ser. 359: 145 – 150.

Sanders, H. L. (1968): Marine benthic diversity: a comparative study. Am. Nat. 102: 243 – 282.

Sanders, H. L. (1969): Benthic marine diversity and the stability-time hypothesis. Brookhaven Symposia in Biology 22: 71 – 80.

Schiemer, F. (1982): Food dependence and energetics of free-living nematodes. I. Respiration, growth and reproduction of Caenorhabditis briggsae (Nematoda) at different levels of food supply. Oecologia 54: 108 – 121.

Schiemer, F. (1985): Bioenergetic niche differentiation of aquatic invertebrates. Verhandlungen der Internationalen Vereinigung f ü r Limnologie 22: 3014 – 3018.

Schiemer, F. (1987): Nematoda. In: Vernberg, J. F. & Pandian, T. J. (eds.) Animal Energetics, Vol. 1, pp 185 – 215. Academic Press, New York.

Schiemer, F., Novak, R. & Ott, J. (1990): Metabolic studies on thiobiotic free-living nematodes and their symbiotic microorganisms. Mar. Biol. 106: 129 – 137.

Schratzberger, M. & Warwick, R. M. (1998a): Effects of physical disturbance on nematode communities in sand and mud: a microcosm experiment. Mar. Biol. 130: 643 – 650.

Schratzberger, M. & Warwick, R. M. (1998b): Effects of the intensity and frequency of organic enrichment on two estuarine nematode communities. Mar. Ecol. Prog. Ser. 164: 83 – 94.

Schratzberger, M. & Warwick, R. M. (1999a): Differential effects of various types of disturbances on the structure of nematode assemblages: an experimental approach. Mar. Ecol. Prog. Ser. 181: 227 – 236.

Schratzberger, M. & Warwick, R. M. (1999b): Impact of predation and sediment disturbance by Carcinus maenas (L.) on free-living nematode community structure. J. Exp. Mar. Biol. Ecol. 235: 255 – 271.

Schratzberger, M., Rees, H. L. & Boyd, S. E. (2000): Effects of simulated deposition of dredged material on structure of nematode assemblages- the role of burial. Mar. Biol. 136: 519 – 530.

Schratzberger, M., Dinmore, T. A. & Jennings, S. (2002a): Impact of trawling on the diversity, biomass and structure of meiofauna assemblages. Mar. Biol. 140: 83 – 93.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

150   3 Ecology of free-living marine nematodes

Schratzberger, M. & Jennings, S. (2002b): Impacts of chronic trawling disturbance on meiofaunal communities. Mar. Biol. 141: 991 – 1000.

Schratzberger, M., Whomersley, P., Warr, K., Bolam, S. G. & Rees, H. L. (2004): Colonisation of various types of sediment by estuarine nematodes via lateral infaunal migration: a laboratory study. Mar. Biol. 145: 69 – 78.

Schratzberger, M., Warr, K. & Rogers, S. I. (2007): Functional diversity of nematode communities in the southwestern North Sea. Mar. Environ. Res. 63: 368 – 389.

Schratzberger, M., Maxwell, T. A. D., Warr, K., Ellis, J. R. & Rogers, S. I. (2008): Spatial variability of infaunal nematode and polychaete assemblages in two muddy subtidal habitats. Mar. Biol. 153: 621 – 642.

Schratzberger, M., Lampadariou, N., Somerfield, P. J., Vandepitte, L. & Vanden Berghe, E. (2009): The impact of seabed disturbance on nematode communities: linking field and laboratory observations. Mar. Biol. 156: 709 – 724.

Schrijvers, J. & Vincx, M. (1997): Cage experiments in an East African mangrove forest: a synthesis. J. Sea Res. 38: 123 – 133.

Selkoe, K. A., Watson, J. R., White, C., Ben Horin, T., Iacchei, M., Mitarai, S., Siegel, D. A,. Gaines, S. D. & Toonen, R. J. (2010): Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol. Ecol. 19: 3708 – 3726.

Slatkin, M. (1993): Isolation by distance in equilibrium and non equilibirum populations. Evolution 47: 264 – 279.

Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K. & Arbizu, P. M. (2008): Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23: 518 – 528.

Smol, N., Huys, R. & Vincx, M. (1991): A 4-years ’ analysis of the meiofauna community of a dumping site for TiO 2 -waste off the Dutch coast. Chem. Ecol. 5: 197 – 215.

Snelgrove, P. V. R. & Smith, C. R. (2002): A riot of species in an environmental calm: the paradox of the species-rich deep-sea floor. Oceanogr. Mar. Biol. Ann. Rev. 40: 322 – 342.

Soetaert, K., Muthumbi, A. W. & Heip, C. (2002): Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns. Mar. Ecol. Prog. Ser. 242: 195 – 204.

Soetaert, K., Franco, M., Lampadariou, N., Muthumbi, A., Steyaert, M., Vandepitte, L., vanden Berghe, E. & Vanaverbeke, J. (2009): Factors affecting nematode biomass, length and width from the shelf to the deep sea. Mar. Ecol. Prog. Ser. 392: 123 – 132.

Soltwedel, T. & Vopel, K. (2001): Bacterial abundance and biomass in response to organism-generated habitat heterogeneity in deep-sea sediments. Mar. Ecol. Prog. Ser. 219: 291 – 298.

Somerfield, P. J. & Clarke, K. R. (1995): Taxonomic levels, in marine communities studies, revisited. Mar. Ecol. Prog. Ser. 127: 113 – 119.

Somerfield, P. J., Rees, H. L. & Warwick, R. M. (1995): Interrelationships in community structure between shallow-water marine meiofauna and macrofauna in relation to dredgings disposal. Mar. Ecol. Prog. Ser. 127: 103 – 112.

Somerfield, P. J., Fons ê ca-Genevois, V. G., Rodrigues, A. C. L., Castro, F. J. V. & dos Santos, G. A. P. (2003): Factors affecting meiofaunal community structure in the Pina Basin, an urbanized embayment on the coast of Pernambuco, Brazil. J. Mar. Biol. Assoc. U. K. 83: 1209 – 1213.

Somerfield, P., Warwick, R. M. & Moens, T. (2005): Meiofauna techniques. In: Eleftheriou, A. & McIntyre, A. (eds.) Methods

for the Study of Marine Benthos, Third edition , pp. 229 – 272. Blackwell Science, Oxford.

Sommer, S. & Pfannkuche, O. (2000): Metazoan meiofauna of the deep Arabian Sea: standing stocks, size spectra and regional variability in relation to monsoon induced enhanced sedimentation regimes of particulate organic matter. Deep Sea Res. Part II 47: 2957 – 2977.

Stevens, G. C. (1989): The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am. Nat. 133: 240 – 256.

Steyaert, M., Garner, N., van Gansbeke, D. & Vincx, M. (1999): Nematode communities from the North Sea: environmental controls on species diversity and vertical distribution within the sediment. J. Mar. Biol. Assoc. U. K. 79: 253 – 264.

Steyaert, M., Herman, P. M. J., Moens, T., Widdows, J. & Vincx, M. (2001): Tidal migration of nematodes on an estuarine tidal flat (the Molenplaat, Schelde estuary, SW Netherlands). Mar. Ecol. Prog. Ser. 224: 299 – 304.

Steyaert, M., Vanaverbeke, J., Vanreusel, A., Barranguet, C., Lucas, M. & Vincx, M. (2003): The importance of fine-scale, vertical profiles in characterizing nematode community structure. Estuarine Coastal Shelf Sci. 58: 353 – 366.

Steyaert, M., Moodley, L., Vanaverbeke, J., Vandewiele, S. & Vincx, M. (2005): Laboratory experiments on the infaunal activity of intertidal nematodes. Hydrobiologia 540: 217 – 223.

Steyaert, M., Moodley, L., Nadong, T., Moens, T., Soetaert, K. & Vincx, M. (2007): Responses of intertidal nematodes to short-term anoxic events. J. Exp. Mar. Biol. Ecol. 345: 175 – 184.

Sudhaus, W. (1974): Nematoden (insbesondere Rhabditiden) des Strandanwurfs und ihre Beziehungen zu Krebsen. Faunistisch Ö kologische Mitteilungen 4: 365 – 400.

Sudhaus, W. & Kiontke, K. (2007): Comparison of the cryptic nematode species Caenorhabditis brenneri sp. n. and C. remanei (Nematoda : Rhabditidae) with the stem species pattern of the Caenorhabditis elegans group. Zootaxa 1456: 45 – 62.

Svensson, J. R., Lindegarth, M., Siccha, M., Lenz, M., Molis, M., Wahl, M. & Pavia, H. (2012): Maximum species richness at intermediate frequencies of disturbance: consistency among levels of productivity. Ecology 88: 830 – 838.

Tchesunov, A. V., Ingels, J. & Popova, E. V. (2012): Marine free-living nematodes associated with symbiotic bacteria in deep-sea canyons of north-east Atlantic Ocean. J. Mar. Biol. Assoc. U. K. 92: 1257 – 1271.

Teske, P. R., McQuaid, C. D., Froneman, P. W. & Barker, N. P. (2006): Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar. Ecol. Prog. Ser. 314: 283 – 293.

Thiel, M. & Gutow, L. (2005): The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr. Mar. Biol. 43: 279 – 418.

Thiermann, F., Vismann, B. & Giere, O. (2000): Sulphide tolerance of the marine nematode Oncholaimus campylocercoides – a result of internal sulphur formation? Mar. Ecol. Prog. Ser. 193: 251 – 259.

Thistle, D. & Eckman, J. E. (1990): The effect of a biologically produced structure on the benthic copepods of a deep-sea site. Deep Sea Res. Part A 37: 541 – 554.

Thistle, D. (2003): The deep-sea floor: an overview. In: Ecosystems of the World, Vol. 28 , pp. 5 – 37. Elsevier, Amsterdam.

Thomas, M. C. & Lana, P. C. (2011): A new look into the small-scale dispersal of free-living marine nematodes. Zoologia 28: 449 – 456.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

Literature   151

Tita, G., Vincx, M. & Desrosiers, G. (1999): Size spectra, body width and morphotypes of intertidal nematodes: an ecological interpretation. J. Mar. Biol. Assoc. U. K. 79: 1007 – 1015.

Tita, G., Desrosiers, G., Vincx, M. & Nozais, C. (2000): Predation and sediment disturbance effects of the intertidal polychaete Nereis virens (Sars) on associated meiofaunal assemblages. J. Exp. Mar. Biol. Ecol. 243: 261–282.

Traunspurger, W. (1997): Bathymetric, seasonal and vertical distribution of feeding-types of nematodes in an oligotrophic lake. Vie et Milieu 47: 1 – 7.

Traunspurger, W., Bergtold, M. & Goedkoop, W. (1997): The effects of nematodes on bacterial activity and abundance in a freshwater sediment. Oecologia 112: 118 – 122.

Trotter, D. B. & Webster, J. M. (1984): Feeding preferences and seasonality of free-living marine nematodes inhabiting the kelp Macrocystis integrifolia. Mar. Ecol. Prog. Ser. 14: 151 – 157.

Udalov, A., Azovsky, A. & Mokievsky, V. (2005): Depth-related pattern in nematode size: What does the depth itself really mean? Prog. Oceanogr. 67: 1 – 23.

Ullberg, J. & Olafsson, E. (2003): Free-living marine nematodes actively choose habitat when descending from the water column. Mar. Ecol. Prog. Ser. 260: 141 – 149.

Underwood, A. J. (1994): On beyond BACI- sampling designs that might reliably detect environmental disturbances. Ecol. Appl. 4: 3 – 15.

Underwood, A. J. (1996): Detection, interpretation, prediction and management of environmental disturbances: some roles for experimental marine ecology. J. Exp. Mar. Biol. Ecol. 200: 1 – 27.

Underwood, A. J. (1997): Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge: Cambridge University Press.

Urban-Malinga, B. & Moens, T. (2006): Fate of organic matter in Arctic intertidal sediments: is utilisation by meiofauna important? J. Sea Res. 56: 239 – 248.

Van Colen, C., Montserrat, F., Verbist, K., Vincx, M., Steyaert, M., Vanaverbeke, J., Herman, P. M. J., Degraer, S. & Ysebaert, T. (2009): Tidal flat nematode responses to hypoxia and subsequent macrofauna-mediated alterations of sediment properties. Mar. Ecol. Prog. Ser. 381: 189 – 197.

Van der Meer, J., Heip, C. H. R., Herman, P. M. J., Moens, T. & Van Oevelen, D. (2005): Flow of energy and matter in marine benthic animal populations. In: Eleftheriou, A. & McIntyre, A. (eds.) Methods for the study of marine benthos, Third edition , pp. 326 – 408. Blackwell Science, Oxford.

Vander Zanden, M. J. & Rasmussen, J. B. (2001): Variations in δ 15 N and δ 13 C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 46: 2061 – 2066.

Van Gaever, S., Moodley, L., de Beer, D. & Vanreusel, A. (2006): Meiobenthos of the Arctic H å kon Musby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments. Mar. Ecol. Prog. Ser. 321: 143 – 155.

Van Gaever, S., Gal é ron, J., Sibuet, M. & Vanreusel, A. (2009): Deep-sea habitat heterogeneity on meiofaunal communities in the Gulf of Guinea. Deep Sea Res. Part I 56: 2259 – 2269.

Van Gaever, S., Raes, M., Pasotti, F. & Vanreusel, A. (2010): Spatial scale and habitat-dependent diversity patterns in nematode communities in three seepage related sites along the Norwegian Sea margin. Mar. Ecol. 31: 66 – 77.

Vanaverbeke, J., Arbizu, P. M., Dahms, H. U. & Schminke, H. K. (1997): The metazoan meiobenthos along a depth gradient

in the Arctic Laptev Sea with special attention to nematode communities. Polar Biol. 18: 391 – 401.

Vanaverbeke, J., Steyaert, M., Vanreusel, A. & Vincx, M. (2003): Nematode biomass spectra as descriptors of functional changes due to human and natural impact. Mar. Ecol. Prog. Ser. 249: 157 – 170.

Vanaverbeke, J., Steyaert, M., Soetaert, K., Rousseau, V., Van Gansbeke, D., Parent, J. Y. & Vincx, M. (2004): Changes in structural and functional diversity of nematode communities during a spring phytoplankton bloom in the southern North Sea. J. Sea Res. 52: 281 – 292.

Vanaverbeke, J., Merckx, B., Degraer, S. & Vincx, M. (2011): Sediment-related distribution patterns of nematodes and macrofauna: two sides of the benthic coin? Mar. Environ. Res. 71: 31 – 40.

Vanhove, S., Arntz, W. & Vincx, M. (1999): Comparative study of the nematode communities on the southeastern Weddell Sea shelf and slope (Antarctica). Mar. Ecol. Prog. Ser. 181: 237 – 256.

Van Oevelen, D., Soetaert, K., Middelburg, J. J., Herman, P. M. J., Moodley, L., Hamels, I., Moens, T. & Heip, C. (2006): Quantifying intertidal food webs, using biomass, tracer and carbon isotope data. J. Mar. Res. 64: 453 – 482.

Vanreusel, A., Vincx, M., Bett, B. J. & Rice, A. L. (1995): Nematode biomass spectra at two abyssal sites in the NE Atlantic with contrasting food-supply. Int. Rev. Der Gesamten Hydrobiol. 80: 287 – 296.

Vanreusel, A., Clough, L., Jacobsen, K., Ambrose, W., Jutamas, J., Ryheul, V., Herman, R. & Vincx, M. (2000): Meiobenthos of the central Arctic Ocean with special emphasis on the nematode community structure. Deep Sea Res. Part I 47: 1855 – 1879.

Vanreusel, A., De Groote, A., Gollner, S. & Bright, M. (2010a): Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review. PLoS One 5: e12449.

Vanreusel, A., Fonseca, G., Danovaro, R & 29 others. (2010b): The contribution of deep-sea macrohabitat heterogeneity to global nematode diversity. Mar. Ecol. 31: 6 – 20.

Varon, R. & Thistle, D. (1988): Response of a harpacticoid copepod to a small-scale natural disturbance. J. Exp. Mar. Biol. Ecol . 118: 245 – 256.

Vermeeren, H., Vanreusel, A. & Vanhove, S. (2004): Species distributions within the free-living marine nematode genus Dichromadora in the Weddell Sea and adjacent areas. Deep Sea Res. Part II 51: 1643 – 1664.

Villano, N. & Warwick, R. M. (1995): Meiobenthic communities associated with the seasonal cycle of growth and decay of Ulva rigida Agardh in the Palude Della Rosa, lagoon of Venice. Estuarine Coastal Shelf Sci . 41: 181 – 194.

Vincx, M. (1989): Free-living marine nematodes from the southern bight of the North Sea. Academiae Analecta, Klasse Wetenschappen 51: 39 – 70.

Vincx, M., Bett, B., Dinet, A., Ferrero, T., Gooday, A., Lambshead, P., Pfannkuche, O., Soltwedel, T. & Vanreusel, A. (1993): Meiobenthos of the deep Northeast Atlantic. Adv. Mar. Biol. 30: 1 – 8.

Vopel, K. & Thiel, H. (2001): Abyssal nematode assemblages in physically disturbed and adjacent sites of the eastern equatorial Pacific. Deep Sea Res. II 48: 3795 – 3808.

Vranken, G. & Heip, C. (1983): Calculation of the intrinsic rate of natural increase, Rm, with Rhabditis marina Bastian 1865 (Nematoda). Nematologica 29: 468 – 477.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM

152   3 Ecology of free-living marine nematodes

Vranken, G. & Heip, C. (1986a): Toxicity of copper, mercury and lead to a marine nematode. Mar. Pollut. Bull. 17: 453 – 457.

Vranken, G. & Heip, C. (1986b): The productivity of marine nematodes. Ophelia 26: 429 – 442.

Vranken, G., Herman, P. M. J., Vincx, M. & Heip, C. (1986): A re-evaluation of marine nematode productivity. Hydrobiologia 135: 193 – 196.

Vranken, G., Herman, P. M. J. & Heip, C. (1988): Studies of the life-history and energetics of marine and brackish-water nematodes. I. Demography of Monhystera disjuncta at different temperature and feeding conditions. Oecologia 77: 296 – 301.

Vranken, G., Vanderhaeghen, R. & Heip, C. (1991): Effects of pollutants on life-history parameters of the marine nematode Monhystera disjuncta. ICES J. Mar. Sci. 48: 325 – 334.

Walker, B. H. (1992): Biodiversity and ecological redundancy. Conserv. Biol. 6: 18 – 23.

Ward, A. R. (1975): Studies on the sublittoral free-living nematodes of Liverpool Bay. II. Influence of sediment composition on the distribution of marine nematodes. Mar. Biol. 30: 217 – 225.

Wares J. P., Gaines S.D. & Cunningham, C.W. (2001): A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55: 295 – 306.

Warwick, R. M. (1984): Species size distributions in marine benthic ecology. Oecologia 61: 32 – 41.

Warwick, R. M. & Gee, J. M. (1984): Community structure of estuarine meiobenthos. Mar. Ecol. Prog. Ser. 18: 97 – 111.

Warwick, R. M., Gee, J. M., Berge, J. A. & Ambrose, W. (1986): Effects of the feeding activity of the polychaete Streblosoma bairdi (Malmgren) on meiofaunal abundance and community structure. Sarsia 71: 11 – 16.

Warwick, R. M. (1988): The level of taxonomic discrimination required to detect pollution effects on marine benthic communities. Mar. Pollut. Bull. 19: 259 – 268.

Warwick, R. M., McEvoy, A. J. & Thrush, S. F. (1997): The influence of Atrina zelandica Gray on meiobenthic nematode diversity and community structure. J. Exp. Mar. Biol. Ecol. 214: 231 – 247.

Warwick, R. M. & Clarke, K. R. (1998): Taxonomic distinctness and environmental assessment. J. Appl. Ecol. 35: 532 – 543.

Warwick, R. M., Platt, H. M. & Somerfield, P. J. (1998): Free Living Marine Nematodes. Part III. Monhysterids. Synopses of the British fauna, First edition . Cambridge: Cambridge University Press.

Warwick, R. M. & Robinson, J. (2000): Sibling species in the marine pollution indicator genus Pontonema leidy (Nematoda: Oncholaimidae), with description of P. mediterranea sp. nov. J. Nat. Hist. 34: 641 – 662.

Warwick, R. M. & Clarke, K. R. (2001): Practical measures of marine biodiversity based on relatedness of species. Oceanogr. Mar. Biol. 39: 207 – 231.

Waters, T. F. (1969): The turnover ratio in production ecology of freshwater invertebrates. Am. Nat. 103: 173 – 185.

Watling, L. & Norse, E. A. (1998): Disturbance of the seabed by mobile fishing gear: a comparison to forest clearcutting. Conserv. Biol. 12: 1180 – 197.

Wei C.L., Rowe, G.T., Escobar-Briones, E., Boetius, A., Soltwedel, T., Caley, M. J., Soliman, Y., Huettmann, F., Qu, F. & Yu, Z. (2010): Global patterns and predictions of seafloor biomass using random forests. PLoS One 5: e15323.

Westheide, W. & Hass-Cordes, E. (2001): Molecular taxonomy: description of a cryptic Petitia species (Polychaeta : Syllidae) from the island of Mahe (Seychelles, Indian Ocean) using RAPD markers and ITS2 sequences. J. Zool. Sys. Evol. Res. 39: 103 – 111.

Wetzel, M., Jensen, P. & Giere, O. (1995): Oxygen/sulfide regime and nematode fauna associated with Arenicola marina burrows: new insights in the thiobios case. Mar. Biol. 124: 301 – 312.

Wetzel, M. A., Weber, A. & Giere, O. (2002): Re-colonization of anoxic/sulfidic sediments by marine nematodes after experimental removal of macroalgal cover. Mar. Biol. 141: 679 – 689.

White, P. S. & Pickett, S. T. A. (1985): Natural disturbance and patch dynamics: an introduction. In: Pickett, S. T. A. & White, P. S. (eds.) The Ecology of Natural Disturbance and Patch Dynamics , pp. 3 – 13. Academic Press, Orlando.

Whomersley, P., Huxham, M., Schratzberger, M. & Bolam, S. (2009): Differential response of meio- and macrofauna to in situ burial. J. Mar. Biol. Assoc. U. K. 89: 1091 – 1098.

Wieser, W. (1953): Die Beziehung zwischen Mundh ö hlengestalt, Ern ä hrungsweise und Vorkommen bei freilebenden marinen Nematoden. Arkiv f ü r Zoologie 4: 439 – 484.

Wieser, W. (1960): Benthic studies in Buzzards Bay. 2. The meiofauna. Limnol. Oceanogr. 5: 121 – 137.

Wright, S. (1951): The genetical structure of populations. Ann. Eugenic s 15: 323 – 354.

Yeates, G. W., Bongers, T., De Goede, R. G. M., Freckman, D. W. & Georgieva, S. S. (1993): Feeding habits in soil nematode families and genera — An outline for soil ecologists. J. Nematol. 25: 315 – 331.

Z ü hlke, R., Blome, D., van Bernem, K. H. & Dittmann, S. (1998): Effects of the tube-building polychaete Lanice conchilega (Pallas) on benthic macrofauna and nematodes in an ina Maritima 29:131 – 138.

Brought to you by | Universidade Federal de São Paulo UNIFESPAuthenticated | gfonseca@unifesp.br

Download Date | 2/24/14 7:02 PM