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Meiofauna matters: The roles of meiofauna in

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Journal of Experimental Marine Biology and Ecology

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Meiofauna matters: The roles of meiofauna in benthic ecosystems

Michaela Schratzberger a,⁎, Jeroen Ingels b,c
a
Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft NR33 0HT, UK
b
Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, UK
c
Florida State University Coastal and Marine Laboratory, 3618 Coastal Highway 98, St Teresa, 32358, Florida, USA

a r t i c l e i n f o a b s t r a c t

Article history: Sedimentary habitats cover most of the ocean bottom and therefore constitute the largest single ecosystem on
Received 31 August 2016 Earth in spatial coverage. The benthic ecosystem contributes to human well-being by providing essential services
Received in revised form 15 December 2016 such as food production and nutrient cycling. Although meiofauna are well-recognised as an abundant and
Accepted 13 January 2017
ubiquitous component of benthic communities, empirical evidence of their wider role in marine ecosystems is
Available online xxxx
scattered across the literature. Some ecologists and decision-makers thus remain sceptical about what meiofauna
Keywords:
can tell them about the provision of ecosystem services. This article investigates empirical evidence on the roles
Meiofauna of meiofauna in benthic ecosystems using a conceptual model that links the supply of an ecosystem service, the
Sediments ecosystem processes that contribute to that service (e.g. production, consumption and decomposition of
Ecosystem processes organic matter, nutrient regeneration, and energy transfer to higher trophic levels) and the meiofaunal activities
Ecosystem services (e.g. bioturbation and feeding) that regulate these processes. Meiofauna activities modify a series of physical,
Species interactions chemical and biological sediment properties. They often do so simultaneously by, for example, displacing
Biodiversity sediment grains during burrow construction and displacing organic matter and microorganisms within the
sediment matrix during feeding. These modifications directly and indirectly, positively and negatively affect
various ecosystem services including sediment stabilisation, biochemical cycling, waste removal and food web
dynamics, at various spatial and temporal scales. Meiofauna can mediate ecosystem processes in sediments
with little or no macrofauna, thereby increasing the resilience of those benthic ecosystem processes that are
essential for the continued delivery of ecosystem services desired by society. This is of growing importance
since benthic ecosystems are under increasing anthropogenic pressure. Whilst studies over the past five decades
have emphasised the important roles meiofauna play in benthic ecosystems, future studies will need to
determine how consistent and widespread these roles are.
Crown Copyright © 2017 Published by Elsevier B.V. All rights reserved.

1. Looking closer at a miniature world
Marine sediments are, by surface, the largest habitat on Earth. A
wide diversity of organisms inhabits these sediments that by their
actions mediate many ecosystem processes (Snelgrove, 1997, 1999).
Several of these processes, such as the reworking of sediments, the
recycling of nutrients, food web dynamics, the degradation and distri-
bution of pollutants, and the decomposition, mineralisation, burial and
storage of organic matter are important on a global scale and are essen-
tial to sustain life on Earth. These processes are maintained and shaped
by intra- and interspecific interactions as well as the interplay between
organisms and their physical and chemical environment (Giere, 2009).
Society obtains great benefits from benthic ecosystems in the form
of provisioning (e.g. food, biotic materials and biofuels), regulating
and maintenance (e.g. nutrient cycling and waste processing), and
enriching (e.g. recreation and tourism) services, all of which are
⁎ Corresponding author.
E-mail address: michaela.schratzberger@cefas.co.uk (M. Schratzberger).
provided on multiple scales and at no charge to society. The protection
of ecosystem services (i.e. the direct and indirect contributions of eco-
systems to human well-being) forms an important part of current envi-
ronmental management practice, designed to ensure ecosystem
services are conserved for human benefit (TEEB, 2010). Ecosystem ser-
vices are ecological in nature and are delivered by the living compo-
nents of the ecosystem (Boyd and Banzhaf, 2007). The number and
composition of species influence ecosystem processes in concert with
the effects of climate and disturbance regimes. Human activities can
modify these factors. It is now widely acknowledged that degradation
of marine sediments which harbour the organisms essential to benthic
ecosystem processes will in turn degrade a range of ecosystem services
(Hooper et al., 2005).
Although ecosystem services are properties of whole ecosystems or
communities, the processes that support them often depend on partic-
ular populations, species, species guilds or habitat types (Prather et al.,
2013). Of the studies that have explicitly tested the effects of species
on benthic ecosystem processes, relatively few have attempted to rec-
oncile the role of those species which, for the most part, are invisible

http://dx.doi.org/10.1016/j.jembe.2017.01.007
0022-0981/Crown Copyright © 2017 Published by Elsevier B.V. All rights reserved.

Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
2 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx

to the naked eye, yet which are crucial elements of the biosphere how meiobenthologists can feed relevant information into
(Sheppard, 2006; Schratzberger, 2012). Meiofauna, a discrete group of decision-making.
small-sized organisms (b1 mm) whose morphology, physiology and
life history characteristics have evolved to exploit a range of terrestrial
Findings are synthesised in a systematic way, using a simple concep-
and aquatic environments, occur in often high abundance and diversity
tual framework that links natural systems with socio-economic systems
in soils and sediments worldwide. They are the most phyletically
via the flow of ecosystem services (adapted from Haines-Young and
diverse fauna on Earth. Some meiofauna species are ancestrally minia-
Potschin, 2010; Liquete et al., 2013; Maes et al., 2016). This is the first at-
ture and were most likely involved in the earliest stages of the diversifi-
tempt that places meiofauna contributions to ecosystem processes into
cation of metazoan life. Others have secondarily evolved miniature
a socio-economic ecosystem services framework. The flow of ecosystem
morphologies from macroscopic ancestors (Rundell and Leander,
services may be translated into specific societal benefits and values
2010; Laumer et al., 2015). The microscopic size reflects the evolution-
(Fig. 1). Whether a particular process is regarded as a service or not
ary benefit these organisms have that enables them to survive and
depends upon whether it is considered as a benefit (De Groot et al.,
thrive in interstitial space. Conversely, the larger macrofauna more
2010). Society will value a particular process differently in different
often exhibit a lifestyle whereby they rely on sediment displacement
places at different times. Therefore, all fundamental ecosystem process-
or burrowing. The highly conservative bimodal body size pattern within
es that operate within benthic ecosystems (including processes that
the benthos is postulated to result from the evolutionary optimisation of
humans find useful) are included here to determine the role of
functional traits such as body size, with intermediate traits being either
meiofaunal organisms within those systems (Jax, 2005). The adapted
impossible or non-viable. Body size bimodalism may, however, be mod-
model in Fig. 1 distinguishes between the supply of an ecosystem ser-
ified by local ecological constraints and disturbances (Warwick, 2014).
vice (e.g. sediment stability and nutrient cycling), the ecosystem pro-
There is considerable debate as to whether high meiofauna abun-
cesses that contribute to that service (e.g. a range of sedimentary,
dance and diversity translate into a significant effect on ecosystem pro-
trophic and ecological processes) and the meiofaunal activities (e.g. bio-
cesses. Meiofauna biomass is low compared to other benthic
turbation and feeding) that regulate these processes (De Groot, 2006).
components and meiofaunal contributions to ecosystem processes will
By virtue of their dominance in marine sediments, universality and
therefore be, at least partially, dependent on their biomass turn-over
robust bodies, nematodes and harpacticoid copepods are the most fre-
and activity (Moens et al., 2013). This article investigates empirical evi-
quently studied components of the meiofauna. Various taxonomic
dence on the roles of meiofauna in benthic ecosystem processes and in
keys for the identification of nematode and harpacticoid copepods
particular those processes that underpin ecosystem services. The prima-
have been published, further stimulating interest in these two groups
ry motivation is to define the current state of scientific knowledge, to
(Schratzberger et al., 2000). Consequently, the great majority of
provide useful information for scientists and environmental managers,
meiofauna articles published in the peer-reviewed scientific literature
and to identify critical gaps to be filled by future research. To that aim,
to date deals with either nematodes or harpacticoid copepods which
the following questions are addressed:
adds inevitable bias to this review.
1) What is the contribution of meiofauna to fundamental ecosystem
processes that operate within benthic ecosystems? This question 2. Biological activities of meiofauna and their effects on benthic eco-
focuses on how ecosystem processes are affected by the presence systems - a pre-21st century perspective
of meiofauna in order to clarify their trophic position and roles in
benthic ecosystems. Meiofauna carry out a range of biological activities. These include
moving through or along the sediment (Cullen, 1973), active sediment
particle reworking as a result of burrowing, construction and mainte-
2) How do meiofauna-mediated effects on sedimentary, trophic and nance of burrows and ingestion and defecation of particles (bioturba-
ecological processes modulate the delivery of ecosystem services? tion sensu Kristensen et al., 2012), and excretion of metabolic wastes.
The focus here lies on how meiofaunal activities (e.g. bioturbation Meiofauna, and nematodes in particular, produce sticky mucus which
and feeding) regulate those ecosystem processes that underpin out- serves for attachment to the sediment for eggs and to stabilise burrows
comes that humans find useful. (Riemann and Schrage, 1978). Reviews published between 1970 and
2000 suggest that these activities are pivotal in shaping benthic ecosys-
tems in shallow-water and deep sea environments.
3) How can scientists best incorporate what is known about the roles of Many meiobenthic species construct microscale burrows in sandy
meiofauna in benthic ecosystems into evidence supporting environ- and muddy sediments where the sediment particles are bound together
mental management and policy? This includes some suggestions of by extracellular polymeric substances (EPS) secreted by the organisms

Fig. 1. Conceptual model linking the supply of an ecosystem service (e.g. sediment stability, nutrient cycling), the ecosystem processes that contribute to that service (e.g. sedimentary,
trophic and ecological processes) and the meiofaunal activities (e.g. bioturbation and feeding) that regulate those processes (adapted from Haines-Young and Potschin, 2010; Liquete
et al., 2013; Maes et al., 2016).

Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
themselves (Chandler and Fleeger, 1984; Nehring et al., 1990; Reichelt,
1991; Nehring, 1993). Some of the binding material is expected to have
major impacts on the stability and erodibility of the surficial sediment
layers. By bioturbating sediments or by generating bioconstructions,
meiofauna is thought to act as vertical conveyors within sediments
and between the sediments and overlying water (Coull, 1999), thereby
modifying hydrodynamics in sediments and affecting nutrient cycling
and biogeochemical fluxes, and changing vertical chemical gradients
in the sediment. Experiments by Aller and Aller (1992), for example,
showed that natural populations of meiofauna can alter sediment
porosity and double solute transport in muds compared to uninhabited
sediments.
Evidence arising from earlier reviews also highlights the potentially
important role of meiofauna in marine food webs, by affecting the struc-
ture and activity of microbial communities and by connecting primary
production and the decomposition of organic matter to higher trophic
levels (Coull, 1999). As meiofauna feed, they remove microbes, diatoms
and other protozoans from the sediment. Meiofauna is capable of eating
its body weight equivalent in microorganisms each day and this grazing
pressure can represent a significant stimulatory effect on the microbial
community (Montagna, 1984; Heip et al., 1985). Meiofauna also stimu-
lates bacterial growth by mechanically breaking down detrital particles
and causing them to be more susceptible to increased bacterial action,
by directly excreting nutrients for microbial use, and by producing
mucus that attracts and sustains microbial growth (Coull, 1973, 1999).
Meiofauna were reported to utilise food resources that are produced
in the pelagic zone, either directly by feeding on sedimented algal cells,
or indirectly by feeding on decomposing organic matter with associated
bacteria (Heip et al., 1985). Studies addressing the utilisation of detritus
by meiofauna consistently reported that the mineralisation of organic
matter is enhanced in the presence of meiofauna (Coull, 1999). The
mineralisation of detritus is largely a microbial process and meiofauna
themselves account for only a small proportion of this mineralisation
directly. The impact of meiofauna grazing on bacteria has been postulat-
ed to exert a major indirect effect on mineralisation rates in the benthos
(Heip et al., 1985; Coull, 1999), as does meiofaunal stimulation of oxy-
gen and nutrient fluxes. Alkemade et al. (1992), for example, demon-
strated that bioturbation by nematodes and the associated increase in
oxygen availability stimulated microbial activity, and led to a 30%
increase in decomposition rates of saltmarsh grass (Spartina anglica)
in tidal sediments in the southern North Sea. Although some meiofaunal
groups were assumed to have close trophic links to microbial communi-
ties (Coull, 1973; Gerlach, 1978; Kuipers et al., 1981), empirical studies
evaluating the precise effects of meiofauna-microbe interactions on
benthic ecosystems remained poorly understood and quantified.
By the 1990s, numerous field and laboratory experiments had ap-
peared in the scientific literature, investigating the transfer of energy
directly between meiofauna and higher trophic levels and in particular
fish (Gee, 1989; Coull, 1990) but also some shore birds (Gaston, 1992;
Sutherland et al., 2000). Most of the evidence was qualitative in nature,
simply indicating that meiofauna form some part of the diet of preda-
tors. Copepods numerically dominate the guts of most meiofaunal pred-
ators although they do often not dominate numerically in situ.
However, rapid digestion of soft-bodied meiofaunal prey such as nema-
todes (as opposed to hard-bodied meiofauna, e.g. copepods with exo-
skeletons) may lead to substantial underestimates of the importance
of meiofaunal prey in juvenile fish (Scholz et al., 1991). In addition to
differential digestion, prey availability (i.e. vertical distribution in the
sediment) and movement have also been postulated, and subsequently
been proven, to contribute to the dominance of copepods in the gut of
meiofaunal predators (McCall and Fleeger, 1995).
It soon became clear that predators feed on meiofauna, some exclu-
sively. When feeding in estuarine habitats, particularly in eelgrass
meadows and mudflats, some juvenile fish prey extensively on only a
few species of harpacticoid copepods, whilst others rely on biofilms
and associated meiofauna grazers (Carpentier et al., 2014). Schückel
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
3
et al. (2013), for example, later reported that diets of solenette and
goby were dominated by meiofaunal prey in the southern North Sea
throughout the year. Scaldfish and dab were only partly reliant on
meiofauna, with the notion that harpacticoid copepod prey densities
decreased with increasing fish size, attesting to the important role of
meiofauna in juvenile fish diets. These authors also showed that fish
predation on harpacticoid copepods can be species-selective despite
multiple copepod species co-existing in high densities (Schückel et al.,
2013). Fish growth and survival to the adult stage depend upon this
early life-history period (Levy and Northcote, 1982) and the absence
of meiofauna would prevent or slow recruitment to fishable stocks. To
these predators, meiofauna thus provide a short-term but compelling
energetic benefit.
Ecological theory would suggest a nutritional advantage in such
feeding behaviour and implies feeding adaptations exist given these
niche developments. In the field, predators have little impact on
meiofauna prey populations. Meiofaunal prey populations tend to be
large and the predatory removal relatively small. Thus, predation is
unlikely to drastically reduce prey populations. Additionally, many
meiofauna have life-history characteristics (e.g. fast turn-over times)
that allow rapid replenishment of the prey population (Coull, 1999).
Estimates of energy flow through the benthic ecosystem followed,
investigating both the grazing pressure of meiofauna on lower trophic
levels and the amount of energy and material made available to higher
trophic levels. Initially, such studies focused on descriptions of standing
stocks and transfer rates between ecosystem components. Whilst some
quantitative understanding of the role of larger-sized benthos in energy
flow was obtained, little attention had been given to meiofauna. The
direct estimation of energy flow through meiobenthic populations
poses several difficulties, mainly relating to sampling problems (i.e. dif-
ficulty of measuring respiration in the field and calculating biomass pro-
duction from an analysis of growth and mortality; Herman et al., 1984).
Hence, most knowledge was initially based on density and biomass of
field populations (Warwick and Price, 1979; Warwick, 1982; Vranken
and Heip, 1986), occasionally combined with modelling approaches
(Kennedy, 1984). Despite considerable variability amongst studies,
agreement was reached that meiofaunal throughput of carbon can be
orders of magnitude higher than its standing stock. In addition, several
studies postulated that production rates (often expressed as
production:biomass ratios) for meiofauna exceeded those of macrofau-
na (Schwinghamer et al., 1986; Warwick et al., 1979; Warwick and
Price, 1979). Hence, the production and flow of energy, rather than its
storage, appeared to be the domain of meiofauna (Giere, 2009). This
paradigm is supported by the fact that some meiofauna are recognised
to harness chemical energy through feeding on chemosynthetic symbi-
otic and/or mutualistic bacteria which can be intracellular or extracellu-
lar, and intra- or extra-corporal. For example, bacterial ecto- and
endosymbionts of meiofauna from several deep and shallow seeps
around the world can be either a source and pathway of
chemosynthetically derived organic matter entering higher trophic
levels or play a role in detoxification in meiofauna inhabiting
sulphide-rich sediments (Levin, 2005). Moreover, predatory and scav-
enging meiofauna preying on or consuming meiofaunal organisms
(Kennedy, 1994), suggest potential carbon recycling within the
meiofauna compartment and increased transfer of low-trophic level
carbon to higher trophic levels, highlighting the role of meiofauna in
energy transfer in benthic ecosystems.
3. Leaps forward in understanding - recent efforts in describing the
often catalytic roles of meiofauna in benthic ecosystems
By the turn of the century, an increasing body of literature had
established that numerous links exist between meiofauna and the
microbiota that, with their enormous metabolic and productive poten-
tial, affect a range of ecosystem processes directly. At the same time
several, mostly experimental, studies provided evidence of the close
4 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
relationship with the macrobiota that hold an important and well-
recognised position as consumer and disturber. Macrofauna-
meiofauna relationships are discussed in more detail in Section 4.3.
Recently, meiofauna research has undergone a revolution as molec-
ular tools have been developed to establish the trophic position and
roles of meiofauna in benthic ecosystems. Metagenomics sequencing
(Bik et al., 2012), barcoding techniques (Bhadury et al., 2006), and mo-
lecular diagnosis of predator-prey relationships (using diagnostic PCR;
Maghsoud et al., 2014) are gaining momentum and are increasingly
used to enhance understanding of meiofaunal biology and ecology.
Additionally, innovative and sophisticated experimental and modelling
approaches have been developed and are being applied to identify the
factors affecting these roles. The contemporary literature provides the
basic knowledge necessary to link meiofauna to the delivery of some
ecosystem services. Of crucial importance in this context is the close
relationship between meiofauna and microbiota. A number of mecha-
nisms that had previously been hypothesised directly and indirectly to
affect microbial growth, activity and community structure have since
been investigated:
- Meiofauna grazing on microbiota: Meiofauna can bring the number
of microbes in sediments down to a sufficiently low level to reduce
the inhibition of microbial growth by substrate shortage, and there-
fore maintain high levels of microbial activity that are in the loga-
rithmic phase of growth. Some microbes (especially bacteria)
ingested by harpacticoid copepods can stay alive, and they can
grow and reproduce rapidly after they are excreted through the
meiofaunal gut because they obtain some hormones and specific nu-
trition whilst in the gut (Cnudde et al., 2013). De Mesel et al. (2004)
observed variable impacts of direct grazing on microbial activity and
community structure in microcosms, depending on nematode
species. An experiment by Hubas et al. (2010) demonstrated that
the presence of nematodes stimulates bacterial and diatom
population growth, thereby enhancing the bacterial and
microphytobenthic production of EPS. In both cases, structuring
effects on microbial assemblages became apparent at low nematode
grazing pressure, implying selective grazing and/or other, indirect
interactions between meiofauna and microbes (see below).
- Meiofaunal secretion of mucus tracks which are utilised by
microbes: Moens et al. (2005) tested whether bacterial communities
growing on nematode mucus differ from extant communities. Their
results suggested that nematode mucus, rich in polysaccharides,
may affect colonisation and succession patterns of bacteria by
providing them with a source of nutrients that are easily
metabolised, thereby stimulating microbial activity and growth.
- Meiofaunal production of exo-enzymes which initiate organic
matter decomposition: Riemann and Helmke's (2002) studies with
oncholaimid nematodes, in contrast, showed no substantial
secretion of nutritious mucus to support microbial development in
oligotrophic agar plates. The authors thus introduced the ‘enzyme
sharing’ concept. It considers the nematode's capacity to secrete an
enzyme which initiates decomposition of sedimentary detritus.
This promotes the growth of bacterial populations and
enhances organic matter decomposition. Nematodes and bacteria
subsequently feed on dissolved and small particulate organic matter
released from this shared use of enzymes, maximising nutrition and
growth of both parties. Hunter et al. (2012a) showed that
extracellular digestion of organic matter (e.g. oxidation of amino
acids) by bacteria may enhance available dissolved food and its
uptake by meiofauna, in addition to direct meiofaunal uptake of
dissolved organic matter without bacterial involvement reported
by Chia and Warwick (1969) previously.
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
- Meiofaunal excretion of metabolic wastes containing nitrogen and
phosphorus: Meiofauna release dissolved matter through excretion
and respiration and particulate matter through production of faecal
pellets, carcasses, moults, and dead eggs. Excretion liberates several
organic carbon, nitrogen and phosphorous compounds and inorgan-
ic nitrogen and phosphorous compounds, with inorganic com-
pounds constituting the larger part. Excess nitrogen is usually
excreted as ammonium and excess phosphate as orthophosphate
(Ferris et al., 1998) which may relieve nutrient limitation for bacte-
ria as well as for primary producers. Faecal pellets play an important
role in the vertical transport of these elements. De Troch et al. (2005)
illustrated the importance of faecal pellets and associated microbiota
as a food source for harpacticoid copepods.
- Microbial symbioses with meiofauna (particularly nematodes):
External and endosymbiotic (intra- and extracellular) bacteria living
in association with nematodes and meiofaunal annelids have been
discovered on numerous occasions (Giere et al., 1995; Ott et al.,
2004; Dubilier et al., 2008; Bayer et al., 2009). Chemoautotrophic
microorganisms can provide a food source by turning chemical ener-
gy (e.g. sulphides) into biomass accessible to meiofaunal organisms
(Musat, 2006).
Despite increasing understanding, there have been limited efforts to
quantify the contributions of meiofauna to ecosystem processes and no
efforts to establish how these contributions translate into the delivery of
ecosystem services. So far, the meiofauna scientific community has
done very little to address the important question of “What happens
to ecosystem processes and the services they provide to society if the
meiofauna is removed from benthic ecosystems?” The following sec-
tions bring together relevant 20th and 21st century research to investi-
gate the contribution meiofauna makes to benthic ecosystem
processes and to conceptualise how trophic and non-trophic activities
of meiofauna and their interaction with other ecosystem components
might affect the delivery of associated ecosystem services.
4. Effects of meiofauna on ecosystem processes and their link to
desired ecosystem services
Benthic organisms interact amongst each other and with the sedi-
ment in which they live. These interactions potentially modify a series
of physical, chemical and biological sediment properties. Physical prop-
erties include sediment texture and cohesion, shear strength, perme-
ability and pore space, and distribution of sediment sizes. Chemical
properties include levels of organic matter, inorganic nutrients, and
oxygen (Glud, 2008; Meadows et al., 2012) and biological properties
include the density and composition of other fauna and microbes.
Many meiofauna species affect various ecosystem processes simulta-
neously by, for example, displacing sediment grains during burrow con-
struction and, at the same time, displacing organic matter and
microorganisms vertically and laterally within the sediment matrix dur-
ing feeding. Meiofauna-mediated effects on marine sediments, which
can be direct or indirect, positive or negative, and at various spatial
and temporal scales, can modulate the delivery of some ecosystem ser-
vices (Fig. 2).
4.1. Sedimentary processes
For simplicity and clarity, the effects of meiofauna on physical and
biochemical sediment properties are treated separately here, because
the driving mechanisms and their consequences for ecosystem process-
es and associated ecosystem services are, although interlinked, quite
distinct.
 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
Fig. 2. Schematic diagram depicting meiofauna-mediated effects on sedimentary, trophic and ecological processes from which desired ecosystem services are derived.
4.1.1. Physical sediment properties
Only recently have the cryptic disturbances caused by meiofauna
gained attention in the scientific literature. Given their often high abun-
dance, meiofauna-induced modifications of the sediment, many of
which are initially at a microscale, can potentially lead to larger-scale ef-
fects worldwide (Murray et al., 2002). In contrast to macrofauna,
meiofauna-induced changes to the sediment texture are characteristi-
cally small in scale and exceedingly subtle in expression but they can
be visually observed in a laboratory environment (cf. Fig. 4 in Bonaglia
et al., 2014). What sets them apart from other forms of biogenic distur-
bance is the tendency to preserve rather than to destroy the sediment's
primary physical structure (Pemberton et al., 2008). These subtle bio-
genic disturbances are of importance to the development of a wider un-
derstanding of the different roles of meiofauna in ancient and modern
sediments.
Pike et al. (2001) were the first to describe a nematode-produced
open burrow network preserved in the geological record from the
Santa Barbara basin (California margin) and the Palmer Deep (west
Antarctic Peninsula). Employing scanning electron microscopy to
image sediment fabric and organic matter morphology in Pliocene-
aged anoxic facies from three geographically widely spaced locations
across the Mediterranean, Löhr and Kennedy (2015) showed that
meiofauna reworked the sediment extensively under oxygen-depleted
conditions that excluded macrofauna. Meiofauna clearly pre-dated
macrofaunal burrowing, providing a leading edge of irrigation and
pelletisation in low-oxygen sediments. Comprehensive meiofaunal
reworking of ancient sediments occurred under a range of environmen-
tal conditions, consistent with studies of modern sediments.
4.1.1.1. Meiofauna-mediated effects on sediment stability. Sediment stabil-
ity depends on the interaction between physical processes, sediment
properties and biological processes, particularly the balance between
stabilising and destabilising effects of biota. Investigations of biotic
factors affecting sediment stability comprise laboratory and in situ
studies that attempt to reflect the complexity of the interactions
between biology, sediment and hydrodynamics. Whilst the effects of
microphytobenthos (Decho, 2000; Malarkey et al., 2015) and a number
of key macrofauna species (Widdows and Brinsley, 2002) on sediment
stability are widely acknowledged, empirical evidence of meiofauna-
mediated effects is much rarer.
Many meiofauna species exert a potentially stabilising effect directly
via the secretion of EPS during the construction of mucus-lined burrows
whereas activities such as bioturbation and grazing on EPS can poten-
tially destabilise sediments. Two recent short-term field and laboratory
experiments, investigating the net effect of meiofauna on sediment sta-
bility, illustrate the complexity that is involved in dissecting the various
aspects of stabilising and destabilising effects from each other, and then
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
5
putting them together again. A destabilising effect of meiofauna,
resulting from bioturbation and grazing on EPS-producing bacteria
was reported in the field (De Deckere et al., 2001). Conversely, results
obtained in the laboratory suggested that nematode grazing on EPS-
producing bacteria stimulated microbial growth and thus the produc-
tion of EPS by bacteria, leading to sediment stabilisation (Hubas et al.,
2010). Despite their contradictory outcomes, these two studies empha-
sise that the complexity of benthic assemblages, rather than the pres-
ence of a particular (group of) organism(s), impacts strongly on
sediment stability, both in terms of microbial abundance and biomass,
and EPS content.
In summary, meiofaunal effects on sediment stability are
hypothesised to be exerted via (Fig. 3):
- Bioturbation (e.g. construction of mucus-lined burrows), leading to
alterations of physical sediment properties including texture, grain
size distribution, permeability, cohesion, and pore space. Physical
parameters affect sediment stability in predictable ways, e.g. in-
creased permeability as a result of burrow construction decreases
sediment stability whereas EPS production during burrow construc-
tion agglutinates sediment particles, thereby stabilising the
sediment.
- Grazing on EPS (Moens et al., 2002) reduces sediment agglutination,
thereby reducing its cohesive strength.
- Grazing on EPS-producing microbiota, which can lead to either
stabilising or destabilising net effects on sediments. Under condi-
tions where nutrients are not limited (partly alleviated by
meiofaunal excretion of carbon, nitrogen and phosphorous com-
pounds), growth and activity of EPS-producing microbiota is stimu-
lated. In the short-term or when nutrients are limited, grazing on
EPS-producing microbiota can inhibit EPS production and thus
destabilise sediments.
4.1.2. Biochemical sediment properties
Meiofauna-induced modifications of the physical properties of sedi-
ments have implications for their biogeochemistry (Meysman et al.,
2006). Although little is known about how mobile meiofauna are, or
how much material they remobilise, their often high abundance in ma-
rine sediments suggests that their microbioturbation and mucus-
supported burrows can alter porosity and permeability of the sedi-
ments, and hence affect the efficiency with which nutrient exchanges
take place.
6 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
Fig. 3. Conceptual diagram illustrating meiofauna-mediated effects on sediment stability. EPS = extracellular polymeric substances, C = carbon, N = nitrogen, P = phosphorous. Arrows
are not indicative of effect size. + stabilising effect, − destabilising effect.
4.1.2.1. Meiofauna-mediated effects on nutrient cycling. Marine sediments
are a globally important reservoir of nutrients. Understanding the fac-
tors controlling the rates and pathways of nutrient cycling is of impor-
tance, because mineralisation and nutrient recycling are essential for
sustaining primary and secondary production in marine ecosystems.
Leduc et al. (2016) reported that equal meiofauna and macrofauna
contributions accounted for a total of approximately 12% of sediment
community oxygen consumption on New Zealand's continental margin.
Seasonal sampling at the Belgian Continental Shelf revealed that nema-
tode respiration is particularly important in spring, shortly after the
deposition of phytodetritus on the sea floor when macrobenthic densi-
ties and biomass are low (Franco et al., 2010). Because respiration rates
are inversely related to body size, meiofauna thus make a dispropor-
tionate contribution to organic matter mineralisation at the seabed.
These estimates give some insights into the direct contribution of differ-
ent size groups to benthic metabolism, but do not reflect indirect contri-
butions (e.g. bioturbation and feeding) which have been investigated in
coastal ecosystems.
However, recent modelling work suggested that meiofaunal carbon
turn-over calculations based on laboratory respiration rates may be
severely overestimated owing to the fact that sediment oxygen concen-
trations in field sediments are generally far from saturated, in contrast
to oxygen saturated laboratory conditions (Braeckman et al., 2013).
Experimental studies with shallow water meiofauna estimated their
direct importance to organic matter mineralisation to be limited (De
Mesel et al., 2006; Urban-Malinga and Moens, 2006; Lillebø et al.,
2007; Nascimento et al., 2012) and their direct grazing rates on settled
organic matter to be low (Nascimento et al., 2008). Direct
mineralisation by meiofauna tends to be small compared to that of the
microbial community. Increased mineralisation observed in field situa-
tions or experimental treatments containing high meiofauna abun-
dance was therefore not a result of increased direct mineralisation by
meiofauna, but instead a consequence of positive interactions between
meiofauna and the microbial community.
Microcosm experiments, designed to study the quantitative impact
of meiofauna populations of different abundance and diversity on nitro-
gen cycling, suggested that meiofauna activities have a stimulating
effect on nitrifying and denitrifying bacteria (Bonaglia et al., 2014;
Stock et al., 2014). Meiofauna-mediated stimulation of nitrification-
denitrification occurred via excretion of large quantities of nitrogen dur-
ing grazing on bacteria. This changed the carbon:nitrogen ratio in the
interstitial water, leading to increased availability of ammonium for
nitrifying bacteria, and increased availability of nitrate and labile
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
organic compounds which specifically stimulated heterotrophic denitri-
fication. Moreover, meiofaunal bioturbation enhanced the transport of
solutes including oxygen, ammonium and nitrate in surficial sediment
layers, resulting in a microhabitat where the essential substrates for ni-
trifying and denitrifying bacteria were more available. Similar effects of
meiofauna on sediment-water fluxes of oxygen, ammonium and nitrate
were measured in situ by Rysgaard et al. (2000) in soft sediments of
Disko Bay (West Greenland). Here, meiofauna enhanced solute trans-
port by a factor of 1.5 to 3.1 compared to molecular diffusion.
In summary, meiofaunal effects on nutrient cycling are hypothesised
to be exerted via (Fig. 4):
- Bioturbation leading to the redistribution of microbiota to places
rich in nutrients, thereby stimulating the growth and activity of
microbes mediating organic matter mineralisation and nutrient
cycling. The construction of burrows, for example, enhances nutrient
and oxygen fluxes and thus stimulates aerobic degradation of organ-
ic matter. Bioturbation provides the sediment with energetically
favourable electron acceptors such as oxygen, which are vital for
high microbial decomposition rates (Middelburg and Meysman,
2007).
- Grazing on microbiota which mediate organic matter mineralisation
and nutrient cycling. This has two important consequences. Firstly,
the microbial community is kept in the active growth phase, imply-
ing a higher demand of nutrients by the microbes and thus resulting
in a higher decomposition rate of the organic matter. Secondly,
meiofauna generally have a higher carbon:nitrogen ratio than
microbes. Nematode grazers on bacteria in particular tend to excrete
large quantities of nitrogen in their mucus which is again available
for the microbial community or can bind to detritus. The secretions
and excretions of meiofauna provide matrix and inorganic nutrients
which are easily metabolised by microorganisms, thereby stimulat-
ing their activity and growth.
4.1.2.2. Meiofauna-mediated effects on waste breakdown and removal.
Whilst grazing by meiofauna on a large number of microorganisms
involved in nutrient cycling and organic matter mineralisation can
have a stimulatory effect (Fig. 4), a similar grazing pressure may inhibit
or have no effect on ecosystem processes mediated by more specialised
microbiota. Using microcosm incubation and addition of meiofauna,
Näslund et al. (2010) observed a significant decrease in the number of
 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx 7

Fig. 4. Conceptual diagram illustrating meiofauna-mediated effects on nutrient cycling. C = carbon, N = nitrogen, P = phosphorous. Arrows are not indicative of effect size. + stimulating
effect.

In summary, meiofaunal effects on waste breakdown and removal

cultivable bacteria that degrade polycyclic aromatic hydrocarbons
are hypothesised to be exerted via (Fig. 5):
(PAHs) in the presence of high meiofauna abundance. These changes
in microbial community structure were concomitant with decreased
mineralisation of the PAH naphthalene. Similarly, Louati et al. (2013)
found that the presence of meiofauna inhibited PAH-degrading bacteria
due to grazing and/or competition for nutrients. Here, the presence of
meiofauna, incubated in PAH-contaminated microcosms for 30 days,
had no discernible effect on the degradation of three types of PAH (fluo-
ranthene, phenanthrene and pyrene). More systematic studies investi-
gating the role of different types of meiofaunal grazers with varying
levels of density and diversity are required to provide a clearer under-
standing of the nature of the interactions involved and the impact of
grazers on the degradation of pollutants (McGenity et al., 2012).
Bradshaw et al. (2006) experimentally used tracers to examine the
role of bioturbation by benthic infauna in transporting sediment-
associated contaminants in the Baltic Sea. Macrofauna and meiofauna
appeared to have an equally important effect on tracer transport (i.e.
burying surface contaminants and remobilising those that were buried).
At their study site (55 to 60 m water depth), as at many other locations
in the Baltic, physical processes are likely to be more important than bi-
ological processes in the longer-term redistribution of contaminants.
- Bioturbation leading to either burial of contaminants or the repeated
transport of particulate material from deeper sediment layers to the
surface and vice versa. In this way, sediment-adsorbed contaminants
transported upwards remain in contact with the overlying water for
longer periods of time, thus enhancing the diffusive loss of contam-
inants from the sediment to the water. The construction of burrows,
for example, transports nutrients and oxygen into deeper sediment
layers. This significantly increases the effective area of the
sediment-water interface (with resulting effects on diffusion gradi-
ents), enhances aerobic zones in the sediment and stimulates the
aerobic microbial community. Such effect is especially important
for the microbial breakdown of persistent compounds including
PAHs, which degrade either slowly or not at all under anaerobic
conditions.
- Grazing on contaminant-degrading microbiota. The stimulatory ef-
fect of grazing pressure on microbes mediating broad ecosystem

Fig. 5. Conceptual diagram illustrating meiofauna-mediated effects on waste breakdown and removal. C = carbon, N = nitrogen, P = phosphorous, PAH = polycyclic aromatic
hydrocarbon. Arrows are not indicative of effect size. + stimulating effect, − inhibitory effect.

Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
8 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
processes such as nutrient cycling and degradation of organic matter
(Fig. 4) can be revoked or reversed for contaminant-degrading mi-
crobes as a result of grazing and/or nutrient limitation.
- Accumulating contaminants in meiofaunal tissue, thereby removing
them from the sediment. Nematodes, for example, have been shown
to detoxify absorbed or ingested metals by using metal-binding pro-
teins and forming subcellular inclusions. These mechanisms often
act jointly to consolidate and enclose excess metals, which subse-
quently accumulate within nematode tissues (Monserrat et al.,
2003).
4.2. Trophic processes
Benthic organisms feed primarily on autochthonous primary pro-
duction, allochthonous organic matter derived from settling seasonal
plankton blooms and/or detritus derived from degraded macrophytes;
only a small proportion rely on chemosynthetically-derived energy
through a microbial pathway. This energy supply to the benthic com-
munity and the processes that decompose the settled organic matter
are amongst the fundamental factors shaping benthic ecosystems.
How benthic communities process and convert organic matter as it
passes through each trophic link has significant consequences for eco-
system services such as food web stability and for linking benthic sec-
ondary production with higher trophic levels that are eventually
harvestable by humans. A major question, therefore, pertains to the
roles of meiofauna in energy flow through benthic food webs.
4.2.1. Energy flow through food webs
Measuring in situ energy flow in spatially and temporally complex
benthic ecosystems represents a major ecological challenge. Food web
structure, energy and nutrient budgets are difficult to measure, in par-
ticular the trophic pathways via which primary production reaches
higher trophic levels. Novel techniques have been developed and are
being used increasingly to trace carbon and nitrogen sources for ben-
thos from different marine and estuarine habitats and energy flow
through benthic food webs, both in situ and ex situ. Measurements of
natural and enriched isotopic quotients (δ13C and δ15N), for example,
allow the pathways of trophic energy to be traced and quantified, and
fatty acid structures can serve as qualitative markers and quantitative
determinants of dietary composition (Leduc et al., 2009). In addition, la-
belled carbon and nitrogen isotope enrichment in situ has the potential
to identify trophic pathways in natural systems, including those involv-
ing microbiota, micro- and macroalgae, meiofauna, and macrofauna as
members of the food web (e.g. Guilini et al., 2010; Galván et al., 2011).
However, feeding and respiration experiments, performed in the
field and under controlled laboratory conditions, can suffer from meth-
odological shortcomings. For instance, the resolution of natural isotope
measurements in meiofauna often suffers from the fact that only com-
munity level information can be obtained, because large numbers of or-
ganisms are needed to get a reliable quantity of carbon or nitrogen.
Recent efforts in adapting existing analytical methods have allowed
for genus- or even species-level trophic information (Carman and Fry,
2002; Moens et al., 2005; Pape et al., 2011; Braeckman et al., 2015). In
addition, laboratory conditions are often poorly representative of field
conditions and most experiments on meiofauna carbon production
tend to be performed on fast-growing, opportunistic species kept
under optimal conditions. Furthermore, loss of the label due to sample
preservation and exploitation of alternative carbon sources not derived
from the labelled ones all contribute to generally low estimates of
meiofauna metabolic activity and carbon production that are inherently
uncertain (Moens et al., 2013).
Meiofauna consume a wide spectrum of food sources, including
microalgae, protozoans, small metazoans, bacteria and organic detritus.
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
At the species level, meiofauna often have specialised diets (Carman and
Fry, 2002; Moens et al., 2002; Rzeznik-Orignac et al., 2008; Maghsoud
et al., 2014) and changes of feeding strategies have been observed de-
pending on the diel and seasonal availability of food sources
(Buffan-Dubau and Carman, 2000; Riera and Hubas, 2003; Lebreton
et al., 2012). In addition, the trophic structure of meiofauna can vary
vertically in response to the availability of specific food sources in differ-
ent sediment layers (Ingels et al., 2011). Moreover, migration of mobile
meiofauna in response to the deposition of organic material at the sed-
iment surface complicates trophic observations in the field.
Labile organic carbon, as derived from microphytobenthos and set-
tled phytoplankton, constitutes an important carbon source for tidal
flat meiofauna (Moens et al., 2002), whereas meiofaunal carbon de-
mands in deep sea sediments are met by labile (Van Oevelen et al.,
2011a) and refractory detritus (Middelburg et al., 2000; Gontikaki
et al., 2011; Van Oevelen et al., 2006, 2012). In both habitats, meiofauna
have been reported to play a marginal role in carbon cycling with inges-
tion rates b5% of total heterotrophic ingestion. Ingels et al. (2010) found
that deep-sea nematodes in polar regions preferred bacteria over phyto-
plankton as a carbon source. This suggests that the trophic link of
meiofauna to microbiota might provide a pathway through which car-
bon that remains unused by metazoans may re-enter the metazoan
food web, thereby affecting food web dynamics and carbon flows.
Other studies have shown that dissolved substances are not taken up
by the deep-sea nematode community and that isotope transfer from
bacteria to deep-sea nematodes is limited (Guilini et al., 2010).
Whilst stable isotope studies implicate a range of carbon sources of
meiofaunal consumers, little is known about how this production is
transferred to higher trophic levels and in particular whether and, if
so, how meiofauna links primary producers and higher trophic levels.
Theoretically, meiofauna can fulfil a predator's nutritional needs in cal-
ories, carbon:nitrogen ratio, amino acids (proteins) and micronutrients,
and especially highly unsaturated fatty acids. The latter cannot be
biosynthesised by most metazoans, but are essential for functioning of
their cell membranes and membrane-bound enzyme systems (Tocher,
2003). Meiofauna can represent a high quality food source due to
their ability to biosynthesise and accumulate highly unsaturated fatty
acids (Leduc, 2009; Braeckman et al., 2015). The ability to synthesise
the appropriate fatty acids is a desirable trait of harpacticoid copepods
for use in mariculture. Meiofaunal copepods are frequently used in
mariculture to provide high-quality nutrition to juvenile fish that re-
quire life feed. Harpacticoid copepods, fed alone or as a supplement,
have been shown to promote faster growth in cultured fish than other
life feed (Fleeger, 2005).
Theoretically, it would thus be advantageous for a consumer to feed
on a concentrated food source (i.e. meiofauna) rather than a dilute me-
dium of the same energetic value (i.e. detritus). However, experimental
studies produced conflicting evidence in relation to such theoretical
predictions. Leduc and Probert (2009), for example, used laboratory mi-
crocosms to identify the pathways through which detritus is assimilated
by amphipods (i.e. directly or indirectly through the assimilation of mi-
crobiota and/or nematodes). They found no clear evidence for an effect
of nematodes on the incorporation rate of fresh macroalgal detritus by
amphipods, although there was some indication that the type of detri-
tus is important in determining the nature and extent of the relation-
ship between nematodes and macrofaunal detritivores. Danovaro
et al. (2007) compared the effects of epibenthic predation on
meiofaunal assemblages by means of experimental exclusion of poten-
tial predators. Here, N75% of total meiofaunal production was channeled
to higher trophic levels through predation on soft-bottom meiofauna,
with polychaetes and nematodes providing major contributions to ben-
thic energy transfers.
Information on carbon processing within the meiofauna component
of the benthic system (i.e. owing to meiofauna predation and scaveng-
ing on other meiofauna) is limited because of the difficulties in observ-
ing direct predator-prey interactions between meiofauna organisms
 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
and flexibility in meiofaunal feeding modes (e.g. exclusive versus facul-
tative feeding behaviour; Moens et al., 1999). However, recent molecu-
lar advances in determining species-specific diets of turbellarians
suggested potential meiofauna predator competition, and spatial
partitioning of prey species which may play a role in the distribution
of predators (Maghsoud et al., 2014). Both hypotheses, however, re-
main to be tested empirically. More recent modelling efforts based on
biomass and carbon processing data revealed that selective and non-
selective feeding meiofauna can provide up to 80% of the diet of preda-
tory and omnivorous meiofauna (Van Oevelen et al., 2006, 2011b),
whilst there can be a significant total meiofauna contribution to carbon
processing (up to 21% of total respiration; Van Oevelen et al., 2011a).
Meiofauna contributions to total carbon processing are highly habitat-
specific, with b10% of benthic respiration reported for meiofauna in
the Barents Sea (Piepenburg et al., 1995) and b1% of total respiration at-
tributed to the meiofauna/nematode community at the bacteria-
dominated Arctic Hausgarten site (Van Oevelen et al., 2011b). Never-
theless, meiofauna can occur in high numbers in bacterially-
dominated vent and seep systems (e.g. Van Gaever et al., 2006). Whilst
benthic food webs are predominantly based on heterotrophic transfer,
there is evidence that chemoautotrophic export may contribute signifi-
cantly to (meio)benthic diets through bacterivory and even archivory
(Sommer et al., 2007; Thurber et al., 2012; Levin et al., 2016).
Given the methodological and conceptual challenges described
above, the role of meiofauna in food web dynamics remains a subject
of debate. An open question is the extent to which they are either a
self-contained energy sink or, alternatively, facilitate the transfer of pri-
mary food resources up the size spectrum, ultimately to commercially
important food species for humans (Fig. 6): Current literature suggests
that:
- Meiofauna food web interactions, both as a consumer of a range of
carbon sources and as a food source for secondary consumers, define
it as a strong ecological interactor. Its combined effects on phyto-
plankton/microbiota grazing and nutrient cycling (Fig. 4), along
with its role as a prey species for secondary consumers (both
meiofauna and macrofauna), cause meiofauna to occupy a unique
position in benthic food webs.
- Meiofauna-mediated effects on the transfer of primary production to
higher trophic levels are direct when meiofauna feed on microalgae
and indirect when meiofauna feed on secretions of primary pro-
ducers (e.g. EPS), decaying organic matter and/or associated
microbiota.
Fig. 6. Conceptual diagram illustrating the ecological role of meiofauna in food web dynamics. POM = particulate organic matter, DOM = dissolved organic matter. The arrow is not
indicative of effect size. The importance of some meiofauna groups as high-quality food for wild capture and cultured juvenile fish is indicated.
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
9
- Consensus has yet to be reached regarding the contribution of
meiofauna to benthic carbon flow. Whilst some studies infer the im-
portance of meiofauna in view of their often high abundance, fast
turn-over and close links to microbiota (Fig. 4), others suggest that
meiofauna process only a fraction of labile organic matter in marine
sediments.
4.3. Ecological processes
Research over the past five decades has uncovered the largely unan-
ticipated, yet striking, influence that interactions of meiofauna with mi-
crobiota and macrofauna have on benthic ecosystems. Numerous
interactions between meiofauna and microbiota have been identified
through field and experimental studies. It is likely that the most impor-
tant of these are microbiota serving as food sources for meiofauna and
the adaptation of meiofauna organisms (e.g. nematodes) to stimulate
bacterial growth to enhance that food source (see Section 4.2.1 and
Moens et al., 2013). Consequently, the meiofaunal role in linking pro-
karyotic (but also detrital) resources to macrofauna and higher trophic
levels is of notable significance for secondary biomass production. Com-
munication mechanisms between and within microbiota and
meiofauna through release of detectable chemical compounds (e.g.
pheromones or ascarosides, Choe et al., 2012) and quorum sensing sig-
nal molecules (Werner et al., 2014) in chemotaxic processes have re-
cently been highlighted as a critical prokaryote-meiofauna link. Such
links require further detailed investigation as they may change the cur-
rently limited understanding of the importance of intra- and inter-
Kingdom interactions in benthic ecosystems.
Interactions between macrofauna and meiofauna include competi-
tion for resources, macrofauna predation on meiofauna (and vice
versa, e.g. Watzin, 1983), physical disturbance and biogeochemical al-
teration of the benthic environment and organisms' habitable niches
by macrofaunal biogenic structures (Braeckman et al., 2011). Intra-
and interspecific interactions, comprising both negative (competitive)
and positive (facilitative) components (Bruno et al., 2003), have been
shown to affect the spatial distribution of meiofauna in terms of density,
diversity and species composition (Ólafsson, 2003). Benthic species
often simultaneously compete with and facilitate each other which
makes the net effects of species interactions on ecosystem processes
and associated services difficult to measure and predict (Arroyo et al.,
2012). For example, the modification of ancient sediment conditions
by meiofaunal cryptobioturbation facilitated the subsequent range ex-
tension of countless associated species, and bioturbating and
bioirrigating activities of macrobenthic organisms in modern subtidal
soft sediments transport organic matter and oxygen from the surface
10 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
to deeper layers, thereby extending the habitat suitable for meiofauna
(Braeckman et al., 2011). Piot et al. (2014) demonstrated experimental-
ly that the effects of macrofauna on nutrient fluxes depend on the pres-
ence of meiofauna, most likely exerted via the catalytic role meiofauna
play in microbially-mediated organic matter mineralisation and nutri-
ent cycling. This suggests that positive biological interactions such as fa-
cilitation from meiofauna have been, and will be, important for
ecosystem processes in soft sediments. Conversely, experiments de-
signed by Nascimento et al. (2011) and Ingels et al. (2014) showed
that macrofaunal consumers clearly controlled (and in some cases lim-
ited) the access of smaller meiofaunal competitors to food. Advance-
ment beyond purely observing meiofauna-macrofauna interactions,
rather than explaining the causal effects, mechanisms and processes
that underlie these interactions, has been slow despite increased efforts
(e.g. Austen et al., 2003; Ólafsson, 2003; Braeckman et al., 2011;
Bonaglia et al., 2014; Ingels et al., 2014). One of the main issues lies in
the confounding effects of predation and physical disturbance, as well
as competition for food by the macrofauna, in addition to the complex-
ity of species-specific responses and interactions. Bioturbation distur-
bance and predation on meiofauna are not exclusively infaunal.
Disturbance and predation by benthic invertebrates and fish may result
in complex effects on meiofauna communities (Schratzberger and
Warwick, 1999; Fleeger et al., 2006) and the ecosystem processes and
services they contribute to.
Facilitative and competitive interactions amongst benthic organisms
create an intricate web of relationships that, collectively, are
hypothesised to affect a range of ecosystem processes (Fig. 7). For
example:
- Bioturbation (e.g. tube-building and burrow construction) by meio-
and macrofauna modifies physical sediment properties (e.g. perme-
ability, water content, cohesion), alters chemical gradients in pore
water, enhances solute transport, draws food and oxygen into
deeper sediment layers and redistributes microbes. Collectively,
these activities extend colonisable habitat for meiofauna and
Fig. 7. Conceptual diagram illustrating some of the multi-faceted top-down and bottom-up interactions between microbiota, meiofauna and macrofauna. POM = particulate organic
matter, OM = organic matter, MPB = microphytobenthos. Effects of microbiota on meio- and macrofauna are not shown. Arrows are not indicative of effect size and competition for
space is not shown. + facilitative interaction, − competitive interaction.
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
microbes and facilitate microbially- and chemically-mediated oxida-
tion reactions (e.g. nitrification).
- Deposit feeding by meio- and macrofauna controls access to food
sources (especially particulate organic matter) for smaller-sized
competitors and may reduce availability of particulate organic sub-
strates for oxygen-consuming microbes. Conversely, extracellular
digestion of organic matter by bacteria may enhance available dis-
solved food uptake by meiofauna, whilst heterotrophic bacterial car-
bon and nitrogen of labile organic matter in the sediments may
affect meiofaunal food availability, particularly in low-oxygen envi-
ronments (not shown in Fig. 7; Hunter et al., 2012a, 2012b).
- Macrofaunal predation on meiofauna potentially reduces meiofauna
prey populations although in situ studies showed that, resulting
from fast meiofauna turn-over times, such reductions are unlikely
to be drastic. Meiofauna predation on small macrofauna and larvae
can potentially reduce macrofaunal prey populations of less mobile
species and affect settlement success.
- Meiofauna grazing on microbiota can either stimulate or inhibit the
growth and activity of oxygen-consuming microbes with resultant
effects on a range of ecosystem processes and services (Figs. 3 to 5).
- Meiofauna grazing on microphytobenthos may reduce or stimulate
microalgal stocks, thereby affecting oxygen production in the
upper layers of the sediment and sediment stability (Fig. 3).
- Meio- and macrofauna defecate organic matter which microbes use
in oxygen-consuming reactions, and excrete nitrogen which
microphytes use in oxygen-producing reactions. The meio- and
 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
macrofauna-mediated efflux of ammonium from the sediment to
the water column subsidises overlying waters with a readily
utilisable form of inorganic nitrogen. This is of particular importance
to nitrogen-limited marine waters (Lohrer et al., 2004) and especial-
ly coastal waters that stratify seasonally.
4.3.1. Meiofauna diversity
Whilst the provision of some ecosystem services may be maximised
through the abundance of functionally important species, wider system
resilience and ecosystem service provision often relies on species diver-
sity (Díaz et al., 2006; Palumbi et al., 2009; Harrison et al., 2014). For ex-
ample, in the deep sea (Danovaro et al., 2008) and in tropical sediments
(Pusceddu et al., 2014), higher nematode diversity has been shown to
support higher rates of some ecosystem processes and an increased ef-
ficiency with which these processes are performed. This suggests that
mutually positive functional interactions may exist that are enhanced
at greater levels of species diversity. High diversity amongst meiofauna
species within functional groups may increase the probability that one
or more species will be adapted to exploit changing availabilities of re-
sources. There may be species that can be lost from some ecosystems
without substantial alteration of ecosystem processes, as two species
can show similarities in the way they feed, reproduce and move within
the sediment. However, they probably do not carry out these activities
in exactly the same way, and the functional significance of these differ-
ences is likely to depend on the species and ecosystem in question, as
well as the specific niches the species occupy (Schratzberger et al.,
2007). Different ecosystem processes are often maximised by different
(groups of) species and consequently, diverse mixtures provide the spe-
cies or combinations necessary to maximise multiple processes
(Lefcheck et al., 2015). Such important processes are not restricted
within size classes; they often cross the boundaries of the niches or en-
vironments occupied by different groups of organisms. The relationship
between meiofauna and macrofauna taxonomic and functional diversi-
ty, for example, has been demonstrated in the Mediterranean deep sea
by Baldrighi and Manini (2015). They concluded that, whilst meiofaunal
and macrofaunal biomass and functional diversity may be decoupled
over similar environmental gradients, the diversity (irrespective of the
type of index used) of both groups (across size classes and phyla, but
also within the nematode phylum) was positively correlated.
Ecosystem processes and associated services may not be maximised
at maximum diversity because of trade-offs between processes (Leduc
et al., 2013; Lefcheck et al., 2015). Ferris and Tuomisto (2015) argue
that if, for example, the desired ecosystem service is the mineralisation
of nutrients in an ecosystem where labile organic matter is supplied reg-
ularly, a relatively low diversity assemblage comprising opportunistic
meiofauna species that rapidly facilitate microbial mineralisation of or-
ganic matter will maintain the ecosystem service. Conversely, in a sys-
tem where more complex organic matter is supplied irregularly or less
frequently, functional successions of diverse meiofauna assemblages in-
cluding enrichment opportunists and species with more conservative
life history characteristics are necessary to maintain the ecosystem
service.
Various experiments and studies in environments where macrofau-
na is rare or absent (e.g. deep sea: Danovaro et al., 2008; Baltic Sea:
Bradshaw et al., 2006; Nascimento et al., 2012) showed that the
meiofauna community can mediate ecosystem processes in sediments
with little or no macrofauna. Nascimento et al. (2012), for example,
found that organic matter mineralisation in sediments with high
meiofauna abundance did not increase further when macrofauna was
present. It follows that the meiofauna community can drive organic
matter mineralisation in sediments with reduced macrofauna abun-
dance. The role of meiofauna is of growing importance since benthic
ecosystems are under increasing anthropogenic pressure. Intermediate
levels of disturbance often affect larger-sized organisms at higher
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
11
trophic levels more strongly than the organisms they consume
(Trexler et al., 2005), especially in benthic ecosystems where macrofau-
nal predators are often larger and have longer generation times, or
lower fecundity, than their meiofaunal prey. Their continuous repro-
duction strategy renders meiofaunal communities less vulnerable to
disturbance than the macrofauna, where a disturbance event during
the recruitment period can destroy the population until the next re-
cruitment. Another advantage of the continuous reproduction strategy
is the constant presence of individuals, facilitating recolonisation of dis-
turbed sediments, whereas recolonisation by macrofauna may proceed
less rapidly (Vanaverbeke et al., 2002). Therefore, activities of
meiofaunal assemblages can increase the resilience of benthic ecosys-
tem processes, such as nutrient regeneration and energy transfer to
higher trophic levels, essential for the delivery of associated ecosystem
services.
5. Meiobenthologists in action - opportunities for future research
Meiofauna play important roles in benthic ecosystems and the con-
ceptual diagrams in Figs. 3 to 7 provide some pointers at how these roles
may affect the delivery of important services benthic ecosystems deliver
to society. Well-designed and targeted hypothesis-driven research will
need to determine how consistent and widespread these roles are. Im-
portant aims of future studies should be to better understand (i.e.
how?) and quantify (i.e. how much?) the direct and indirect contribu-
tions of meiofauna to ecosystem processes. Critical areas for future
meiofauna research include:
- Fundamental studies of the autecology of meiofauna. Population dy-
namics, growth, metabolism, production etc. of some species
(groups) in certain habitats will most certainly have wider implica-
tions on ecosystem processes and in particular on the flow of energy
through benthic food webs (see below).
- Quantification of the contribution meiobenthos makes to the flow of
organic matter to higher trophic levels and hence the productivity of
benthic ecosystems. There is a need to better understand how these
contributions differ across habitats and how they change under var-
ious natural and anthropogenic disturbance regimes.
- Investigations of facilitative and competitive interactions amongst
benthic organisms across habitats and environmental gradients.
Building on past studies is necessary to assess how interactions af-
fect the density, diversity, composition, succession and productivity
of those organisms that mediate important ecosystem processes.
Outcomes from future experimental and modelling studies (see
below) are needed to better understand how species interactions
will evolve under anthropogenic stress.
- Integration of the empirical and conceptual roles of meiofauna in
benthic ecosystems (synthesised in this review) into models to pro-
vide more meaningful and robust predictions of future states of ben-
thic ecosystems and marine ecosystems more widely.
Funders have been placing increased emphasis on the potential
impact of the research that they fund and scientists are expected to
have a clear understanding of how their research will impact not
only on the scientific community, but also on society more broadly
(Lok, 2010). Future states of marine ecosystems will thus need to
be considered in the context of a coupled social-ecological system,
with the socio-economic system influencing the ecological system,
and vice versa. Complex positive and negative interactions amongst
benthic organisms create an intricate web of relationships that,
12 M. Schratzberger, J. Ingels / Journal of Experimental Marine Biology and Ecology xxx (2017) xxx–xxx
collectively, affect a range of ecosystem processes and associated
services. Environmental changes that affect any one benthic compo-
nent will most likely affect others as well. Managers seeking to sus-
tain and enhance ecosystem services afforded by benthic
ecosystems have the option to either conserve existing species and
habitat delivering these services and/or restore elements which
have been lost or damaged (Koch et al., 2009). Each option involves
interactions amongst the various effects organisms (including
humans) have on benthic ecosystems. In some cases, desired effects
may be mutually exclusive (e.g. protection of sensitive benthic hab-
itat may preclude commercial trawling and vice versa), whilst in
others interactions are less severe. It will be problematic, and in
some cases impossible, for managers to optimise all desired effects
simultaneously, making ecosystem-wide decisions difficult to
achieve. The effective application of relevant research findings from
hypothesis-driven research to societal needs thus presents the next
grand challenge for meiobenthologists. This article is a first attempt
to address this challenge.
5.1. Spreading knowledge of meiofauna
Whilst multiple sources of knowledge inform the management of
the marine environment (Schratzberger, 2012), the importance of
incorporating knowledge generated through research into
decision-making processes is widely recognised. However, cultural
differences between producers (i.e. scientists) and end-users of sci-
entific knowledge (i.e. policy-makers and ultimately the public)
often hamper the effective knowledge exchange amongst these
two groups (Cvitanovic et al., 2015). Scientists construct theories,
test hypotheses and refine conceptual models, based on rigorous
methodological approaches to withstand the highest degrees of sci-
entific scrutiny and criticism. Conversely, decision-makers often
manage a process of negotiation and compromise amongst the com-
peting interests of diverse stakeholders so that their decisions can
withstand public scrutiny. The future success of meiobenthology
will depend not only on advancing scientific understanding but
also on disseminating findings from problem-focused fundamental
and applied research to a diverse audience including scientists
from a range of disciplines, environmental managers, policy-
makers and the public. One may argue that publishing in peer-
reviewed journals adequately brings scientific knowledge into the
public domain, and thus is the end of the scientist's responsibility.
However, scientists have an ethical responsibility to make a more
concerted effort to better engage with, and communicate to, the
end-users of scientific findings. Collaborating with scientific peers
across disciplines will help to provide high-quality scientific infor-
mation and developing partnerships with the end-users of scientific
information will undoubtedly aid relevance and application of scien-
tific findings to real-world problems (Schratzberger, 2012). The lack
of attention a group as dominant in sediments as meiofauna has re-
ceived from the wider scientific community and decision-makers is
no longer justified on methodological nor ecological grounds.
Acknowledgements
This article is based on a keynote presented at the 16th International
Meiofauna Conference in Heraklion, Crete, 3 to 9 July 2016. Participation
at this conference (MS) was jointly funded by the Hellenic Centre for
Marine Research and the Centre for Environment, Fisheries and Aqua-
culture Science. JI was supported by a Plymouth Marine Laboratory
Post-doctoral Research Fellowship in collaboration with University of
Exeter and a Marie Curie Intra-European Fellowship within the 7th
European Commission Framework Programme (Grant Agreement
FP7-PEOPLE-2011-IEF no. 00879). Paul Somerfield provided valuable
comments on the manuscript prior to submission. [SW]
Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
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Please cite this article as: Schratzberger, M., Ingels, J., Meiofauna matters: The roles of meiofauna in benthic ecosystems, J. Exp. Mar. Biol. Ecol.
(2017), http://dx.doi.org/10.1016/j.jembe.2017.01.007
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