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MINISTRY OF AGRICULTURE, FISHERIES AND FOOD
Date project completed:
Research and Development
Final Project Report
(Not to be used for LINK projects)

Section 1 : Identification sheet
1.
(a)
MAFF Project Code
AE1113
(b)
Project Title
THE DEVELOPMENT AND MEASUREMENT OF
BIODIVERSITY INDICES FOR THE MARINE ENVIRONMENT
(c)
MAFF Project Officer
Paul Leonard
(d)
Name and address
of contractor
CCMS Plymouth Marine Laboratory
Prospect Place
Plymouth, PL1 3DH
(e)
Contractor’s Project Officer
Richard M. Warwick
(f)
Project start date
01/10/1995
(g)
Final year costs:
(h)
Total project costs / total staff input:
approved expenditure
£38,100
actual expenditure
£38,100
approved
Project endproject
date expenditure
£297,500
actual project expenditure
£297,500
*approved
Project end staff
date input
10.4
*actual staff input
10.4
25/01/2000
(i)
Date report sent to MAFF
(j)
Is there any Intellectual Property arising from this project ?
*staff years of direct science effort
CSG 13 (1/97)
Project endPostcode
date
31/12/1999
1
NO
Section 2 : Scientific objectives / Milestones
2.
Please list the scientific objectives as set out in CSG 7 (ROAME B). If necessary these can be expressed
in an abbreviated form. Indicate where amendments have been agreed with the MAFF Project Officer,
giving the date of amendment.
1. To develop statistical models appropriate to the definition, sampling and understanding of biodiversity
of coastal marine organisms. This will be a generic study in the sense that all groups of marine organisms
will be covered (benthos, pelagos, animals, plants).
2. To elucidate by means of field observations (both from the literature and original), and by
manipulative experiments, the relationships between biodiversity, productivity and disturbance. The field
observations will be generic (see above), but for logistic reasons the experimental component must be
confined to benthic invertebrates (macrobenthos and meiobenthos).
3. To determine the consequences of changes in biodiversity for biologically mediated ecosystem
processes (specifically in this proposal, the mineralisation of particulate organic matter by the meiofaunal
decomposer food chain: amendment to the original proposal agreed on 2 February 1999).
3.
List the primary milestones for the final year.
It is the responsibility of the contractor to check fully that ALL primary milestones have
been met and to provide a detailed explanation if this has not proved possible
Milestones
Target
date
Number
01/05
Title
Code and run the sampling strategy simulations.
Draw conclusions on efficient sampling for
biodiversity indices oriented in specific ways.
01/06
Milestones met?
01/03/1999
in full
YES
on time
YES
Further development of novel taxonomic and
functional biodiversity indices.
01/09/1999
YES
YES
01/07
Produce prototype software product
01/09/1999
YES
YES
02/06
Further field evaluation of productivity/disturbance
effects on biodiversity.
01/09/1999
YES
YES
03/02
Complete experiments on mineralisation of
particulate organic matter by nematode decomposers.
01/09/1999
YES
YES
If any milestones have not been met in the final year,
an explanation should be included in Section 5.
Section 3 : Declaration
4.
I declare that the information I have given in this report is correct to the best of my knowledge and belief. I
understand that the information contained in this form may be held on a computer system.
Signature
Name
Date
Richard M Warwick
Position in Organistation
CSG 13 (1/97)
Research Scientist
2
25/01/2000
Section 4 : Executive summary
This was a large project, resulting in 29 publications in refereed scientific journals that were directly funded by
this contract, and the production of a prototype software package for biodiversity analysis. The programme had
three main objectives:
Objective 1. To develop statistical models appropriate to the definition, sampling and understanding of
biodiversity of coastal marine organisms. This was a generic study in the sense that a wide range of groups of
marine organisms was covered .
Three new biodiversity indices have been formulated. The first two, taxonomic distinctness and variation in
taxonomic distinctness, are measures of phylogenetic structure rather than species richness; they have
desirable statistical properties and in some senses are more ecologically relevant than species richness
measures. These indices have been explored in the context of macrobenthos, freeliving nematodes and
groundfish. The third, structural redundancy, is an indicator of community resilience and has been applied to
the macrobenthos off Northumberland and the Bay of Morlaix. Patterns of biodiversity have been studied in
relation to taxonomic levels and to spatial scales, the latter off Plymouth, in Scottish sea-lochs and an Arctic
fjord. A Windows version of the PRIMER sotware package for the statistical analysis of community data has
been developed, and incorporates routines for the new biodiversity indices.
Objective 2. To elucidate by means of field observations (both from the literature and original), and by
manipulative experiments, the relationships between biodiversity, productivity and disturbance. The field
observations were generic (see above), but for logistic reasons the experimental component was confined to
benthic invertebrates (macrobenthos and meiobenthos).
Field data taken along gradients of enrichment and disturbance have been used to evaluate the relation of
diversity and community structure with these variables in the Skagerrak and North Sea. Field experiments
using artificial substrate units have followed community development in relation to organic enrichment, both
along a field gradient and using units modified with slow-release NPK fertiliser. Manipulative transplant
experiments have been used to study macrofauna/meiofauna interaction. In laboratory mesocosms the effects of
five important macrobenthic bioturbators on the biodiversity of the associated macrobenthos and meiobenthos
have been studied, and the effects of interactions beween organic enrichment and physical disturbance
investigated. In laboratory microcosms, the effects of physical disturbance, organic enrichment and biological
disturbance on meiobenthic biodiversity and community structure have been compared in sand and mud
sediments. Three striking conclusions are: the practical demonstrations of Huston's intermediate disturbance
hypothesis (diversity increases for intermediate levels of disturbance); the greater impact on community
structure of a single large enrichment event, in comparison with the same degree of enrichment administered in
smaller doses, and the mitigating effects of moderate physical disturbance on enrichment impacts.
Objective 3. To determine the consequences of changes in biodiversity for biologically mediated ecosystem
processes (specifically in this proposal, the mineralisation of particulate organic matter by the meiofaunal
decomposer food chain).
In collaboration with colleagues at the University of Ghent, we have studied the effects of a guild of four
species of bactivorous nematodes, in various combinations, on community respiration, bacterial numbers and
proteolytic activity. In these experiments, no relationship was found between species diversity per se and any
of the measured ecosystem functions. The failure to demonstrate a relationship should not be taken as
evidence that such relationships do not exist. This is an important emerging area of research, and our work
has led directly to a proposal for a NERC thematic on this topic.
These findings are of direct relevance to MAFF policy issues. For example, the new biodiversity indices will
provide a cost effective means of detecting and monitoring the biological effects of human impacts, and the
effectiveness of remediation projects. The results of the experimental work will provide a scientific basis for
decision-making in such areas as the disposal of organically enriched sediments at sea, where the timing and
location of disposal have been shown to be critical factors with regard to effects on biodiversity.
CSG 13 (1/97)
3
Section 5 : Scientific report
CSG 13 (1/97)
4
The research programme has resulted in 29 publications in refereed scientific journals, and the results are impossible to
report in detail here. Instead, a summary is provided to put each element of the work in the context of the overall
objectives, and a number is given (in parenthesis) which refers to the relevant paper(s), listed at the end, from which
further details can be obtained. A reprint collection of these papers accompanies the report.
Objective 1: Definition, measurement and sampling of biodiversity
We have explored the use of an alternative measure of biodiversity, taxonomic distinctness, which is a measure not of
the number of species present but how closely related they are to each other (5,17). This does not appear to be at all
sensitive to the number of individuals in the sample, unlike standard diversity indices, and means that values may be
comparable across studies with differing and uncontrolled degrees of sampling effort. A randomisation test has also
been devised to address the question of whether an impacted locality has lower average taxonomic spread than
expected from the global species list for that region. Taxonomic distinctness is more closely linked to functional
diversity and appears to decline monotonically in response to environmental degradation whilst being relatively
insensitive to major habitat differences. In its simplest form, it utilises only simple species lists (presence/absence
data). These techniques have been tested for freeliving marine nematodes (5,6,17) and bottom-dwelling fish (10) and
macrobenthos (16).
We have examined the assumptions made about the weighting of step lengths between successive taxonomic levels
(species to genera, genera to families etc.), which when accumulated give the overall path lengths between species, which
are then averaged to calculate taxonomic distinctness (6). Using data on freeliving marine nematodes from 16
localities/habitat types in the UK, we have shown that the relative values of taxonomic distinctness for the 16 sets are
robust to variation in the definition of step length. For example, there is a near perfect linear relationship between values
calculated using a constant increment at each level and a natural alternative in which the step lengths are proportional to
the number of species per genus, genera per family, family per suborder etc.
The degree to which certain taxa are over- or under-represented in samples from a particular locality, in relation to the
regional species pool, is another biodiversity attribute of ecological relevance. We have devised a new metric, variation in
taxonomic distinctness, which is essentially a measure of the evenness of the distribution of species and higher taxa across
the taxonomic tree (25). It has similarly desirable properties to the taxonomic distinctness measure (e.g. near invariance
to sample size), and is also amenable to significance testing. The combination with average taxonomic distinctness gives a
powerful bivariate descriptor of biodiversity, with the two components measuring approximately independent diversity
properties in the practical cases we have considered.
In previous studies a continuous decrease in taxonomic distinctness was found in marine macrofaunal assemblages
along a gradient of increasing environmental contamination, in a situation where species diversity remained constant, in
the vicinity of one oilfield in the Norwegian sector of the North Sea. These indices have been tested using species
abundance data from three other oilfields in the Norwegian sector, each sampled on three different occasions (16). No
consistent pattern of decreasing taxonomic distinctness with increasing environmental contamination was evident
however.
Very low values of taxonomic distinctness have been found in certain taxa in grossly polluted environments. We have
used multivariate analyses of morphometric characters to resolve the status of sibling species within the nematode genus
Pontonema, which frequently dominates the macrofaunal biomass in organically enriched locations (23).
We have developed a method of quantifying the extent of structural and functional redundancy by extracting a series of
subsets of species, the multivariate response pattern of each of which closely matches that for the whole community (4).
Structural redundancy is then reflected in the number of such subsets, which we term ‘response units’, that can be
extracted without replacement. We have applied this technique to the effects of the Amoco-Cadiz oil-spill on marine
macrobenthos in the Bay of Morlaix, France, and to the natural interannual variability of macrobenthos at two stations
off the coast of Northumberland, England. The level of structural redundancy may be an indirect measure of the
resilience or compensation potential within an assemblage, a key feature in understanding the function of biodiversity.
The idea that abundances of higher taxa, or particular groups of organisms, may be used as surrogates for the total fauna
in studies of marine macrofauna in soft sediments has been explored (21). Species abundances from a range of studies
from areas of the North Sea with differing pollution histories, together with matching environmental data, formed the
basis of the study. Univariate and multivariate analyses of these data were compared and contrasted with similar
analyses based on abundances of higher taxa such as genera, families, orders, classes and phyla, and also on
taxonomically coherent subsets of the total fauna, including polychaete species and families, molluscs, crustacea and
echinoderms, each of which might be considered to have potential as an indicator group. The general conclusion was
that, in surveys of soft sediment macrofauna in the North Sea, little information about inter-sample relationships is lost
in disturbed areas using data based on family, polychaete species, or polychaete family abundances, rather than species
abundances. In more pristine areas correlations between calculated diversity indices and similarity in faunal patterns
between species and family abundances are still very high, but less so for polychaete species or polychaete family
abundances. This suggests that identification to the level of family may be satisfactory in many routine monitoring
surveys. Identification of only the polychaetes, either to the level of species or family, may also be a possible
alternative if there are clear disturbance gradients in the survey area.
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The spatial scale of local patterns in the fauna of two contrasting shallow water sediment assemblages has been
investigated using hierarchical sampling (7). Replicate samples were taken at separations of 50cm, 5m, 50m and 500m.
No significant differences between samples could be detected on any of these scales in a fine sand assemblage.
However, in a heavily bioturbated sandy mud, samples separated by more than 50m were significantly different from
each other. This separation was largely a result of changes in the patterns of dominance among the most abundant
species, particularly annelids. In a complementary set of analyses, animals were regrouped either by higher taxa or by
body size. The numerically important annelids and crustaceans showed a pattern of spatial similarity close to the full
data set, but that shown by molluscs was clearly distinct. Large bodied animals were also independent of the main
pattern while smaller species conformed to it. In the case of the latter, separation of sites at the 50m scale could be
related to patterns of species richness as well as dominace.
Data from samples arranged at different spatial scales have also been gathered from the literature and from their original
authors. Using macrofaunal abundance data from van Veen grab samples collected 20 m to 100 m apart in known
spatial arrangements from Scottish sea-lochs, the relationships between patterns in macrobenthic species composition
and distances between samples have been explored using matrix correlations in a non-parametric framework (22).
Changes in community structure were found to be positively correlated with distance at all sites in Loch Etive, on both
current swept muddy sands and soft deep muds. Simple spatial structure were also detectable at a muddy-sand site in L.
Creran, but not on soft mud, or at the soft mud site in the Firth of Lorne. Relationships between similarity and distance
were neither simple nor consistent. Analyses of the spatial structure at these 7 sea-loch sites suggested that, by ensuring
that samples are at least 40 m apart, an investigator is unlikely to underestimate variability or otherwise invalidate
statistical analyses based on the use of the samples as replicates. Spacing samples up to 100 m apart may increase
variability estimates, further reducing the chance of concluding that a difference exists when one does not.
Spatial patterns of diversity and community structure have also been examined along two intersecting transects in a
glacial bay in Kongsfjord, Svalbard (26). This physically disturbed area lacks species with typical opportunistic life
history characteristics. We found a clear faunal response to the gradient of physical disturbance away from the glacial
front, and in the absence of species which produce planktonic larvae this suggests that at high latitudes the ability to
resist disturbance, rather than the ability to exploit newly vacant resources, determines the sequence of colonisation.
A comparison has also been made of some methods commonly used for the collection of sublittoral sediments and their
associated fauna (15). The four methods were: 1. Direct collection by divers. 2. Collection using a Craib corer. 3.
Subsampling from an USNEL pattern box corer. 4. Subsampling from a van Veen grab. Nematodes in the samples
were identified and the resulting data analysed using a range of techniques. Univariate measures of community
structure, such as diversity indices, did not reveal any significant difference between sampling methods, neither was any
significant difference detected in diversity profiles (k-dominance curves). However, multivariate analyses did reveal
significant differences in community structure between samples retrieved by different methods. The detected
differences, although significant, were small, and did not suggest a strong, or ecologically meaningful, explanation. A
modified index of multivariate dispersion was devised, and this was used to examine differences between sampling
methods in intra-sample variability. This showed that differences in variability contribute to, but do not fully explain,
the observed differences.
The analyses of the wide range of assembled literature and de novo data sets, described above, was both facilitated by the
synthesis of existing methodology, particularly as it is applied to mesocosm and microcosm experiments (3), and by much
new methodological development, especially in relation to spatial and temporal field studies (4, 5, 6, 15, 22, 25). In
particular, the theoretical and practical studies on biodiversity measurement showed the almost insurmountable problems
of comparing indices based on species richness for historic data sets, collected at different times by different workers and
thus employing non-standardised levels of sampling effort. Instead, as described earlier, we have devised and applied
indices (5, 6, 10, 16, 17, 25), based on properties of the taxonomic structure in an assemblage which are insensitive to
sample size, as well as being highly relevant descriptors of biological diversity. The referral of pairs of values of average
and variation in distinctness to a bivariate confidence region, representing biodiversity ‘expectation’ under non-impacted
conditions, is based on running a simulation model whose inputs consists of the taxonomic structure of a more-or-less
comprehensive, wide-area species list. This allows the user to identify how large a sample size is likely to be required to
detect a specified (%) change in the indices, reflecting the direction and magnitude of change seen in other impact studies.
Both these univariate and new multivariate techniques arising from this research were incorporated into a totally rewritten
version of the PRIMER software package (Plymouth Routines In Multivariate Ecological Research). This is the first
Windows version of PRIMER, which at the time of this report is in prototype form, as specified by the contract (in fact
much of it is more advanced and already in an alpha-test version). It is planned to move to the beta-test stage rather
quickly (by April 2000), and by the summer of 2000 a finalised product will be available to be distributed to MAFF and
its associated laboratories. Because this product builds on the DOS v4 of PRIMER, which is used by several thousand
marine (and terrestrial) scientists in 65 countries, it will have worldwide exposure (and due acknowledgement to MAFF
for their part funding of this product will be given on the PRIMER v5 ‘splash’ screen, displayed when the program is
loaded – see attached papers).
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Objective 2: Relationships between biodiversity, productivity and disturbance.
Field sampling studies
We have examined field data taken along gradients of enrichment and disturbance, to evaluate the relation of diversity
and community structure with these variables.
We have used multivariate analyses of macrofauna and environmental data from 20 separate investigations in the
Skagerrak and North Sea to examine faunal patterns at different taxonomic levels (9). Data are analysed at the level of
species, genus, family, order, class and phylum. The degree of transformation is as important in determining the
outcome of subsequent analyses as the taxonomic level to which individuals are identified. Correlations between the
underlying similarity matrices at the species level and higher taxonomic levels show highest values in polluted areas,
lower values in less disturbed areas and lowest values in pristine areas, indicating that the faunal patterns for the various
taxonomic levels become more similar as the degree of disturbance increases. For all 20 investigations highest
correlations between faunal patterns (i.e. the underlying similarity matrices) and environmental variables were mainly
found at the levels of species, genus and family, and often there was a distinct drop in correlation value between family
and order. In most cases, independent of the level of pollution, there is only a minor reduction in correlation between
species and family, suggesting that identification to the level of family may be satisfactory in many routine monitoring
surveys.
A similar study was undertaken on data from a survey of 27 stations in the vicinity of the Valhall oilfield in the
Norwegian sector of the North Sea (8). As the taxonomic level increased, the effects of transformations became
stronger, so although both taxonomic resolution and transformation affected the results of analyses, the effects of each
were different and, to a large extent, unrelated. The highest correlations between matrices derived from measured
environmental variables and biotic matrices were between environmental variables related to drilling activity and mildly
transformed family abundances, suggesting that analyses of higher taxonomic levels are more likely to reflect a
contamination gradient than are analyses based on species abundances.
Field experiments
Field experiment was carried out to examine the effects of productivity on the benthic diversity. Artificial substratum
units were constructed from spherical pan scourers and secured to the seabed for 10 weeks to investigate effects of a
small domestic sewage outfall on cryptofaunal communities at Downderry, Cornwall. Similar artificial substrata were
modified with of slow-release NPK fertilizer in an experiment to investigate the effects of a nutrient/productivity
gradient on cryptofaunal communities. These were deployed at Cawsand, Cornwall for 20 weeks. It was hoped to
subsequently obtain comparable results from the two experiments. Both experiments successfully collected diverse and
abundant cryptofaunal communities, comparable to their natural counterparts. Univariate measures revealed a clear
gradient of abundance, number of taxa and species richness in response to distance from the sewage outfall. Species
diversity (H') and evenness remained fairly constant throughout. MDS demonstrated a loose cluster most effected by the
outfall, and a tightly formed distant unimpacted group. Variability of all measures increased at impacted sites, although
the influence of this outfall was not extensive. Cryptofauna appear to respond in a similar manner to a generalised
model of community structure in relation to an organic enrichment gradient. The second experiment failed to elicit any
significant changes in community structure in relation to a gradient of increasing nutrients alone. Results suggest that
three-dimensional artificial substrata represent a potentially useful quantitative technique for ecological impact studies
on hard substratum communities comparable to those currently employed on sediment benthos.
A manipulative experiment has also been carried out to examine the effects of the large pinnid bivalve Atrina zelandica
on benthic communities (24). Dead shell treatments were included in the experiments to discriminate between the
hydrodynamic effects of the physical presence of Atrina, and the effects of their biological activity (e.g. biodeposition).
No treatments had significant effects on meiofaunal biodiversity or community structure, in contrast to the clear
differences evident between established Atrina patches and bare sediment. Explanations for this are being pursued.
Laboratory experiments in mesocosms and microcosms
In order to examine how different types and intensities of disturbance affect biodiversity of benthic assemblages
experiments have been undertaken in the mesocosm facilities of the Norwegian Institute for Water Research (NIVA) at
Solbergstrand, Norway (1, 2, 18, 19, 27, 28, 29). Experiments were conducted to compare the effects of sediment
disturbance by different bioturbating, macrofaunal organisms on the diversity and structure of the associated infaunal
community. The four species investigated were the bivalves Nuculoma tenuis (Montagu, 1808) and Abra alba (Wood,
1802), the heart urchin Brissopsis lyrifera (Forbes, 1841) and the burrowing decapod Calocaris macandreae (Bell,
1846). These organisms were chosen to allow assessment of the effects of contrasting feeding activities and body sizes
of the bioturbating species on the diversity of the macrobenthic communities. Bioturbation by the sub-surface deposit
feeders Nuculoma and Brissopsis was shown to promote higher levels of  and  diversity in treatments exposed to
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intermediate levels of disturbance. Whilst no such “intermediate response” was demonstrated for Abra or Calocaris, it
was evident that changes in the associated fauna were influenced by the feeding type of the bioturbating organism
responsible. It was also shown that different elements of the associated community responded differently to biotic
disturbance. The results indicate that the variability in the density and distribution of such bioturbators are important
factors in the structuring of infaunal communities, and in setting and maintaining levels of diversity in apparently
homogeneous areas.
Effects on macrofaunal biodiversity of the interaction between organic enrichment and physical disturbance have been
investigated in an experimental test of Huston’s “Dynamic Equilibrium Theory” (28). Using 7 different levels of
enrichment and 7 frequencies of physical disturbance (49 treatment combinations) strong interactions were
demonstrated, but the relationship was not smple. With low disturbance the diversity in high organic enrichment
treatments was lower than in low enrichment treatments. With more frequent disturbance, diversity in the high organic
treatments became greater., but in low enrichment treatments the greater the disturbance the lower the diversity. At the
highest disturbance level, diversity was the same at all 7 enrichment levels.
Microcosm experiments have also been carried out to evaluate the effects of:
1. Continuous and spasmodic physical disturbance of differing frequency on the structure of meiofaunal communities
of intertidal mud and sand (11).
2. The response of meiofaunal communities to three different quantities of organic matter (high/medium/low). Given
once at the beginning of the experiment the response differs from that for the same quantities given in several
smaller doses during the experimental period. Both univariate and multivariate analysis of the data showed that the
same amount of organic matter administered in many small doses had a milder effect on community structure than
when administered in fewer but larger doses (12).
3. The effects of biological disturbance, by crabs, on both sediment types (13).
We have shown that assemblages exhibit various characteristic changes when exposed to different types of disturbances
(15). For both sand and mud assemblages, biological disturbance caused the least severe changes in assemblage
structure. For the sand assemblages, most extreme changes were the result of organic enrichment, while mud nematodes
showed the most intense response to treatments of physical disturbance. Assemblages are most affected by the kinds of
disturbance that they do not normally experience naturally.
The response of an estuarine macrobenthic community to different intensities of physical disturbance was also
examined using comparable field and mesocosm experiments (20). More statistically significant differences were
observed between the different disturbance intensities in the mesocosm experiment than in the field study.
Objective 3: Consequences of biodiversity change
[A rather longer description is given here because the work described below has not yet reached publishable stage and is
therefore not described in the attached papers]
In this part of the study we aimed to address the question of the extent to which the number of functionally analogous
species can be reduced within a community before the that function begins to become impaired in terms of rate or
efficiency, and the extent to which the number of functional groups may be reduced before the whole ecosystem starts
to malfunction. This is an area of biodiversity research that is currently receiving a great deal of interest, although that
interest and the importance of the underlying questions are not matched by the number of publications appearing in the
scientific literature. This is a reflection of the difficulty of constructing meaningful experiments and seeing them to a
sensible conclusion. The difficulties arise in several general areas. The first is defining a so-called ‘ecosystem
function’ that may be readily quantified and attributed unambiguously to a particular well-defined group of species. If
such a function, with its associated functional group, may be defined and measured the next area of difficulty involves
problems with confounding in experimental design. If the contribution of an organism to ecosystem function depends
on the organism’s size or stage in its lifecycle, or is density dependent, it makes it extremely difficult to tease apart the
effects of pure ‘diversity’ and other factors. The third general area of difficulty involves the power of experiments that
can be constructed. The difficulties of constructing and maintaining artificial assembalges of live healthy organisms,
and the subtlety of the effects being measured in comparison to the general variability in such systems, makes it
difficult to demonstrate unambiguously that the effects are significant as it is almost impossible to introduce enough
replication into experiments in order so to do. These are problems common to all research in this area of biodiversity,
whether it involves terrestrial vegetation, freshwater protozoa, or in the context of the current project, marine
invertebrates. The difficulty of this area of research, and its fundamental importance, are reflected in the fact that those
experiments that do produce sensible results appear in prestigous journals such as Nature, and invoke considerable
debate when they do appear.
Work in this area within this project has reflected the current status of the research in other fields. The first difficulty
was to define an ecosystem function that could be measured, with an associated functional group that could be
manipulated. Initially it was intended to work on the clearance rate of phytoplankton by filter feeding organisms.
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Practical difficulties in constructing the artificial communities and in defining the function unambiguously in the light
of our increasing knowledge of the complex interplay between different filter-feeders, microscale current regimes,
phytoplankton and seston concentration and constitution and other factors lead us ultimately to abandon this function.
Instead we decided to resurrect an area of research - bactivorous nematodes associated with decomposing plant
material in estuarine systems - which had in the past proved to be fruitful in related experiments. Although PML has a
history of success in experimentation in this area it has not received much attention in recent years, and the current
centre of excellence in this field is the University of Ghent in Belgium. It was therefore decided to do this work in
collaboration with workers from that university.
Bacteria are intimately associated with the breakdown of detritus in estuarine ecosystems. It has been shown that
nematodes that eat those bacteria influence the rate at which those bacteria mineralise organic carbon. One group of
those nematodes are considered to be functionally analogous, in that they have very similar buccal structures and
ecologies, and also many of them in the family Monhysteridae are closely related. The aim was to construct an
experiment in which the diversity of bacterivorous nematodes was manipulated, and aspects of bacteria-mediated
ecosystem function was measured.
The first step was to isolate bacterial communities and nematode species that could be used in constructing the
experiment. Bacterial communities were extracted from plant detritus from the Westerschelde estuary in a liquid
nutrient medium made with ultra-filtered estuarine water. Nematodes were isolated from plant detritus spotted on
sloppy agar. Once mixed nematode cultures were established, individual species were isolated in consecutive steps, to
give monospecific cultures of four species – the Monhysterids Diplolaimella dievegatensis, Diplolaimelloides meyli and
Monhystera sp., and the Rhabditid Pellioditis marina. These bacteria and nematode cultures, topped up with
conspecific nematode cultures at the University of Ghent, were used to construct a factorial experiment using thin liquid
films in petri dishes. The treatment levels were: Blank (baterial culture); 1 species; 2 species; 3 species and 4 species,
each treatment replicated 4 times (8 for the 1 species treatment). 204 individual nematodes were used in each of the
nematode treatments – 204 of a single species in the 1 species treatment, 102 of each species in a 2 species treatment,
68 of each species in a 3 species treatment and 51 in a 4 species treatment. Incidentally, it was accepted from the outset
that the variability within the 4 species treatment and the blanks (all replicates had the same initial makeup) would have
to be taken into account in subsequent statistical analyses. As measures of ecosystem function the following
measurements were made at periodic intervals: community repiration (measured using a Stathkelvin polarographic
oxygen electrode setup with a six-cell respirometer and associated computer software); bacterial numbers (in equalvolume aliquots from each plate preserved in formalin); proteolytic activity (measured fluorometrically in aliquots
using a fluorescently labelled casein). The experiment was run for 2 weeks at 20C in the dark. Initial statistical
analyses based on the resulting data did not reveal a relationship between species diversity and any of the measured
ecosytem functions.
The failure to demonstrate a relationship between ecosystem function and species diversity in this experiment should
not be taken as evidence that such relationships do not exist. Given the difficulties outlined above, the experiment as
conducted should be seen as preliminary in nature. It is likely that the experiment suffered from power problems.
Although the presence of nematodes appeared to influence the measured ecosystem functions, the differences between
species and combinations of species were relatively small. In order to detect species-related differences the experiment
would need to be reconducted using levels of replication orders of magnitude greater than those used in the current
experiment. This on its own would represent a significant research project requiring considerable resources. It is
intended to continue this work beyond the end of the current MAFF finded project, and to seek funding to do so
elsewhere.
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File reference: RSC
Full list of papers published on work funded by MAFF contract AE1113, as at Jan 2000
Highlighted in bold are the individuals from PML whose contributions to the described work were directly funded by
contract AE1113
1. Austen, M.C. and Widdicombe, S. (1998). Experimental evidence of effects of the heart urchin Brissopsis
lyrifera on associated subtidal meiobenthic nematode communities. Journal of Experimental Marine
Biology and Ecology, 222, 219-238.
2. Austen, M.C., Widdicombe, S. and Villano-Pitacco, N. (1998). Effects of biological disturbance on
diversity and structure of meiobenthic nematode communities. Marine Ecology Progress Series, 174,
233-246.
3. Clarke, K.R. (1999). Non-metric multivariate analysis in community-level ecotoxicology. Environmental
Toxicology and Chemistry, 18, 118-127.
4. Clarke, K.R. and Warwick, R.M. (1998). Quantifying structural redundancy in ecological communities.
Oecologia, 113, 278-289.
5. Clarke, K.R. and Warwick, R.M. (1998). A taxonomic distinctness index and its statistical properties.
Journal of Applied Ecology, 35, 523-531.
6. Clarke, K.R. and Warwick, R.M. (1999). The taxonomic distinctness measure of biodiversity: weighting
of step lengths between hierarchical levels. Marine Ecology Progress Series, 184, 21-29.
7. Kendall, M.A. and Widdicombe, S. (1999). Small scale patterns in the structure of macrofaunal
assemblages of shallow soft sediments. Journal of Experimental Biology and Ecology, 237, 127-140.
8. Olsgard, F., Somerfield, P.J. and Carr, M.R. (1997). Relationships between taxonomic resolution and
data transformations in analyses of a macrobenthic community along an established pollution gradient.
Marine Ecology Progress Series, 149, 173-181.
9. Oslgard, F., Somerfield, P.J. and Carr, M.R. (1998). Relationships between taxonomic resolution,
macrobenthic community patterns and disturbance. Marine Ecology Progress Series, 172, 25-36.
10. Rogers, S.I., Clarke, K.R. and Reynolds, J.D. (1999). The taxonomic distinctness of coastal bottomdwelling fish communities of the North-east Atlantic. Journal of Animal Ecology, 68, 769-782.
11. Schratzberger, M. and Warwick, R.M. (1998). Effects of physical disturbance on meiofaunal
communities in sand and mud: a microcosm experiment. Marine Biology, 130, 643-650.
12. Schratzberger, M. and Warwick, R.M. (1998). Effects of the intensity and frequency of organic
enrichment on two estuarine nematode assemblages. Marine Ecology Progress Series, 164, 83-94.
13. Schratzberger, M. and Warwick, R.M. (1999). Impact of predation and sediment disturbance by
Carcinus maenas (L.) on free-living nematode community structure. Journal of Experimental Marine
Biology and Ecology, 235, 255-271.
14. Schratzberger, M. and Warwick, R.M. (1999). Differential effects of various types of disturbances on the
structure of nematode assemblages: an experimental approach. Marine Ecology Progress Series, 181,
227-236.
15. Somerfield, P.J. and Clarke, K.R. (1997). A comparison of some methods commonly used for the
collection of sublittoral sediments and their associated fauna. Marine Environmental Research, 43,
145-156.
16. Somerfield, P.J., Oslgard, F. and Carr, M.R. (1997). A further examination of two new taxonomic
distinctness indices. Marine Ecology Progress Series, 154, 303-306.
17. Warwick, R.M. and Clarke, K.R. (1998). Taxonomic distinctness and environmental assessment.
Journal of Applied Ecology, 35, 532-543.
18. Widdicombe, S. and Austen, M.C. (1998). Experimental evidence for the role of Brissopsis lyrifera
(Forbes, 1841) as a critical species in the maintenance of benthic diversity and the modification of
sediment chemistry. Journal of Experimental Biology and Ecology, 228, 241-255.
19. Widdicombe, S. and Austen, M.C. (1999). Mesocosm investigation into the effects of bioturbation on
the diversity and structure of a subtidal macrobenthic community. Marine Ecology Progress Series,
189, 181-193.
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File reference: RSC
Papers in press
20. Cowie, P.R., Widdicombe, S. and Austen, M.C. (2000). Effects of physical disturbance on an estuarine
intertidal community: field and mecocosm results compared. Marine Biology
21. Olsgard, F. and Somerfield, P.J. (2000). Surrogates in marine benthic investigations – which taxonomic
unit to target? Journal of Aquatic Ecosystem Stress and Recovery
22. Somerfield, P.J. and Gage, J.D. (2000). Community structure of the benthos in Scottish sea-lochs. IV.
Multivariate spatial pattern. Marine Biology
23. Warwick, R.M. and Robinson, J. (1999). Sibling species in the marine pollution indicator genus
Pontonema Leidy (Nematoda: Oncholaimidae), with a description of P. mediterranea sp. nov. Journal
of Natural History
Manuscripts submitted or in draft (substantially complete)
24. Austen, M.C., Thrush, S.F. and Cummings, V.J. (in draft). Experimental evidence that meiofaunamacrofauna interactions do not evolve within short time scales (47 days).
25. Clarke, K.R. and Warwick, R.M. (in draft). A further biodiversity index applicable to species lists:
variation in taxonomic distinctness. (To Marine Ecology Progress Series?)
26. Kendall, M.A., Widdicombe, S. and Weslawski, J.M. (in draft). Spatial patterns of the macrobenthic
infauna in areas disturbed by run-off from the Kongsbreen Glacier, Svalbard. (To Marine Ecology
Progress Series?)
27. Widdicombe, S., Austen, M.C., Kendall, M.A., Warwick, R.M. and Jones, M.B. (submitted).
Bioturbation as a mechanism for setting and maintaining levels of diversity in subtidal macrobenthic
communities. Hydrobiologia
28. Widdicombe, S. and Austen, M.C. (in draft). Mesocosm investigation into the effects of physical
disturbance and organic enrichment on the diversity and structure of a subtidal macrobenthic
community. (To Marine Ecology Progress Series?)
29. Widdicombe, S. and Austen, M.C. (in draft). Mesocosm investigation into the effects of bioturbation by
Calcaris macandreae (Crustacea: Thalassinidea) on the diversity and structure of a subtidal
macrobenthic community. (To Journal of the Marine Biological Association of the UK?)
Software
PRIMER (2000). Plymouth Routines in Multivariate Ecological Research, v5.0 alpha for Windows
(prototype version complete, beta-test scheduled for end-March 2000)
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